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Reproductive efficiency of swine as influenced by feeding fructose during lactation or glutathione during early gestation

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Title:
Reproductive efficiency of swine as influenced by feeding fructose during lactation or glutathione during early gestation
Creator:
Campbell, Wendy Jo, 1960-
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[s.n.]
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English
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xii, 354 leaves : ill. ; 28 cm.

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Subjects / Keywords:
Fats ( jstor )
Gilts ( jstor )
Insulin ( jstor )
Lactation ( jstor )
Piglets ( jstor )
Plasmas ( jstor )
Pregnancy ( jstor )
Rats ( jstor )
Sows ( jstor )
Swine ( jstor )
Animal Science thesis Ph. D
Dissertations, Academic -- Animal Science -- UF
Fructose ( lcsh )
Glutathione ( lcsh )
Swine -- Feeding and feeds ( lcsh )
Swine -- Reproduction ( lcsh )
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bibliography ( marcgt )
non-fiction ( marcgt )

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Thesis:
Thesis (Ph. D.)--University of Florida, 1988.
Bibliography:
Bibliography: leaves 280-353.
General Note:
Typescript.
General Note:
Vita.
Statement of Responsibility:
by Wendy Jo Campbell.

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University of Florida
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University of Florida
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Copyright [name of dissertation author]. Permission granted to the University of Florida to digitize, archive and distribute this item for non-profit research and educational purposes. Any reuse of this item in excess of fair use or other copyright exemptions requires permission of the copyright holder.
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19087371 ( OCLC )
AFG4290 ( NOTIS )
AA00004794_00001 ( sobekcm )

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REPRODUCTIVE EFFICIENCY OF SWINE AS INFLUENCED BY
FEEDING FRUCTOSE DURING LACTATION OR
GLUTATHIONE DURING EARLY GESTATION
By
WENDY JO CAMPBELL
A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL
OF THE UNIVERSITY OF FLORIDA IN
PARTIAL FULFILLMENT OF THE REQUIREMENTS
FOR THE DEGREE OF DOCTOR OF PHILOSOPHY
UNIVERSITY OF FLORIDA
1988


The author dedicates this dissertation to all of the swine who so
enthusiastically cooperated during this project while receiving such
little recognition.


ACKNOWLEDGEMENTS
The professional guidance, time, and patience of Dr. Fuller W.
Bazer are gratefully acknowledged. The author also extends
appreciation to Dr. W. C. Buhi, Dr. R. M. Shireman, Dr. D. C. Sharp
and Dr. W. W. Thatcher for their advice, encouragement and efforts
throughout this program. For providing the author with a listening
ear and helping hand, sincere gratitude is extended to Dr. J. H.
Brendemuhl who often helped motivate the author. Appreciation is
also extended to Dane Bernis for mixing diets and for providing both
practical and humorous information, and to him and his wife, Lynda,
for their friendship. To other faculty members who were helpful, the
author extends her gratitude for their concern during her education.
The author has been blessed with numerous friends who often
assisted with projects and elevated the quality of her life. For
example, F. and A. Fliss have been a constant source of encouragement
and assistance. Likewise, for the cooperation of her laboratory
companions, C. Ashworth, M. Murray, J. Dore, J. Vallet, K. Young, J.
Harney, D. Dubois, M. Dones-Smith, M. Mirando, T. Ott, L. Smith and
their spouses and(or) friends, the author is grateful. Thanks is
also extended to W. Grubaugh, Dr. K. Bachman, Dr. C. J. Wilcox, Dr.
R. Miller and P. Miles for their technical assistance. Without the
help of L. Joe Padgett and K. Corbett, work at the swine unit would
have been unbearable. The friendship of L. and R. Lawrence, M.
iii


McGuire, A. Williams, B. and M. Schwingel, T. Dawson, K. Bailey, S.
and V. Williams, P. and R. Miles, S. Black, J., D. and B. Yates and
T. and S. TenBroeck will be remembered long after the completion of
this dissertation.
The author extends deep appreciation to J. Weithenauer, for
providing a comfortable home when the author's husband got tired of
her and for unending humor and encouragement. For their constant
love and support, the author will be forever indebted to her family.
Lastly and certainly not the least, the author expresses heartfelt
gratitude to her husband, Donnie Ray, for his blend of affection and
humor without which the author would have had less of a reason to
pursue her goals.
IV


TABLE OF CONTENTS
Page
ACKNOWLEDGEMENTS iii
LIST OF TABLES viii
LIST OF FIGURES x
ABSTRACT xi
CHAPTERS
I INTRODUCTION 1
II REVIEW OF THE LITERATURE 4
//Introduction: Reproductive Efficiency 4
Control of the Estrous Cycle in Swine 7
Maternal Recognition of Pregnancy and Factors Associated
with the Establishment of Pregnancy 16
Embryonic/Fetal Mortality 28
Effects of Nutrition or Manipulation of Metabolism of Sows
During Gestation on Embryonic Survival, Litter Size and
Sow and Litter Performance During Lactation 50
¡/Influences of Nutrition Prior to Breeding or During Early
Gestation on Embryonic Survival 52
Effects of Nutrition During Mid- or Late-Gestation on
Piglet Birth Weight and Survival 54
(/Effects of Manipulating Sow Metabolism During Gestation
on Piglet Survival and Growth 61
Control and Initiation of Parturition 63
Physiology and Characteristics of Lactation in Swine. ... 75
Influence of Nutrition on Sow Performance During Lactation. 83
i/Influence of Nutrition on Post Weaning Sow Performance. . 92
Lactation 92
Post Weaning 101
Factors Influencing Piglet Survival 103
Factors Associated with Anestrous During and After
Lactation in Sows 107
Metabolism of Glutathione 116
Functions of Glutathione 126
Previous Research Associating Glutathione With Factors
Affecting Embryonic Growth 142
Metabolic Influences of Dietary Fructose 148
Occurence and Utilization 148
General Physiological Roles of Fructose 149
V


Influences of Fructose in Swine in Comparison to
Other Species 150
Digestion, Absorption and Transport 157
General Metabolism 159
Implications in Diabetes 164
Glucose Tolerance as Affected by Dietary Fructose .... 166
Effects on Other Glucoregulatory Hormones 173
Effects on Lipogenesis and Blood Lipids 175
Effects on Uric and Lactic Acid Production 179
Effects on Mineral Status 180
Effects on Amino Acid Absorption 181
Effects on Ethanol Metabolism 181
Previous Research Designed to Assess Effects of Fructose
on Sow and Litter Performance 183
III EFFECTS OF SUPPLEMENTAL GLUTATHIONE IN GESTATION DIETS OF
GILTS ON FACTORS ASSOCIATED WITH EARLY EMBRYONIC
SURVIVAL 196
Introduction 196
Materials and Methods 198
Results 201
Discussion 201
IV EFFECTS OF MATERNAL CONSUMPTION OF FRUCTOSE DURING LACTATION
ON SOW AND LITTER PERFORMANCE DURING LACTATION, INTERVAL
FROM WEANING TO ESTRUS AND METABOLIC INDICES IN PLASMA. 207
Introduction 207
Materials and Methods 210
Animals, Dietary Treatments and Collection of
Performance Data 210
Catheterization and Blood Collection Protocol 214
Glucose Tolerance Test 215
Processing of Blood Samples 215
Assay Procedures for Plasma Samples 216
Fructose 216
Growth hormone 216
Glucose 216
Nonesterified fatty acids 217
Insulin 217
Assay Procedures for Milk Samples 218
Milk fat 218
Lactose 218
Protein 218
Statistical Analyses 218
Results 221
Litter Performance 221
Litter size 221
Average piglet weight 221
Litter weight 224
Sow Performance 224
Sow weight change and feed consumption during
lactation 224
Postweaning interval to estrus 227
Milk yield 227
Milk composition 227
VI


Plasma Constituents 231
Fructose 231
Glucose 235
Insulin 237
Nonesterified fatty acids 246
Growth hormone 251
Response to glucose infusion 251
Discussion 257
V SUMMARY AND CONCLUSIONS 276
LITERATURE CITED 280
BIOGRAPHICAL SKETCH 354
vi i


LIST OF TABLES
Table Page
3-1 COMPOSITION OF THE GESTATION DIET (PERCENT BASIS) 199
3-2 EFFECTS OF DIETARY GLUTATHIONE ON FACTORS ASSOCIATED
WITH EARLY EMBRYONIC MORTALITY/CONCEPTUS DEVELOPMENT
AND METABOLISM OF GLUTATHIONE 202
4-1 COMPOSITION OF GESTATION DIET (PERCENT BASIS) 211
4-2 DIETARY COMPOSITION OF TREATMENTS DURING LACTATION .... 213
4-3 LITTER SIZE (LSMEANS) FOR EACH DIETARY TREATMENT BY
WEEK (WK) AND PARITY 222
4-4 AVERAGE PIGLET WEIGHT (LSMEANS) FOR EACH DIETARY
TREATMENT BY WEEK (WK) AND PARITY 223
4-5 LITTER WEIGHT (LSMEANS) FOR EACH DIETARY TREATMENT BY
WEEK (WK) AND PARITY 225
4-6 SOW WEIGHT CHANGE (LSMEANS) FOR EACH DIETARY TREATMENT
BY WEEK (WK) AND PARITY 226
4-7 AVERAGE (MEAN+SE) YIELD, CONTENT AND COMPOSITION OF MILK
FROM SOWS ON D 18 AND 22 OF LACTATION 230
4-8 PRE- AND POST-PRANDIAL MEAN SE CONCENTRATIONS
(MG/100 ML) OF FRUCTOSE IN PLASMA OF SOWS FED FRUCTOSE
OR DEXTROSE BY DAY 232
4-9 ANALYSIS OF REGRESSION CURVES OF CONCENTRATIONS OF
FRUCTOSE IN PLASMA 236
4-10 PRE- AND POST-PRANDIAL MEAN + SE CONCENTRATIONS
(MG/100 ML) OF GLUCOSE IN PLASMA OF SOWS FED FRUCTOSE
OR DEXTROSE BY DAY 238
4-11 ANALYSIS OF REGRESSION CURVES OF CONCENTRATIONS OF
GLUCOSE IN PLASMA 241
4-12 PRE- AND POST-PRANDIAL MEAN SE CONCENTRATIONS
(uU/10 ML) OF INSULIN IN PLASMA OF SOWS FED FRUCTOSE OR
DEXTROSE BY DAY 242
V i i


4-13 ANALYSIS OF REGRESSION CURVES OF CONCENTRATIONS OF
INSULIN IN PLASMA 245
4-14 PRE- AND POST-PRANDIAL CONCENTRATIONS (uEQ/L) OF
NONESTERIFIED FATTY ACIDS IN PLASMA AVERAGED OVER THE SIX
SAMPLING DAYS BY TREATMENT 247
4-15 ANALYSIS OF REGRESSION CURVES OF CONCENTRATIONS OF
NONESTERIFIED FATTY ACIDS IN PLASMA 250
4-16 PRE- AND POST-PRANDIAL LSMEANS SE CONCENTRATIONS (NG/ML)
OF GROWTH HORMONE IN PLASMA OF 14 SOWS SAMPLED ON D 27
OF LACTATION 252
4-17 CONCENTRATIONS (MEAN + SE) OF GLUCOSE AND INSULIN IN
PLASMA PRE- AND POST-INFUSION OF GLUCOSE 260
IX


LIST OF FIGURES
Figure Page
4-1 Percentage of sows that returned to estrus 229
4-2 Concentrations of fructose in plasma after ingestion of
Dextrose or HFCS 234
4-3 Concentrations of glucose in plasma after ingestion of
Dextrose or HFCS 240
4-4 Concentrations of insulin in plasma after ingestion of
Dextrose or HFCS 244
4-5 Concentrations of nonesterified fatty acids in plasma
after ingestion of Dextrose or HFCS 249
4-6 Concentrations of glucose in plasma in response to
glucose infusion for each day and treatment 254
4-7 Concentrations of insulin in plasma in response to
glucose infusion for each day and treatment 256
4-8 Glucose clearance for each treatment and day 259
X


Abstract of Dissertation Presented to the Graduate School
of the University of Florida in Partial Fulfillment of the
Requirements for the Degree of Doctor of Philosophy
REPRODUCTIVE EFFICIENCY OF SWINE AS INFLUENCED BY
FEEDING FRUCTOSE DURING LACTATION OR
GLUTATHIONE DURING EARLY GESTATION
By
Wendy Jo Campbell
August, 1988
Chairman: Fuller W. Bazer
Major Department: Animal Science
Supplemental glutathione (GSH) was fed to gilts on d 2 through 29
in a corn soybean meal-based diet; 0 (n = 5) or 10 (n = 5) mg GSH/kg
body weight (BW) per d. Embryonic survival, uterine, placental and
embryo weights, activities of glutamic-oxalacetic and glutamic
pyruvic transaminase in plasma, number of corpora ltea, number of
live embryos and total embryos and allantoic fluid and amnionic fluid
volumes were not influenced (P > .05) by dietary GSH on d 30.
In a second experiment, 45 multiparous (M) and 36 primiparous (P)
crossbred sows were fed, on a metabolic BW basis, from d 0 though d
28 of lactation, isonitrogenous and isocaloric corn-soybean
meal-based diets containing either 28% high fructose corn syrup or
22% dextrose (D). Plasma of sows fed fructose (F) contained: (1)
lower (P < .05) concentrations of glucose (G) postprandially; (2)
lower (P < .05) insulin preprandially and (3) higher (P < .05) F pre-
and post- prandially. Concentrations of growth hormone (GH) and
XI


nonesterified fatty acids in plasma and response to G challenge were
not altered (P > .05) by treatment. However, postprandially, GH in
plasma of P sows tended (P = .09) to be greater than for M sows.
Milk yield was not altered by treatment. Milk from D sows had higher
(P < .05) concentrations of lactose and milk from F sows had more (P
< .05) fat. Treatment did not affect (P > .05) weight loss of sows
or the postweaning interval to estrus. However, P sows lost more (P
< .05) weight than M sows and produced milk with greater (P = .06)
concentrations of protein. Litter size (LS) was higher (P < .05) for
sows fed F, and F had a greater effect (P < .05) over time on litter
weight than D. However, weights of piglets and litters at weaning
were similar (P > .05) between treatments. Sows fed F have lower
concentrations of G in plasma initially, but conversion of F to G
results in similar performance except for a slight advantage for F on
piglet survival.
Xll


CHAPTER I
INTRODUCTION
Reproductive efficiency in swine is not represented by any one
trait but rather the net sum of animal performance during various
stages of reproductive life. Reproductive efficiency is partially
determined by embryonic survival during gestation and by performance
of sows and their litters during lactation. These two major areas
greatly influence number and weight of piglets weaned for that
interval. However, another relevant factor is reproductive
performance of sows after weaning which influences number of piglets
produced per year. Various factors impact upon reproductive
performance of swine. One of the more important elements required
for production is nutrition; however, its specific interaction with
reproduction is not well defined. Because producers can easily
implement new feeding regimes, it is an area through which knowledge
gained through research can yield rapid benefits. Objectives of this
dissertation were to clarify effects of specific dietary ingredients
on embryonic survival and lactational and rebreeding performance in
swine.
In the first experiment, specific objectives were to determine
effects of supplementation of glutathione (GSH) in diets during early
gestation on factors associated with conceptus development and
embryonic survival. Because up to one-third of potential piglets are
lost due to embryonic mortality during gestation, factors associated
with survival are relevant. In swine and other species in which
1


2
multiple offspring are born, it is intriguing that certain embryos
survive while others perish within the same uterine environment.
This has led to the suggestion that embryos which survive are able to
more effectively compete for nutrients, growth factors or conceptus-
endometrial contact and(or) secretions during early blastocyst
expansion. Glutathione has been associated with numerous
physiological events. Most relevant is its apparent involvement in
in vitro growth of the ovum and stimulation of ovum growth and
uterine proliferation in rabbits. Concentrations of GSH also
increase in pig conceptuses during early growth and differentiation.
Therefore, it was hypothesized that exogenous GSH may provide
additional stimuli for growth in conceptuses and, if so, allow less
advanced embryos to survive. Since dietary ingredients provide the
most practical method of adminstering exogenous compounds, GSH was
incorporated into diets of gestating swine. Objectives included
evaluating effects of dietary GSH on embryonic survival, weights of
uteri, embryos and placentae, numbers of corpora ltea and live, dead
and total embryos, activities of glutamic-oxaloacetic and glutamic-
pyruvic transaminase and volumes of allantoic and amnionic fluid.
Measurements were obtained at d 30 of gestation, because most
embryonic losses occur prior to this time.
Milk production of sows is one of the primary factors limiting
piglet growth. In addition, primiparous sows often experience
anestrus after weaning which can decrease number of piglets born per
sow per year. Therefore, it is of interest to determine the optimum
and cost-effective dietary composition which will alter metabolism of
sows to allow maximum milk production while not hindering subsequent


3
reproductive performance after weaning. For numerous reasons,
effects of replacing part of the dietary energy source of sows with
high fructose corn syrup (HFCS) during gestation and(or) lactation
have been inconclusive. However, promising effects of dietary
fructose were reported on milk production of sows during lactation
and weights of litters at weaning, while negative effects on sow
weight change during lactation may be detrimental during the
postweaning interval to estrus. These effects have not been
confirmed and have been controversial. Effects of ingestion of
fructose in numerous species often depends upon other dietary
ingredients, metabolic status of animals prior to experimentation and
duration of fructose consumption. In some studies fructose resulted
in increased concentrations of insulin and glucose in plasma, while
opposite effects have been reported following other experiments.
Therefore, objectives of one aspect of this study were to further
evaluate effects of replacing part of the dietary energy source of
lactating sows with high fructose corn syrup and dextrose.
Production traits of interest were: (1) litter size and litter weight
gain throughout a 4 wk lactation; (2) sow milk production, weight
loss and interval to estrus after weaning; (3) plasma metabolic
indices, including concentrations of glucose, fructose, growth
hormone, insulin and nonesterified fatty acids in plasma pre- and
post-prandially and (4) response to glucose challenge.


CHAPTER II
REVIEW OF THE LITERATURE
Introduction: Reproductive Efficiency
Factors affecting reproduction in pigs and management
considerations to enhance their reproductive efficiency have been
reviewed (Johnson, 1984; Terqui and Legault, 1984; Dziuk and Bellows,
1983; Yen et al., 1987). As Johnson (1984) indicated: "reproductive
efficiency is a function of age at puberty, fertility (the percentage
of breeding herd females that conceive), fecundity (the number of
offspring per pregnancy) and offspring survival to weaning." Terqui
and Legault (1984) stated that the number of offspring weaned per dam
is one of the best estimate of reproductive efficiency in all species
and that this has been called "numerical productivity." In swine,
numerical productivity (P ) of sows can be expressed as [0'(1 -
em)(l pm)/I] x 365, where "0" is ovulation, rate, "em" is embryonic
mortality rate from ovulation to parturition, "pm" is mortality rate
from birth to weaning and "I" is the interval between successive
parturitions in days. Terqui and Legault (1984) indicated that "I"
represents the interval from weaning to fertilization in lactating
sows. They suggested that numerical productivity should also include
age at first parturition (m^) and the interval between last
parturition and culling of the female (m2). Therefore, their
estimate of productivity would be: P'n = [N x 0(1 em)(l -
pm)]/[m-^ + (N 1) x I + m2] x 365, where "N" represents the
average number of reproductive cycles at culling. Although
4


5
reproductive efficiency can be defined in numerous ways, e.g., "Sow
Productivity Index" (Yen et al., 1987), all methods estimate number
of pigs produced within the sow's reproductive life. Goals of
producers include maximizing piglets per litter and litters per sow
per year. Factors which influence reproductive efficiency include
genetics, environmental conditions, e.g., photoperiod, temperature,
social interactions, and nutrition.
Age at puberty has moderate heritability (.30) in swine
(Cunningham et al., 1974) and is influenced most by environmental
factors. Tess et al. (1983) determined that the most important
economic consideration in reproductive efficiency of swine is number
of live pigs per litter at birth. This can be influenced by
ovulation and fertility rates, embryonic mortality and losses at
parturition. Although ovulation rate can be increased by selection
(Cunnigham et al., 1979) or administrations of exogenous hormones
(Webel and Day, 1982), it is balanced by decreased embryonic survival-
(Cunningham et al., 1979). Fertility is not a major problem in swine
with the exception of summer or heat-induced infertility (Wetteman
and Bazer, 1985), which can be overcome to a large degree with proper
management. Likewise, parturition is not a major complication in
swine, but can be successfully induced (First and Lohse, 1984) to
increase management efficiency; however, it has limited usefulness
for decreasing the interval between farrowings. Genetic selection
for reproductive efficiency has limited potential, due to low
heritabilities for reproductive traits (Johnson, 1984; Terqui and
Legault, 1984) and other production traits are important in meat
producing animals. Nutritional factors may be exploited to maximize


6
reproductive efficiency. However, optimum nutritional regimens for
the various stages of sows reproductive cycles have not been
determined. Supplementation of certain nutrients, e.g., riboflavin,
during gestation may increase embryonic/fetal survival to term (F. W.
Bazer and M. T. Zavy, personal communication). Manipulation of the
metabolic status of sows during gestation by dietary or
pharmacological agents which induce a diabetic state may increase
fetal energy reserves and enhance survival at birth (Britt, 1986).
Nothing is more vital to neonatal piglets than availability of
immunoglobulins and energy from colostrum at birth. Therefore,
nutrition during gestation and(or) lactation has a significant
influence on piglet survival and growth by influencing milk
production. Similarly, nutritional status influences weight loss and
body condition of sows and, therefore, their ability to rebreed after
weaning which, in turn, affects the interval between parturition.
Scientists are continually searching for factors which will
enhance reproductive efficiency. These approaches enhance our
understanding of physiological mechanisms associated with
reproduction and suggest management protocols to enhance reproductive
efficiency. Nutrition is definitely not a solitary factor, but as
innovative goals are realized, larger litters will be produced and
nutritional requirements will need to be modified to complement
advances in other disciplines that maximize reproductive efficiency
in swine. This review summarizes our knowledge of factors affecting
reproductive efficiency in swine.


7
Control of the Estrous Cycle in Swine
Estrous cyclicity in all mammalian species is dependent upon
proper interactions between the components of the hypothalamic-
pituitary-gonadal axis and the uterus (Anderson, 1974b). Appropriate
morphological modifications and altered secretory functions of these
reproductive tissues allow the sexually mature female pig to display
polyestrous activity (Anderson, 1974b) under domestic conditions and
to complete one estrous cycle approximately every 21+3 days
(Anderson, 1974b; Sorenson, 1979). Although the pig is not a
seasonal breeder, seasonal variation does exist (Ledwitz-Rigby and
Rigby, 1987; Claus and Weiler, 1985). Numerous reviews concerning
reproductive physiology of swine have been published (Anderson,
1974b; Hansel and Convey, 1983; Foxcroft and Van de Wiel, 1982).
This review is not intended to describe mechanisms associated with
follicular growth, intrafollicular communication, selection of
ovulatory follicles, ovulation and other specific events. Rather,
this review is to provide a general overview of the reproductive
biology of female pigs.
The 21-day-estrous cycle in swine is commonly divided into four
phases: estrus, metestrus, diestrus and proestrus (Anderson, 1974b).
The female is sexually receptive to a boar for approximately 24 to 66
h during estrus and the first day of "estrus" is referred to as day
(d) 0 of the estrous cycle. At estrus, concentrations of estrogen,
follicle stimulating hormone (FSH) and progesterone in plasma are low
(Anderson, 1974b). Approximately 38 to 42 h after onset of estrus,
multiple Graffian follicles, selected by a yet undefined mechanism,
ovulate. Ovulation itself results from a complex physiological


8
cascade of events (Murdoch, 1985) initiated primarily by the
ovulatory surge of luteinizing hormone (LH). The LH surge is induced
by the positive feedback of estrogen produced from growing follicles
on the hypothalamic-pituitary axis. Concentrations of LH in plasma
decline rapidly following the LH surge. Metestrus begins as the
female ceases to be sexually receptive and is characterized by low
levels of estrogen, FSH and LH, but increasing concentrations of
progesterone in plasma produced by developing corpora ltea (CL).
During diestrus (d 3 to 4 though d 15 to 16), progesterone secretion
is maximal while concentrations of LH, FSH and estrogen in plasma
remain low. In nonpregant pigs, the CL begin to regress between d 15
to 16 due to prostaglandin F 2-alpha (PGF) secretion by the uterus.
Therefore, progesterone secretion by CL declines and there is
initiation of the proestrous phase. Simultaneously, preovulatory
follicles begin to develop and produce estrogen so that
concentrations in plasma peak around d 18. The elevated estrogen
levels decline to low levels before the subsequent estrous period
begins, but are elevated sufficiently to initiate the ovulatory surge
of LH and initiate a new estrous cycle. Some of these events will
now be discussed in more detail. The luteal phase (diestrus),
terminated by the mechanism of luteolysis, the early follicular
phase, late follicular phase and pre-ovulatory period (proestrus and
estrus) and the periovulatory period (including the early luteal
phase (metestrus) will be discussed in this order as suggested by
Foxcroft and Van de Wiel (1982).
Maintenance of luteal function and thus, continued progesterone
production (Foxcroft and Van de Wiel, 1982), blocks the final stages


9
of follicular growth and steroidogenesis and controls the length of
the estrous cycle. A rise in progesterone generally occurs on d 3 to
4 of the estrous cycle (Van de Wiel et al., 1981). Although the
pattern of secretion may be altered by season (Perotti et al., 1979),
progesterone secretion, as measured in the ovarian vein (Gomes et
al., 1965), is maximal on d 10 to 12, declines slowly to d 13 to 15
and then falls rapidly. However, Masuda et al. (1967) reported
maximal progesterone production on d 8 in the ovarian vein. It is
possible that pigs can sequester progesterone in body fat and return
progesterone into the circulation after luteolysis resulting in a
latent fall in progesterone, and thus, longer effects of progesterone
on the hypothalamic-pituitary axis (Foxcroft and Van de Wiel, 1982).
Whether there is a physiological requirement for a luteotrophin other
than LH in swine is not clear. Prolactin has been demonstrated to
stimulate progesterone secretion by luteinized pig granulosa cells
(Veldhuis et al., 1980) and isolated luteal cells in vitro
(Gregoraszczuk, 1983; Grinwich et al., 1983). Recently, Bramley and
Menzies (1987) characterized receptor numbers for prolactin in the
porcine corpus luteum. Prolactin receptors were low during the
periovulatory and early luteal period, increased in the mid-luteal
phase and declined in the late luteal phase. In pregnant swine, as
gestation advanced, prolactin receptor concentrations in CL
increased. It is known that exogenous estrogens elevate plasma
progesterone levels, prolong CL lifespan (Ford et al., 1982) and
stimulate progesterone production by porcine granulosa cells in vitro
(Goldenburg et al., 1972). However, whether estrogen and prolactin


10
play necessary and direct luteotrophic roles endogenously is not
certain.
Luteolysis in pigs is strongly associated with production of PGF
by the uterus (see Bazer et al., 1982). Moeljono et al. (1976, 1977)
proposed that PGF is the luteolysin in swine and reported increasing
PGF levels in utero-ovarian vein plasma coincident with luteal
regression (Gleeson et al., 1974; Moeljono et al., 1976; Ford et al.,
1982) Exogenous PGF was luteolytic in gilts in which CL were
maintained beyond their normal life span by estradiol treatment
(Kraeling et al., 1975) or hysterectomy (Moeljono et al., 1976).
However, PGF can only exert a luteolytic effect after d 12 (Diehl and
Day, 1974; Moeljono et al., 1976). To reach the ovary,
prostaglandins produced by the uterus can be transferred to the
ovarian artery and possibly into the lymphatic circulation (Kotwica,
1980). Since exogenous gonadotropins cannot maintain CL of the cycle
in the presence of an intact uterus (Anderson, 1966) it is suggested
that PGF inactivates some component of the LH stimulatory mechanism
that is effective in maintaining luteal function in hysterectomized
females. Thus, PGF overrides the luteotrophic effect of LH by
blocking the LH-adenylate cyclase pathway. It appears that a loss of
LH-receptor mediated mechanisms within luteal tissue results in the
decline in progesterone synthesis (Foxcroft and Van de Wiel, 1982).
Evidence of coincident increases in prolactin and decreases in
progesterone (Van de Wiel et al., 1981) and indications that
prolactin inhibits progesterone secretion by porcine granulosa cells
(Rolland et al., 1976), have led to speculation that prolactin plays
a role in luteolysis. However, the initial fall in progesterone and


11
increases in estradiol and prolactin occur simultaneously, so it is
difficult to establish exact cause and effect relationships.
However, the majority of literature indicates that PGF is the
luteolysin which, in the absence of a conceptus, overrides
luteotrophic effects of LH and(or) prolactin (see Bazer et al., 1982;
Moeljono et al., 1976).
Resumption of follicular growth and production of estrogens are
initiated following luteolysis. The factor responsible for
initiating onset of increased estrogen production by follicles during
the late luteal/early follicular phase of the cycle is not known.
Whether progesterone blocks ovarian follicular development directly
(thus, removal of progesterone may involve removal of an inhibitory
influence on intra-ovarian factors necessary for initiation of late
follicular growth) or by acting on the hypothalamic-pituitary axis to
inhibit an appropriate pattern of LH:FSH production is not clear.
Whatever the exact mechanism, as the luteal phase ends, certain large
follicles which had previously begun development have increased: (1)
granulosa LH receptor numbers (100 X); (2) LH-stimulated cAMP
production; (3) ability of granulosa cells to secrete progesterone
and convert androgen to estrogens and (4) responsiveness to FSH to
stimulate androgen aromatization in granulosa cells (Anderson et al.,
1979; Leung et al., 1979; Schwartz-Kripner and Channing, 1979).
These changes may be similar to those proposed for rats (Armstrong
and Dorrington, 1977; Richards et al., 1978). Foxcroft and Van de
Wiel (1982) suggest that these follicular responses involve estrogen-
dependent changes in receptors for LH and FSH in granulosa cells and
induction of aromatase enzymes intracellularly. This would allow for


12
LH-induced increases in androgen production by theca cells followed
by increases in aromatization of androgens to estrogens by granulosa
cells. It is important to note that, unlike sheep and cows, pig
granulosa cells produce estradiol in the absence of detectable
androgens. This is possibly due to stored androgens of thecal origin
in the granulosa cells (Evans et al., 1981). Additionally, porcine
thecal cells, as well as granulosa cells, can aromatize androgens to
estradiol. Although the exact mechanism is not clear, Graffian
follicles develop and estrogen production increases in the early
follicular phase. As a result, during the late follicular phase and
pre-ovulatory period, concentrations of circulating estrogens are
elevated between d 18 to 20 (Van de Wiel et al., 1981). Estrogens
exert a positive feedback on the hypothalamus in pigs (Edwards, 1980)
and, in vivo, the pre-ovulatory surge of LH and FSH occurs
approximately 50 to 55 h after the rise in estrogens. However, the
rise in estradiol initially results in suppression of episodic LH
release and, later, inhibition of FSH production which results in low
gonadotrophin levels immediately prior to their surge (Vandalem et
al., 1979; Foxcroft, 1978; Van de Wiel et al., 1981). The rise in
plasma LH and its characteristic preovulatory surge 40 to 48 h prior
to ovulation, with a duration of approximately 20 h concident with
the onset of estrus, has been confirmed by numerous researchers
(Liptrap and Raeside, 1966; Niswender et al., 1970; Henricks et al.,
1972; Rayford et al., 1971; Parvizi et al., 1976; Vandalem et al.,
1979; Edwards, 1980; Van de Wiel et al., 1981). However, the
relationship between the onset of behavioral estrus and timing of the
LH surge is variable (Foxcroft et al., unpublished data in Foxcroft


13
and Van de Wiel, 1982). Van de Wiel et al. (1981) reported maximum
LH levels of 6 ng/ml during the LH surge versus 3 ng/ml associated
with tonic secretion of LH during the luteal phase. Thus, the LH
surge of the pig is not characterized by a discrete LH surge, but one
of rather long duration (Foxcroft and Van de Wiel, 1982). The
response of FSH to estradiol positive feedback is variable. However,
it appears that estrogen directly induces a surge of FSH release
(Elsaesser and Foxcroft, 1978; Edwards, 1980) concident with the LH
surge, but of lower magnitude. As a result of the LH surge,
luteinization of the theca and granulosa cells occurs, estradiol
production declines rapidly, progesterone synthesis gradually
increases and ovulation occurs (Catt et al., 1979; Hunzicker-Dunn et
al., 1979). The requirement of the FSH surge for these phenomena is
questionable (Edwards, 1980), since periovulatory events have been
observed in early weaned sows which did not experience an FSH surge.
Ovulation generally occurs near the end of d 2 of the estrous
cycle when LH levels are low and FSH levels are high (Rayford et al.,
1974; Vandalem et al., 1979; Edwards, 1980; Van de Wiel et al.,
1981) Whether this rise in FSH is due to removal of inhibin at the
time of ovulation (Channing, 1979) or declining estradiol (Edwards,
1980) is not certain. Foxcroft and Van de Wiel (1982) suggest that
inhibin would specifically regulate FSH secretion. Furthermore,
whether or not the increase in FSH is important for recruitment of
follicles destined to ovulate during the subsequent estrous period
has not been resolved for pigs. Increasing concentrations of
progesterone in the postovulatory period are associated with a
decline in FSH (Vandalem et al., 1979; Edwards, 1980, Van de Wiel et


14
al., 1981), and simultaneously, development of episodic LH release
with increasing amplitude and decreasing frequency. Wilfinger (1974)
and Van de Wiel et al. (1981) also reported increased prolactin
secretion at this time with no known role, but with a possible
function in expression of behavioral estrus. Although numerous
patterns of hormonal secretion have been characterized, the exact
mechanism(s) responsible for follicular recruitment have not been
defined.
Attempts to control length of the luteal or follicular phase of
the cycle pharmacologically to facilitate management of labor and
increase reproductive efficiency have led to inconsistent results
(for review, see Webel and Day, 1982; Day, 1984). Currently, the
most promising approach towards effective regulation of the estrous
cycle in swine involves the use of synthetic steroids with progesta
tional activity, e.g., altrenogest. Altrenogest has been effective
in synchronizing estrus to a 4-day period in approximatly 95% of
gilts which have already exhibited estrus by administering altreno
gest (15 to 20 mg/day) orally for 18 consecutive days (Redmer and
Day, 1981). Other regimens and doses have been tested (see Webel,
1978; Webel and Day, 1982; Day, 1984), and treatment of young gilts
with altrenogest appears to be a potentially useful management tool.
Genetic selection, pharmacological agents and elevating the
nutritional plane of energy (flushing) (Anderson and Melampy, 1972;
Den Hartog and Van Kempen, 1980; Dziuk and Bellows, 1983) prior to
ovulation have all been utilized to increase ovulation rates in
gilts. It is firmly established that increased feed or energy intake
prior to mating will increase ovulation rate, and the optimum intake


15
period has been reported to be in excess of 11 d (Den Hartog and Van
Kempen, 1980) or as little as 8 to 10 d (Anderson and Melampy,
1972). However, whether flushing increases ovulation rate beyond
normal expectations, or reverses nutritional inhibition due to
previous low levels of feeding is not certain (Anderson and Melampy,
1972). For a review of management recommendations (genetic,
nutritional and age considerations) of gilts aimed at improving
ovulation rates refer to Christenson (1986) or Aherne and Kirkwood
(1985).
The mechanism whereby increased dietary energy elevates ovulation
rate is not known. However, neither increased dietary energy or
exogenous insulin is necessarily accompanied by changes in
gonadotropins or estradiol (Cox et al., 1987). Cox et al. (1987)
suggest the increased ovulation rate induced by diet and insulin may
be due to recruitment of more follicles or lessening of atresia, thus
providing more preovulatory follicles. Direct effects of insulin on
the ovaries have been reported, including promotion of progesterone
production by granulosa (May and Schomberg, 1981) and luteal cells
(Ladenheim et al., 1984) in culture, and androstenedione production
by thecal cells (Barbieri et al., 1983). In addition, insulin and
insulin receptors have been identified in the vicinity of
gonadotropin releasing hormone-producing neurons (Havrankova et al.,
1978) in the hypothalamus. The effects of high energy and insulin on
LH secretion were not clear in the study of Cox et al. (1987). In
experiment 1, both dietary energy and insulin were positively related
with number of LH pulses and ovulation rate. However, in experiment
2 no treatment differences were detected. In a separate report by


16
Flowers et al. (1986), FSH and LH were positively influenced by
flushing between 2 and 5 d prior to estrus.
Thus, the effects of flushing and of insulin are not well
defined, but any or all components of the hypothalamo-hypophyseal-
ovarian axis may be affected by insulin (Cox et al., 1987). Since
increased ovulation rate is accompanied by decreased embryonic/fetal
survival (Johnson et al., 1985), it may be more practical to select
for larger litters and attempt to reduce prenatal and postnatal
losses in pigs rather than attempt to increase ovulation rates.
Maternal Recognition of Pregnancy
and Factors Associated with the Establishment of Pregnancy
Under normal conditions, the luteolysin (presumed to be PGF; see
Bazer et al., 1982) in the pig causes regression of the CL, beginning
around d 15 in nonpregnant pigs. This allows for recurrent estrous
cycles. However, should the female become pregnant, the developing
conceptuses must signal their existence to the uterine endometrium in
order to maintain functional CL and endometrial development and
secretory activity which will permit a gestation period of 114 to 115
d to follow. As reviewed by Bazer et al. (1982), the conceptus is
believed to initiate luteostatic mechanisms via the production of
estrogens (also see Flint et al., 1979a). The exocrine-endocrine
theory (Bazer and Thatcher, 1977) suggests that under the influence
of estrogen produced by the conceptuses, PGF and other components of
endometrial origin, including necessary histotrophic factors, are
directed into the uterine lumen (exocrine direction) (Marengo et al.,
1986). This prevents release of the luteolysin towards the uterine
vasculature (endocrine direction). Thus, establishment and
maintenance of pregancy are initiated.


17
Probably the single most important requirement for establishment
of pregnancy is maintenance of CL. Loss of CL function at any stage
of gestation leads to abortion within 24 to 36 h (Belt et al., 1971)
since CL are required for progesterone production. Concentrations of
progesterone in maternal plasma during pregnancy reach 30 to 40 ng/ml
on d 12 to 14, decline to 10 to 25 ng/ml by d 25 (Guthrie et al.,
1974; Robertson and King, 1974; Knight et al., 1977), and remain
fairly constant until d 100. Then, progesterone levels decline
gradually prior to parturition at which time they decrease abruptly
to <1 ng/ml. However, DeHoff et al. (1986) reported that concentra
tions of progesterone peak at d 45 (35 ng/ml), decline at d 60 and
then remained farily constant until a rapid periparturient decrease.
The CL of pigs appear to be autonomous until d 14, and then
require only basal LH support until d 40 to 50. After that time, a
possible role for prolactin in CL maintenance has been suggested (see
Heap et al., 1973). However, based on later studies (Whitacre and
Threlfall, 1981; R. R. Kraeling, unpublished data, cited by Bazer et
al., 1982), it appears that prolactin may not be necessary for CL
maintenance after d 70 of gestation. Recently, Bramley and Menzies
(1987) suggested that prolactin may be luteotrophic during pregnancy
as indicated by increasing numbers of prolactin receptors as gesta
tion advances. Whatever the luteotropic agents may be, it is impera
tive that they function properly to ensure successful pregnancy.
Following fertilization, embryos move through the oviducts and
into the uterine horns at about the 4-cell stage, approximately 48 h
after ovulation (Hunter, 1974). Transport through the oviduct is
entirely a maternal function involving flow of secretions, movement


18
of cilia, peristaltic contractions, and the actions of gonadal
steroids and prostaglandins (Hunter, 1974). Pig embryos fail to
develop beyond the early blastocyst stage if confined to the oviduct
(Murray et al., 1971; Pope and Day, 1972). Therefore, it is a
requirement that the embryos reach the uterine environment.
Having passed through the oviduct, porcine embryos temporarily
are free to move throughout the uterus (Dziuk et al., 1964), but are
actively undergoing morphological changes. Niemann and Elsaesser
(1986) suggested that estradiol-17B is necessary for
morula-blastocyst transformation in vitro and that the effect is
mediated through specific binding sites. Niemann and Elsaesser
(1986) tested in vitro effects of withdrawing estradiol on
development of porcine morula using an antiestrogen or an antiserum
to estradiol. These compounds reduced rate of blastocyst formation,
and this reduction could be partially reversed by addition of
estradiol-17B to the culture medium. In a subsequent study, Niemann
and Elsaesser (1987) confirmed that estradiol-17B is a potentially
important factor in morula-blastocyst transformation in vitro. The
effects of estrone on transformation were less evident. Whether in
vitro effects of estradiol on transformation is physiologically
relevant remains to be determined.
Embryos reach the blastocyst stage by d 5 and hatch from the zona
pellucida between d 6 and 7. After hatching, blastocysts expand from
0.5 to 1 mm diameter to 2 to 6 mm diameter on d 10. Then, between d
10 to 12, blastocysts undergo the most rapid elongation phase,
changing from spherical (3 to 10 mm diameter), to tubular (10 to 50
mm long) and filamentous (>100 mm long) forms, resulting in lengths


19
of 700 to 1000 mm by d 16 of pregnancy (Perry and Rowlands, 1962;
Anderson, 1978). Geisert et al. (1982a) reported that initial
elongation (from 9-10 mm to 100-200 mm) is due to remodeling of
existing trophectoderm. The final elongation (100-200 mm to
800-1,000 mm; d 14 to 16) involves cellular hyperplasia. Albertini
et al. (1987) have begun to investigate the role of actin
cytoskeleton reorganization during premiplantation development of pig
embryos from d 1 through d 8 of gestation. Their experiment was
based on the premise that actin filaments may be involved in
contractile events during compaction (Johnson and Maro, 1984) and
differentiation of trophectoderm (Lehtonen and Bradley, 1980; Reima
and Lehtonen, 1985). Although inconclusive, their results suggest
that actin is important in mechanisms responsible for blastocyst
elongation. Failure of blastocyst elongation can lead to embryonic
death early in gestation or submaximal placental development (Perry
and Rowlands, 1962; Knight et al., 1977).
Although, pig embryos are initially freely mobile, elongated
conceptuses cannot undergo further spacing so they lie end-to-end
along the length of the uterine horns in preparation for
implantation. Spacing of spherical conceptuses is a necessary
requirement since they must compete for a limited amount of
endometrial surface area to obtain support from the endometrial
secretions during placentation. Scheerboom et al. (1987) measured
uterine motility in sows during the estrous cycle and early
pregnancy. They suggested that increased frequency of myoelectrical
complexes (episodes of activity and subsequent interval of
inactivity) may be involved in the process of intra-uterine migration


20
of conceptuses. The interval between myoelectrical complexes
decreased on d 12 of gestation. They also reported that myometrial
activity of low magnitude and high frequency was present during d 8
to 9 of gestation. Pope et al. (1982b) had previously indicated that
contractions of the myometrium are involved in the process of embryo
spacing. Pope et al. (1982b) suspended uterine strips in baths,
during the period of intrauterine migration (d 12 of gestation), and
showed increased myometrial activity in comparison to uterine strips
excised on d 6 to 9 of gestation.
In a subsequent study, Pope et al. (1986a) attempted to examine
the process of intrauterine migration of porcine embryos by studying
a model involving migration of estradiol- and cholesterol-releasing
beads in tero. The presence of estradiol-releasing beads resulted
in activity that induced adjacent beads (estradiol and cholesterol
beads) within the uterus to migrate posteriorly from the uterine
tips. However, cholesterol releasing-beads failed to migrate as far
as estradiol-impregnated beads. The possibility that adjacent
embryos migrate as a result of activated myometrial function was
examined in a second experiment. The results were not clear, but
estradiol release locally tended to induce a random distribution of
cholesterol- impregnated beads. In a third experiment (Pope et al.,
1986a), however, estradiol tended to induce anterior migration when
cholesterol-containing beads were placed at the base of the uterine
horn. Pope et al. (1986a) could not conclude whether the uterus was
responding differentially depending on the site of estrogenic action
or whether the anterior, posterior migrations were due to random
intermixing. None-the-less, it appears that estrogen is involved in


21
embryo migration and the waves of uterine contractions. However,
Scheerboom et al. (1987) suggested the myometrial activity is
dependent on ovarian hormones and independent of the blastocyst
because of similar responses in cyclic and pregnant gilts.
Pig conceptuses are known to produce estrogens while undergoing
elongation (Flint et al., 1979a). In addition, Fischer et al. (1985)
demonstrated that estradiol production is initiated by large (7 mm)
spherical conceptuses and then estrone and estradiol are produced by
tubular conceptuses in amounts greater than are produced by d 12
filamentous conceptuses. Fischer et al. (1985) also demonstrated
that [ H]-progesterone could be converted to estrogens. Their
results agree with data obtained from analyses of uterine flushings
and uteroovarian vein plasma for estrogens. In addition, Fischer et
al. (1985) reported that both the conceptus and pregnant endometrium
converted progesterone to estrogens. The initial increase in
estrogen content in uterine flushings (Geisert et al., 1982b) occurs
when conceptuses reach approximately 10 mm in diameter (late
spherical, d 11.5), which coincides with the time of maternal
recognition of pregnancy (Dhindsa and Dziuk, 1968; Bazer and
Thatcher, 1977; Flint et al., 1979a) and just precedes initiation of
trophectoderm elongation. Based on measurements of estrone sulfate
in maternal plasma, estrogen production by pig conceptuses is
triphasic with the first peak occurring between d 10 to 12 (Stoner et
al., 1981). Maternal estrone sulfate increases from d 16 (60 pg/ml)
to d 30 (3 ng/ml) (Robertson and King, 1974; Stoner et al., 1981),
decreases to d 46 (35 pg/ml), increases slightly to d 60, and then
increases steadily to parturition (3 ng/ml) (Robertson and King,


22
1974). Knight et al. (1977) reported the same pattern for
unconjugated estrone and estradiol in peripheral and uterine vein
plasma and amniotic and allantoic fluids. However, Kensinger et al.
(1986) reported higher estradiol values than Knight et al. (1977) and
concentrations similar to Robertson and King (1974). Robertson et
al. (1985) measured estrogens in fetal fluids and maternal blood and
urine and confirmed previous estimates. DeHoff et al. (1986) also
reported patterns of estradiol, estrone and their sulfated forms
similar to those described above. In addition, Robertson et al.
(1985) suggested that the second rise in estrogen concentrations (d
30) reflects estrogen synthesis by the fetus rather than the
trophoblast. Kensinger et al. (1986) and Knight et al. (1977)
indicated that conjugated estrogens at d 30 and during late pregnancy
are primarily of feto-placental origin. Furthermore, during the last
third of gestation, maternal concentrations of estrogen sulfate and
estrone are directly affected by the number of conceptuses present.
According to the exocrine-endocrine theory (Bazer and Thatcher,
1977) failure of conceptuses to produce adequate estrogens can
result in regression of CL and loss of pregnancy, since PGF will be
allowed to be secreted in an endocrine direction. That estrogens
themselves and not prostaglandin E-^ or E2 are responsible for
movement of PGF into the uterine lumen was demonstrated by Marengo et
al. (1986).
While, conceptuses are undergoing extensive remodelling and
initiating steroid synthesis, the endometrium is actively preparing
for gestation. Similar to conceptuses, the uterine horns and
endometrium elongate (Perry and Rowlands, 1962) from 190 cm on d 3 to


23
a length of 360 cm at d 13 to 18. Some aspects of early embryonic
development have been reviewed by Allen (1984) and Bazer and First
(1983). On approximately d 13 of gestation, porcine conceptuses
begin physical attachment, seen histologically as discrete areas of
cell-to-cell contact, which is maintained by the adhesive properties
of endometrial gland exocrine secretions (Crombie, 1970).
Although the mechanism(s) involved in attachment of blastocysts
to the uterine epithelium is not well understood, Morgan et al.
(1987a,b) suggested that estrogen is involved. Morgan et al. (1987a)
speculated that ultrastructural and biochemical changes occur in the
plasmalemma of the uterine surface epithelium in response to estrogen
for blastocyst attachment. Schlafke and Enders (1975) previously
suggested that attachment is likely mediated by such changes in the
plasma membrane surface of the trophoblast and uterine specific
epithelium. Alteration of protein and polysaccharide composition
occurs on the apical surface of the rabbit endometrium at the time of
implantation (Anderson et al., 1986). Alterations of glycoprotein
coatings on both the trophoblast and epithelial cell plasma membrane
have been suggested by other researchers to be responsible for close
apposition necessary for interdigitation of microvilli (Enders and
Schlafke, 1974; Jenkinson and Searle, 1977).
Keys et al. (1986) utilized a technique involving systemic
injection of Evans blue and localization of endometrial fluorescence
to determine extravascular content of the dye, and thus, endometrial
vascular permeability in the pig. Only in pregnant gilts, at d 12 of
gestation, was a well-defined area of endometrial fluorescence
detected. The response appeared in conjunction with blastocyst


24
elongation and was consistently confined to areas of conceptus
membranes. The coincidence of increased uterine vascular
permeability at the site of attachment and elevated blood flow,
suggest enhanced transport of nutrients toward the conceptus and
movement of conceptus- induced products into the maternal
circulation. Furthermore, it appears that embryonic factors act in a
localized manner to increase uterine vascular permeability
selectively during attachment. Histamines (Dey and Johnson, 1980),
prostaglandins, e.g., PGE (Davis et al., 1983) and estrogens (King
and Ackerley, 1985) of conceptus origin have all been suggested to be
involved in this response (Keys et al., 1986).
From d 16, a microvillous attachment develops between trophoblast
and endometrial epithelium and extends rapidly to cover almost the
entire chorion by d 22 (Bjorkman, 1965). Expansion and development
of the allantois rapidly occurs between d 18 and 30 of gestation.
Fetal and maternal surfaces undergo complex folding to increase
surface area, and areolae develop on the chorioallantois at points
where endometrial glands open into the uterine lumen. Additional
folding of the chorion occurs in each areolus to increase surface
area and to allow for uterine gland secretions to accumulate
(Crombie, 1970). Fusion of chorion and allantois occurs between d 30
and d 60 of pregnancy, and by d 60 to 70, placental development is
complete. Because placentation in the pig is superficial with no
invasion of maternal uterine endometrium, transfer of histotroph from
the endometrial surface occurs at least through the second trimester
of gestation (Bazer and First, 1983). Maintenance of pregnancy
requires successful development of the placenta, so the embryo-fetal


25
units can receive nutrients, wastes can be removed and the conceptus
will be protected from the maternal immune system.
Because of the noninvasive nature of placentation in the pig, it
is likely that a high proportion of the nutrients of the trophoblast
are secreted by endometrial glands and surface epithelium (Amoroso,
1952; Dantzer et al., 1981). Numerous reviews of uterine secretions
during pregnancy and blastocyst-endometrial interactions are
available (Bazer and First, 1983; Flint et al., 1982; Bazer and
Roberts, 1983; Bazer et al., 1986; Roberts and Bazer, 1988).
Fazleabas et al. (1985) demonstrated that, depending upon the
physiological purpose of a protein, some proteins (uteroferrin) are
secreted by uterine gland epithelium, while other proteins (plasmin
inhibitor) are secreted by the surface epithelium. Thus, the pig
epithelium is regionally differentiated. In addition, results of
Fazleabas et al. (1985) confirmed previous reports (Knight et al. ,
1973, 1974a,b) that uterine secretory proteins are under
progestational control. Furthermore, while secretion of proteins by
the pregnant uterus is induced by progesterone, estradiol modulates
the magnitude of secretion of progesterone induced proteins.
Included among the list of endometrial secretory proteins,
induced at least partially by progesterone (Knight et al., 1973) and
produced in early pregnancy (Zavy et al., 1977), are three enzymes:
uteroferrin, lysozyme and leucine aminopeptidase. These enzymes have
been shown to accumulate in allantoic fluid after d 30 of pregnancy
(Bazer et al., 1975; Roberts et al., 1976). Based on
immunoflourescent studies, these and certain other compounds of
endometrial origin can pass into the fetus via the chorio-allantoic


26
areolae (Chen et al., 1975). Uteroferrin is involved in the
transport of iron from uterine glands to the conceptus (Roberts and
Bazer, 1980; Bazer et al., 1981b; Ducsay et al., 1986). Other
transport proteins such as retinol and retinoic acid binding
proteins, hydrolytic enzymes and regulatory proteins have been found
in uterine secretions of ovariectomized pigs injected with
progesterone. A high content of riboflavin in uterine flushings has
been reported during the initial period of blastocyst expansion
(Moffatt et al., 1980; Murray et al., 1980). Riboflavin appears to
increase embryonic survival when administered orally during early
gestation (F. W. Bazer and M. T. Zavy, personal communication).
Glucose, fructose and ascorbic acid are also found in uterine
flushings and increase in the pregnant uterus as gestation progresses
(Zavy et al., 1982). Thus, the allantoic fluid of pigs contains
substantial quantities of nutrients, including proteins detected in
uterine flushings, glucose, fructose, water, minerals, electrolytes
and vitamins (see Bazer et al., 1981a). The placental areolae appear
to transport these nutrients to the fetus, by fluid-phase pinocytosis
(Friess et al. 1981) or by an active transport process, e.g., water
and glucose, in order for a successful gestation to occur. So, the
allantois and amnion do not simply play a passive role in protection
of the fetus and expansion of the chorioallantoic membranes. Because
of the roles and composition of the fetal fluids, they are active in
the mechanisms associated with embryonic survival (see Bazer and
First, 1983). Thus, cooperative interactions of the endometrium and
placenta are required for the developing embryo/fetus to receive
adequate nutritional/metabolic support.


27
In addition to requirements for maintenance of pregnancy,
maternal immunological tolerance of the antigenically dissimilar
conceptus must occur (for review, see Koch, 1985) Although the
conceptus possesses antigens on its surface which are accessible to
and frequently elicit responses from the maternal immune system,
pregnancy normally progesses with no adverse effects. Although the
mechanism of immunological tolerance is not well defined, Beer and
Billingham (1979) suggested that the following events occur during
pregnancy: (1) excess antigen shedding by trophoblast may lead to
blocking of T and B cell immune responses; (2) antigen-antibody
complex production during pregnancy may block T and B cell immune
response and (3) suppressor T lymphocyte production may be enhanced
during pregnancy. Data of Murray et al. (1978) suggest that uterine
secretions of pigs contain an immunosuppressive factor. Masters et
al. (1983) indicated that a large glycoprotein (Mr>660,000) secreted
by pig blastocysts may coat the conceptus and prevent maternal
lymphocytes from recognizing conceptus antigens. Recently, Murray et
al. (1987) identified a high molecular weight glycoprotein
(MW>660,000) purified from d 16 porcine conceptus culture medium that
had potent immunosuppressive effects. This was evidenced by
suppression of phytohemagglutinin and mixed lymphocyte-induced
blastogenesis of lymphocytes. In addition, the authors suggested
that this high molecular weight glycoprotein caused immunosuppressive
effects on anticonceptus immune responses by the mother while leaving
the systemic immune system unaffected.
As mentioned previously, pregnancy usually progresses with no
adverse affects from the antigenic incompatability. In some cases,


28
antigenic disparity might be advantageous for implantation and
continued intrauterine development (Gill and Repetti, 1979). Several
investigators have reported that number of conceptuses, placental
weights and fetal growth rates are higher in allogeneic versus
syngeneic matings (Billington, 1964; James, 1965, 1967; Beer and
Billingham, 1974; Beer et al., 1975).
In summary, numerous interactions between the conceptus and
maternal endometrium are required to assure proper growth,
implantation, nutritional support and immunological acceptance of the
conceptus. In spite of all the mechanisms designed to assure
maintenance of pregnancy, as will be reviewed in the next section,
the incidence of embryonic mortality is high in pigs.
Embrvonic/Fetal Mortality
Litter size is determined by ovulation rate, fertilization rate,
conceptus deaths during gestation and fetal deaths during the
perinatal period. Although ovulation rate can be increased by
nutritional means (Anderson and Melampy, 1972; Den Hartog and Van
Kempen, 1980; Dziuk and Bellows, 1983), greater embryonic death
losses during gestation generally occur so that litter size at birth
changes very little (Legault, 1978). In addition, as the incidence
of ovulation is increased via genetic selection or by gonadotropic
induction, less viable ova are produced (Koenig et al., 1986).
Developing hyperprolific lines such as Meishan pigs have led to
larger litters (Legault et al., 1981). However, an extensive system
of backcrossing with sows of more desirable growth and carcass traits
is required to enhance overall production successfully (Legault and
Caritez, 1983). In addition, the availability of hyperprolific


29
animals is limited. Heritability estimates of live pigs per litter
at birth range from .1 to .18 (Young et al., 1976; Legault; 1983).
Thus, selection for ovulation rate or litter size is not completely
practical. Therefore, the primary focus of this discussion will
concern embryonic mortality.
The majority of pregnancy wastage occurs before or during
embryogenesis and is referred to as embryonic mortality (Flint et
al., 1982). Rates of embryonic mortality, calculated by counting
embryos and using numbers of CL as a measure of the number of eggs
ovulated, usually range from 20 to 45% (see Flint et al., 1982). In
a study utilizing superovulated cows, some follicles were observed to
rupture and luteinize, but oocytes were not released (Monniaux et
al., 1983). Furthermore, fertility rates as well as the quality of
follicles and ovulations can also contribute to higher embryonic
mortality (see Terqui and Legault, 1984). Therefore, the number of
CL may not always represent the number of eggs shed (Terqui and
Legault, 1984) and embryonic mortality may be over-estimated.
However, in pigs, embryonic mortality estimates are usually in good
agreement with the number of CL and substantial loss due to embryonic
mortality does occur (Flint et al., 1982).
Numerous factors are associated with embryonic loss, including
chromosomal aberrations (Bishop, 1964). Based on karyotypes of
blastocysts recovered from pig uteri, McFeely (1967) and Day and
Polge (1968) suggested that 8 to 12% of fertilized eggs are abnormal
due primarily to polyspermy (which is likely to be lethal). Van der
Hoeven et al. (1985) indicated that this high percentage of
chromosomal abnormalities has not been confirmed. In agreement with


30
Van der Hoeven et al. (1985), Boyd (1965) reported that genetic
abnormalities account for only a small percentage (0 to 4%) of
embryonic mortality in domestic animals. Most losses due to
chromosomal abnormalities were reported to occur after d 10 (McFeely,
1967). Van der Hoeven et al. (1985) reported the karyotypes of 3- or
4-day-old pig embryos after short in vitro culture and confirmed that
a low frequency of chromosomal abnormalities exists in pig
conceptuses. This was true for both 10-day-old pig blastocysts
(Dolch and Chrisman, 1981) and 3- or 4-day-old embryos in which
hatching had not yet taken place (Van der Hoeven et al., 1985). Of
115 embryos cultured (3 to 4-day-old embryos), 80 were judged to be
of normal karyotypes. In contrast, Koenig et al. (1986) reported
25.1% of ova (8 to 32 h post-ovulation) are chromosomally abnormal.
Percentages of immature ova (70% of which never resumed meiosis)
ranged from 8.2 to 15.7%. Thus, Koenig et al. (1986) estimated that
a substantial portion of embryonic loss in swine could be accounted
for by chromosomal abnormalities and(or) ovulation of immature ova.
It is probable that certain boars (Perry and Rowlands, 1962) and
inbreeding (Squires et al., 1952; Rampacek et al., 1975) are
associated with greater losses due to genetic factors. As indicated
by Bazer and First (1983) because the genotype of the fetus and its
membranes is determined by both the dam and sire genotypes,
production of protein and steroid hormones by the placenta will be
unique. Since these hormones influence conceptus development and
survival in tero, certain sire-dam matings will have higher levels
of fertility and larger litter sizes. However, the effectiveness of
genetic selection for prolificacy in pigs at this time is limited


31
(for review see, Bichard and David, 1985; Johnson et al., 1985,
Legault, 1985).
Genes affecting early embryonic development have been identified
by Goldbard and Warner (1982). They reported that an H-2 associated
gene, named Ped (preimplantation embryo development) controlled
either fast or slow embryonic development in mice. Warner et al.
(1984) speculated that a slower rate of development was associated
with more embryonic mortality and indicated that this was true for
outbred strains of mice (e.g., CF1, a strain in which a population of
mixed morulas and blastocysts often indicates morulas are moribund)
(C. Warner, unpublished observations cited in Warner et al., 1984).
Furthermore, Warner et al. (1984) speculated that the Ped gene may be
biologically critical. For example, they raised the possibility that
more advanced pig embryos are the ones that survive to birth. In
addition, they wished to pursue whether domestic species have a
homologue to the mouse MHC associated Ped gene. Warner et al. (1986)
have since demonstrated the presence of MHC antigens on 2 to 4 cell
stage and blastocyst stage pig embryos. In addition, Conley et al.
(1987) reported that litters from either sows or boars with the d
haplotype were larger than for all other matings. The authors
concluded that although ovulation rate was higher in SLA sows
(swine MHC, haplotype d), an additional effect of the d haplotype on
embryonic survival was indicated by a significant effect of paternal
genotype on litter size. Thus, the Ped gene initially detected in
mice appears to be present in pigs as well. Recently, Warner et al.
(1988) indicated that the Ped gene product may be the Qa-2 antigen.
In addition, they indicated that although there is no known function


32
for any of the Q-region genes, Qa-2 antigens would be expected to be
expressed on preimplantation embryos possessing Qa-2a alleles but
not Qa-2^ alleles (Warner et al., 1987). Strains of mice
expressing the Qa-2 antigen produce embryos with the slow Ped allele
(Warner et al., 1988). Precisely how the Ped gene regulates
embryonic growth and(or) maternal immunological tolerance remains to
be determined.
It is recognized that pubertal gilts have greater embryonic
losses than multi-estrous pigs (Warnick et al., 1951; MacPherson et
al. 1977). Uterine capacity does not appear to be the contributing
factor. Up to d 30 of gestation, the gilt can accommodate
approximately twice as many fetuses as are normally present (Dziuk,
1968; Rampacek et al., 1975). Archibong et al. (1987) determined
that changes in the ratio of systemic levels of estrogen and
progesterone may be related to early embryonic mortality in gilts
bred at pubertal estrus. Embryonic survival in the study by
Archibong et al. (1987) was 78.1 vs 95.4% on d 15 and 66.7 vs 89.4%
on d 30 of gestation in gilts bred at the first vs the third estrus,
respectively. Although serum estrogen and progesterone were not
significantly different, the ratio of progesterone:estrogen was
higher on d 15 (439 vs 210) and d 30 (597 vs 179), but lower on d 3
(187 vs 444) of gestation for gilts bred at their first or third
estrus, respectively. It is possible that the low
progesterone:estrogen ratio on d 3 may have altered uterine secretory
activity and resulted in early embryonic death. The higher steroid
ratios at d 15 and 30 are probably due to a reduced number of
surviving conceptuses and reduced estrogen production by the placenta


33
after d 12 of gestation. Although further investigation will be
required, the altered steroid ratios may be involved in embryonic
loss in gilts.
It is well known that progesterone is required for the
establishment and maintenance of pregnancy in the pig. Furthermore,
it has been suggested that a deficiency of progesterone leads to
embryonic loss. Although it is generally assumed that the maternal
hormone profile is always appropriate for establishment of pregnancy,
Ashworth et al. (1984) suggest that naturally occurring levels of
progesterone can be inappropriate and as a result embryonic loss
occurs. Because of this, experiments have been conducted utilizing
progesterone supplementation as a protective measure (Flint et al.,
1982). Results have been inconsistent. Heap et al. (1984) suggest
that progesterone therapy reduces early embryonic loss in certain
circumstances, e.g., high environmental temperatures. However, Heap
et al. (1984) indicate that designing the appropriate dose and time
frame for supplementation is difficult because of the lack of
knowledge of the ways that progesterone supports early embryonic
survival. In addition, Heap et al. (1984) emphasize that it is not
yet known whether progesterone plays an obligatory or a permissive
role. These authors attempted to clarify the role of progesterone in
embryonic survival by utilizing passive immunization against
progesterone in early pregnancy in mice and reported multiple actions
of the antibody (Heap et al., 1984). When anti-progesterone
monoclonal antibody was given repeatedly to BALB/c mice as five daily
injections from the day of mating, implantation was blocked in all
six mice. Furthermore, few of the embryos of treated dams progressed


34
to the blastocyst stage and there was no indication of delayed
implantation. No remnants of degenerating conceptuses were detected
at autopsy on d 30 after copulation. The authors indicated that the
primary effect of the antibody was to arrest cleavage of embryos.
This effect was stated to occur during activation of the embryonic
genome. Based on these findings, Heap et al. (1984) stated that
progesterone production in the first 3 d after fertilization is
essential for normal embryonic development. Furthermore, they
indicated that one effect of progesterone is to provide a tubal
environment in which the embryos can develop at normal rates. Their
work is supported by results of Cline et al. (1977) who found that
estrogen dominated females had embryos with retarded development.
However, if progesterone was also supplied, embryonic development
proceeded at a normal rate. Thus, the possibility remains, as
indicated by Ashworth et al. (1984), that insufficient progesterone
production due to inadequate CL function can lead to increased
embryonic losses.
Other researchers have taken the approach that a combination of
exogenous progesterone and estrone will have a more beneficial effect
than progesterone alone on embryonic survival (Sheridan et al.,
1986). Knight et al. (1973) established that a 2000:1 ratio of
progesterone:estrogen was effective in inducing a synergistic effect
on uterine protein secretion in pigs. Although Knight et al. (1974a)
did not find a significant effect on embryonic survival following
steroid injections from d 4 to 15 of gestation, mean placental weight
and allantoic fluid volume increased when measured at d 40 of gesta
tion. Knight et al. (1974b) also demonstrated a negative effect of


35
doses higher than 50 mg progesterone and 25 ug estradiol per 45.4 kg
BW on uterine protein secretions. Since then, Wildt et al. (1976)
and de Sa et al. (1981) reported increased litter size following
combined injections of progesterone and estrone between d 14 to 23
and d 16 to 17 of gestation, respectively. However, since primarily
multiparous sows were in the treated group and primiparous were in
the control group, these results may be misleading. Recently,
Sheridan et al. (1986) reported results of administration of proges
terone (25 mg) and estrone (12.5 ug) on both d 16 and 17 or on either
d 16 or 17 of gestation. Gestation length was reduced and litter
sizes were larger at birth for steroid-treated sows. However, subse
quent litter size at weaning and interval from weaning to rebreeding
were not altered by treatment. Their results support the theory that
injection of progesterone and estrone at a 2000:1 ratio in
quanitities less than 50 mg progesterone and 25 ug estrone/45.4 kg BW
will effectively decrease embryonic mortality. Although Sheridan et
al. (1986) did not determine uterine secretory response or placental
growth in response to exogeneous steroid treatment, they suggested
that due to increased protein secretion or placental growth rate
previously reported by Knight et al. (1973), nutrient availability to
embryos increased and embryonic survival was enhanced.
In many countries, a period of lowered fertility exists in the
summer (see Claus and Weiler, 1985). Ledwitz-Rigby and Rigby (1987)
suggest that part of the decreased reproductive capacity of pigs in
summer may be due to decreased capacity for follicular development
within the ovary as a result of an altered endocrine signal. They
suggest that granulosa cell responsiveness to signals is altered by


36
photoperiod and(or) heat (such as decreased FSH; Mauget, 1982) which
results in a their decreased ability to secrete progesterone.
Conception rate is decreased in summer and tends to be elevated in
autumn and winter (Keindorf and Plescher, 1981; Britt et al., 1983;
Dobao et al., 1983; Mattioli et al., 1983). Mattioli et al. (1983)
and Love (1981) reported that a higher incidence of embryonic loss
occurs in the summer months (June-September). Problems due to timing
of artificial insemination or mating may be responsible for reduced
conception rates. It is known that duration of estrus is prolonged
during the summer (Signoret, 1967; Nauk and Sekrii, 1983). Reduced
farrowing rates due to embryonic loss has been reported (Stork, 1979;
Mattioli et al., 1983) with the highest incidence of abortions
detected in September/October for sows mated between June and
September. Litter size is higher after mating in autumn and winter
compared to summer (Tomes and Nielsen, 1979; Bevier and Backstrom,
1980; Keindorf and Plescher, 1981; Dobao et al., 1983; Mattioli et
al., 1983; Noguera et al., 1983; Aalbers et al., 1984). According to
Bevier and Backstrom (1980) and Mattioli et al. (1983), litter size
for sows mated in the summer is usually reduced by 1 piglet or more
compared to that for sows mated in autumn or winter. Concentrations
of progesterone in early pregnancy (dlO to 60) are lower (21.5 vs
32.4 to 40.3 ng progesterone/ml plasma) in August-September than in
all other months (Beilanski and Kremer, 1983). Seasonal influences
on the weaning-to-estrus interval may be removed by imposing
conditions of decreased photoperiod in summer (Claus et al., 1984).
However, effects of reduced photoperiod on litter size, embryonic
mortality and conception rates have not been reported. It appears


37
that sensitivity to photoperiodic stimuli present in wild pigs
(Mauget, 1982) may not have disappeared completely in domestic pigs
(Claus and Weiler, 1985). However, Claus and Weiler (1985) indicate
that interactions between photoperiod and embryonic/fetal survival
need to be clarified. In addition, this author suggests that effects
now attributed to photoperiod are also due, in part, to temperature
variations.
Environmental factors such as elevated ambient temperature are
also known to influence embryonic mortality (Wettemann et al., 1984;
Wettemann and Bazer, 1985). Although the following discussion deals
with effects of heat stress, it is relevant to the overall discussion
on embryonic mortality. For example, altered endocrine function in a
non-heat stressed sow may also lead to the loss of embryos. Thus, an
overall understanding of factors associated with embryonic survival
can be gained by studying this model.
Wettemann et al. (1984) indicated that heat stress of male swine
results in a decrease in fertilization rate. Furthermore, increased
embryonic mortality occurs when gilts are artificially inseminated
with extended and stored semen from heat stressed boars. However,
when heat stressed boars are naturally mated, conception rate, but
not litter size, is altered (Wettemann et al., 1976, 1979). Heat
stress of gilts prior to breeding did not influence ovulation rate or
embryonic survival (Edwards et al., 1968). However, heat stress
during the intervals from 1 to 15 days (Edwards et al., 1968) or 0 to
8 days (Omtvedt et al., 1971) after breeding reduced conception rate
and litter size when measured at d 30. Kreider et al. (1978)


38
reported that plasma progesterone increased and estradiol decreased
following heat stress of gilts from estrus until d 8 of gestation.
When gilts were exposed to elevated ambient temperatures from d 8
to 16 after breeding, decreased conception rates and reduced litter
size were detected at d 30 of gestation (Omtvedt et al., 1971). In
addition, Omtvedt et al. (1971) suggested that the implantation
period may be the most susceptible to heat stress. Wettemann et al.
(1984) reported effects of heat stress between d 8 to 16 after
breeding on concentrations of progesterone, corticoids and estradiol
in plasma. Luteal function, as measured by progesterone production,
was not altered between days 9 through 28 of pregnancy by heat stress
in those gilts that maintained preganancy. However, in heat
stressed, nonpregnant gilts on d 13 to 19 after estrus, concentra
tions of progesterone were reduced in comparison to nonpregnant
control gilts and all pregnant gilts. Yet, by d 25, progesterone in
plasma of heat stressed, pregnant gilts had not decreased to
concentrations usually present at d 25 of pregnancy. Wettemann et
al. (1984) suggested that prolonged luteal regression occurred in
these gilts following maternal recognition of pregnancy and subse
quent embryonic mortality. Polge et al. (1966) previously reported
an extended luteal phase and estrus on approximately d 26 after
breeding in gilts with less than 4 embryos on d 12 of pregnancy.
Concentrations of estradiol in plasma in gilts heat stressed from
d 8 to 16 after breeding were greater compared to control nonpregnant
and all pregnant gilts on d 10 to 12 after estrus. Thus, the
increase in estradiol preceeded the decrease in progesterone.
Wettemann et al. (1984) suggested that because the increase in


39
estradiol occurred in heat stressed gilts prior to the normal
initiation of blastocyst synthesis of estrogens, improper timing of
steroidogenesis may have caused detrimental effects on conceptus
development.
Support for this theory has been generated by Morgan et al.
(1987a). Exogenous estradiol treatment on d 9 of pregnancy resulted
in advanced uterine secretory response. This was evidenced as
increased calcium, protein and acid phosphatase levels in uterine
flushings of pregnant gilts unilaterally hysterectomized on d 11.
Following removal of the remaining uterine horn on d 12, increased
protein and acid phosphatase and decreased calcium and PGF were
reported in the estradiol- treated gilts. However, in a second
experiment (Morgan et al., 1987a), exogenous estradiol followed by
hysterectomy at d 16 revealed no differences in calcium, PGF or
protein and decreased acid phosphatase. Blastocysts were fragmented
and degenerating on d 16 in these estradiol- treated gilts, although
they appeared normal in the previous trial at d 12. Collectively
these data suggest that early estradiol exposure in the uterus
advances uterine secretory response and, although blastocyst
elongation occurs, blastocysts fail to survive to d 16. Geisert et
al. (1987) previously indicated that loss of progesterone support was
not responsible for embryonic mortality observed in estradiol-
treated gilts. In addition, estradiol is not directly embryocidal
(Pope and First, 1985) since gilts maintain pregnancy when estrogen
is administered after d 11. Therefore, Morgan et al. (1987a) suggest
that failure of blastocyst attachment is the result of premature
estradiol action on uterine secretions and(or) surface proteins.


40
Thus, as Wettemann et al. (1984) suggested, alteration of the
hormonal sequence which influences the endometrium is detrimental to
embryonic survival.
Wettemann et al. (1984) also studied the response to exogenous
adrenocorticotropin hormone (ACTH) in heat stressed (from d 8 through
d 16 after breeding) versus control pregnant and nonpregnant gilts.
Concentrations of corticoids and progesterone (during the first 2 h
after ACTH) were reduced in heat stressed nonpregnant gilts. Marple
et al. (1972) previously reported that gilts and barrows exposed to
elevated ambient temperatures had increased ACTH concentrations in
plasma. The combined results suggest that heat stress may alter
adrenal steroid secretion. Wettemann et al. (1984) indicate that
endogenously, excessive ACTH may have the same effect on steroids as
seen following exogenous ACTH treatment. Therefore, altered adrenal
activity may decrease embryonic survival either by lowering
concentrations of necessary steroids or by stimulating greater
production of steroids which have detrimental effects. Two lines of
evidence support their suggestion. First, Tilton et al. (1972)
reported that adrenalectomy may prevent embryonic mortality induced
by heat stress of sheep. Secondly, Howarth and Hawk (1968) reported
that injection of ewes with hydrocortisone acetate resulted in
decreased embryonic survival.
Wettemann et al. (1984) also reported the effects of heat stress
from d 8 through d 16 after breeding on embryonic and uterine
responses. The amount of embryonic tissue present at d 16 was less
for heat stressed gilts. However, protein synthetic ability, as
measured by amount of labelled leucine incorporated into


41
macromolecules by conceptus tissue, was not altered when
incorporation was adjusted for dry weight of conceptus tissue.
Similarly, on d 16, total protein and PGF content per uterine flush
were similar for heat stressed and control pregnant gilts. In
addition, uterine endometrial function at d 16 after estrus was not
altered by heat stress, as indicated by similar dry weight of tissue
and incorporation of leucine into macromolecules by uterine
explants. Furthermore, steroidogenesis by conceptuses and uteri were
not altered by heat stress, as measured by total amounts of estrogens
in uterine flushes on d 16 after breeding.
Significant effects of heat stress on concentrations of the
metabolite of PGF, 13,14-dihydro-15-keto-prostaglandin (PGFM),
composition of blood gases and blood flow to the uterus were not
detected (Wettemann et al., 1984). However, concentrations of
prolactin in plasma were elevated in gilts exposed to higher ambient
temperature following breeding (d 8 to 16) (Wettemann and Bazer,
1985). The authors indicated that the precise role of these factors
in embryonic mortality was not readily apparent (Wettemann and Bazer,
1985), but could not rule out the possibility of their importance.
Putney et al. (1987) indicated that increased embryonic mortality
in cows may result from alterations in signals between the conceptus
and maternal endometrium necessary for maintenance of pregnancy.
Heat shock (39 C for 6 h; 43 C for 18h) reduced (54.2%) protein
secretion of conceptuses, and in particular, decreased (74.3%)
conceptus secretion of bovine trophoblastic protein-1 in comparison
to control (39 C for 24 h) conceptuses. However, protein secretion
by endometrial explants was not altered. In addition, a 1225%


42
increase in endometrial PGF2a]_pha secretion was detected in
response to heat shock. Endometrial PGE2 production and secretion
of prostaglandins by conceptus tissue were not significantly
altered. An analagous situation to that for heat shock in the bovine
(Putney et al., 1987) may occur in porcine conceptus-endometrial
interactions in response to heat stress.
Elevated ambient temperatures during d 53 to 61 of gestation did
not influence conception rate, litter size, piglet birth weights or
survival rates (Omtvedt et al., 1971). However, heat stress during
later gestation (d 102 to 110 of gestation) increased fetal mortality
(Omtvedt et al., 1971). Wettemann and Bazer (1985) emphasize that
during late gestation the requirements of the fetal-placental unit
for estrogen, nutrients, and gaseous exchange are great. Therefore,
conditions leading to deficiencies during late gestation may result
in fetal death. In contrast, during mid-gestation, heat stress may
not be detrimental because the fetus is only about 10% of birth
weight and fetal-placental steroidogenic function (Knight et al.,
1977) is minimal compared to late gestation (Wettemann and Bazer,
1985) .
In summary, Wettemann et al. (1984) demonstrated that exposure of
swine to elevated ambient temperature during early gestation leads to
lower conception rates and litter sizes. Wettemann et al. (1984)
emphasized that concentrations of steroid hormones control uterine
secretions (Knight et al., 1973; Bazer, 1975) and can alter transport
of ova, embryos and sperm (Chang, 1966; Hawk and Conley, 1971; Hawk,
1975). Therefore, it is possible that heat stress alters conception
rate or embryonic survival indirectly via the endocrine system or


43
through direct effects on the gametes or embryos (Wettemann et al.,
1984). Although these studies were conducted to determine effects of
elevated ambient temperature, it is possible that factors associated
with embryonic mortality in heat stressed animals may be induced by
other conditions and also result in embryonic loss.
The effects of migration, distribution and spacing of pig embryos
on pregnancy and fetal survival have been reviewed by Dzuik (1985) .
Dziuk (1985) indicated that embryonic survival is not influenced by
uterine space prior to d 30. It is essential that a minimum of 4
conceptuses occupy the uterus at d 12 for pregnancy to be maintained
(Polge et al., 1966). Furthermore, the proportion of the uterus that
is occupied is inversely related to the probability that pregnancy
will continue (Dhindsa and Dziuk, 1968). Proper spacing must occur
prior to d 12 (Dziuk, 1985). Furthermore, prenatal growth and
survival of fetuses is greatly influenced by spacing and migration of
embryos (Webel and Dziuk, 1974; Anderson and Parker, 1976; Pope and
First, 1985). Because some embryos die between d 13 and 40 of
gestation, gaps between fetuses result since attachment takes place
at d 12 (Dziuk, 1985). In addition, the distribution and spacing of
embryos is not apparently uniform thoughout the length of the
uterus. At d 40 of gestation, the greatest space available to each
fetus was at the tip of the horn and near the uterine body, with the
least available space in the middle of each horn (Hentzel et al.,
unpublished results, cited by Dziuk, 1985). Dziuk (1985) suggested
that this spacing results from death and partial resorption of
embryos initially crowded near the uterine body. Although uterine
space available to each embryo had little influence on embryonic


44
survival prior to d 25 to 30, in later gestation (d 70) few fetuses
survived in the crowded segments according to Dziuk (1968). Dziuk
(1985) suggested that optimum conditions for litter size, fetal
growth and survival involve uniform distribution of embryos with each
occupying 20 cm of space. He also emphasized that it is imperative
that migration, spacing and distribution be equitable very early in
gestation to maximize survival.
Koch (1985) discussed immunological implications of pregnancy in
the pig. Because cells of all higher vertebrates possess
histompatibility antigens on their surface, some mechanism has
evolved to allow for immunological acceptance of the conceptus by the
maternal immune system (Koch, 1985). It has been demonstrated that
the uterus is not a privileged site for survival of conceptuses in
various species including the pig, by continued development of
trophoblastic tissue when transplanted to ectopic sites (Samuel,
1971). In pigs, the major histocompatability complex is the swine
lymphocyte antigen (SLA) complex (Vaiman et al., 1970; Viza et al.,
1970). The SLA complex is responsible for discrimination of self and
non-self and must be dealt with for successful pregnancies to occur
in swine. Although spermatozoa, seminal plasma and tissues of the
conceptus represent sources of antigenic material, embryonic tissues
are considered to be the primary immunological challenge (Koch,
1985). One hypothesis proposed to explain the non-rejection of the
feto-placental unit is the masking of transplantation antigens on the
conceptus. A general suppression of the immune response during
pregnancy has also been suggested. In addition, antigenic disparity
between the mother and conceptus in certain circumstances may be


45
beneficial for implantation and continued intrauterine development
(Gill and Repetti, 1979). However, Koch (1985) indicates that the
precise nature of the maternal immune response towards the conceptus
is not known. None the-less, it is imperative that the proper
immunological relationship exist between the fetus and mother or
embryonic mortality will result.
Ford and Stice (1985) have evidence of interactions between pig
conceptuses and uterus affecting uterine blood flow previously
described by Ford and Christenson (1979). Results from numerous
studies suggest that pig conceptuses, through catechol estrogen
production, increases arterial distensibility locally, resulting in
increased baseline blood flow to each fetal-placental unit. However,
contractility of the uterine arterial vasculature to adrenergic
agonists or other vasoactive agents is not affected. This allows
conceptuses to maintain locally elevated blood flow required for
their survival. Simultaneously, the maternal system responds to
life-threatening stimuli by transiently rerouting blood flow away
from the uterus and towards other vascular supplies necessary for
maternal survival (Ford and Stice, 1985). A malfunction in this
system could result in embryonic/fetal death.
As reviewed by Bazer and First (1983), the developing conceptus
may, in part, control its own destiny via the synthesis of certain
compounds. It had previously been postulated that litter size is, in
part, limited by the availability of an essential biochemical factor
(Bazer, 1975). Most embryonic mortality in pigs has been reported to
occur prior to d 12 of gestation (Perry and Rowlands, 1962). Bazer
and First (1983) indicate that loss of pregnancy may be a function of


46
conceptus rather than maternal deficiencies. This may explain why
some embryos survive while others die within the same uterine
environment in polytocous species (Bazer and First, 1983). Thus, if
blastocysts do not develop and elongate at an adequate rate, they
fail to produce compounds critical to their own survival (Bazer and
First, 1983).
One of these necessary signals in the pig is estrogen, which is
produced by the pig blastocyst beginning on about d 11 of gestation
(Geisert et al., 1982b). Estrogen is required to ensure CL
maintenance (Bazer and Thatcher, 1977), and nutrient availability
through stimulation of histotroph secretion (Geisert et al., 1982b)
and increased uterine blood flow (Ford and Christenson, 1979) .
Numerous reviews describe substances produced by the endometrium
and blastocyst which may allow interactions between the conceptus and
endometrium required for embryo survival (Flint et al., 1982; Bazer
and Roberts, 1983; Bazer et al., 1986). At this time, there is no
conclusive immunoelectophoretic or chromatographic evidence for
pregnancy-specific endometrial proteins involved in stimulating
blastocyst growth. However, Flint (1981) suggests that blastocyst
estrogens control secretion of endometrial embryotrophic factors
which should be considered further. If growth promoting substances
are secreted by the endometrium, competition for growth factors may
be involved in deciding which embryos are lost (Flint et al., 1982).
Therefore, conceptuses which elongate first may obtain a higher
proportion of available growth-supporting substances and deprive
those elongating later (Flint et al., 1982).


47
There is considerable variation in blastocyst size during the
time of elongation (Anderson, 1978). As reviewed by Wilmut et al.
(1985), relatively retarded embryos are much less likely to survive
than synchronous embryos or embryos advanced by up to 24 h (Webel et
al., 1970; Polge, 1982). Thus, factors that advance embryonic growth
or are inherent in an embryo make the advanced embryo much more
likely to survive in the uterine environment of a single sow (Wilmut
et al., 1986) .
Pope et al. (1982a) reported that more developed embryos have an
advantage over less developed embryos when a 2 d range in age and
development was tested. More recently, Pope et al. (1986b) examined
this in embryos within a closer range of development. Utilizing
asynchronous superinduction to test the range of blastocyst
development on embryonic survival in swine, Pope et al. (1986b)
reported the following. When the proportion of less developed
embryos within a litter increased, subsequent mortality also
increased during the first 30 d of gestation. Thus, naturally
occurring variation in stage of embryonic development might explain
some of the loss. This is in agreement with conclusion of Wilmut et
al. (1986) who reviewed factors contributing to embryonic loss and
indicated that variation in stage of embryonic development can be
sufficient to prejudice survival in polytocous species. In another
study lending support to this theory, Morgan et al. (1987b) tested
effects of estradiol treatment on d 11 in synchronous and
asynchronous (blastocysts 24 h behind recepient uterus) gilts and
compared to control asynchronous gilts. Embryos were recovered in
uterine flushings on d 14. Only in the asynchronous,


48
estradiol-treated group did blastocysts fail to develop. Acid
phosphatase activity was higher and amount of calcium recovered was
lower in both the asynchronous and synchronous estradiol-treated
gilts. Thus, estradiol advanced uterine secretory activity. Morgan
et al. (1987b) indicated that this effect was embryocidal to embryos
that are behind in their development, since neither asynchrony or
estradiol itself resulted in embryonic loss. Furthermore, results of
Morgan et al. (1987b) indicate that blastocysts left to develop at
their own rate stimulate uterine environmental changes at the onset
of elongation and allow blastocyst development to proceed normally.
Thus, the uterus appears to play a permissive role with blastocysts
regulating appropriate uterine responses (Morgan et al., 1987b).
Morgan and co-workers (1987b) also indicated that immature
blastocysts may not possess receptors to recognize changes in
regulatory proteins of uterine origin either released by the
endometrium or exposed on the uterine surface epithelium after
estrogen stimulation. Therefore, immature blastocysts do not undergo
developmental changes required for survival. In summary, three
possibilities have been suggested to account for embryonic loss in
gilts with advanced uterine secretion due to estradiol
administration: (1) inability of blastocysts to elongate; (2) altered
uterine surface epithelium and (3) a direct embryocidal effect of the
uterine environment. These studies clearly demonstrate that
blastocysts must attain a degree of morphological maturation before
they can respond to and survive in the altered uterine environment
normally induced by estrogen on d 11 to 12 of gestation. Although
these conditions were experimentally induced (Morgan et al., 1987b),


49
there is normally a high degree of variation in morphological
maturity between conceptuses within the same uterus. Failure of
immature conceptuses to survive the change in intrauterine
environment induced by faster developing conceptuses may be a signi
ficant factor contributing to embryonic death losses in pigs. When
conceptuses within the same uterus are similar in development, each
may have a greater ability to respond to the uterine environment and
greater chance for survival. Evidence for this was obtained from a
study of conceptus development in prolific Chinese Meishan gilts
(Bazer, 1987). In comparison to less prolific breeds, Meishan have
less variation in conceptus development between d 8 to 14 of gesta
tion and rate of development between d 11 and 12 of gestation was
faster. These results suggest that minimizing variation among con
ceptuses may be part of the mechanism by which Meishan pigs produce
larger litters. The larger litters do not result from higher ovula
tion rates, but factors associated with higher embryonic survival.
In summary, neither fertilization failure (Robertson et al.,
1951a; Squires et al., 1952; Day et al., 1959; Spies et al., 1959;
Perry and Rowlands, 1962) or chromosomal aberrations (McFeeley, 1967;
Lupse, 1973), insufficient luteal development (Webel et al., 1975) or
insufficient uterine space (Webel and Dziuk, 1974) explain all of the
30% loss of potential embryos common to swine. In addition, no
single factor can explain embryonic loss or be manipulated to
adequately alter embryonic survival (Bazer and First, 1983).
Genetic, nutritional, environmental, disease and endocrine factors
all can lead to embryonic/fetal death. In a later section,
nutritional factors affecting embryonic/fetal loss, litter size and
postnatal survival will be reviewed.


50
Effects of Nutrition or Manipulation of Metabolism of Sows
During Gestation on Embryonic Survival. Litter Size
and Sow and Litter Performance During Lactation
Numerous factors must be considered when formulating a gestation
diet, i.e., feeding recommendations for gilts are much different than
those for sows. Gilts are now bred at young ages and leaner pork is
being produced resulting in lower body fat at breeding. Brooks
(1982) suggested that because the loss of body fat of sows during the
first 2 or 3 farrowings is great, either body fat of gilts should be
increased prior to the first farrowing to provide fat for later
depletion or sows should be fed to avoid body fat depletion. Brooks
(1982) indicated that increasing body fat prior to the first
farrowing is not practical for two reasons: (1) increased feed intake
during pregnancy reduced voluntary feed intake during lactation (Dean
and Tribble, 1961; Salmon-Legagneur and Rerat, 1962; Baker et al.,
1969) and (2) among gilts that receive the same gestation allowance
there is a tendency for those which farrow at heavier weights to lose
more weight during lactation (Brooks and Cole, 1973; Brooks and
Smith, 1980). Thus, it is more practical to maintain body fat by
providing adequate feed allowances from the first farrowing onward.
This may reduce the problem of lower ovulation rates frequently
encountered in gilts having become catabolic during lactation
(Brooks, 1982).
Cole (1982) indicated that sows do not reach reproductive
maturity until about their fourth parity. The most prolific period
will extend beyond that. Therefore, nutritional considerations
should be for more than just short-term. Cole (1982) emphasized that
nutrition impacts on reproductive performance of sows in the


51
following ways: (1) short term reproductive performance evaluated by
how nutrition during pregnancy affects litter size, lactation and
weights of piglets and sows at weaning; (2) performance during the
subsequent pregnancy affected by nutrition during lactation and (3)
long term reproductive performance as influenced by nutrition in
early stages of their reproductive lives. Thus, long term plans
should be developed. In general, diets are designed to conserve body
condition during lactation. Since greater weight gains during
pregnancy result in greater losses in lactation, limited weight gains
in pregancy are desirable (see Cole, 1982).
Nutrition of the breeding pig is not the only consideration,
however. Since piglets are born with limited energy reserves, diets
fed during gestation are formulated to increase fetal glycogen
stores. In addition, attempts are being made to reduce embryonic
death losses through altered nutrition. Because of these different
goals, determination of nutrient requirements for sows is difficult.
Lewis and Reese (1986) listed additional factors which make
formulating diets for sows difficult. First, sows reproduce well
during periods of nutrient deficiency by drawing on their own body
reserves. Pregnants sows have considerably greater feed efficiency
than nonpregnant females (Salmon-Legagneur and Rerat, 1962). Second,
large numbers of sows must be utilized to draw conclusions because
variability in reproductive traits is great. Third, carry-over
effects from pregnancy to lactation and to the next gestation must be
considered. None-the-less, nutrient requirements for sows during
gestation are being determined which will allow maximum reproductive
performance.


52
Influences of Nutrition Prior to Breeding or During Early Gestation
on Embryonic Survival
Feeding recommendations during early pregnancy are not well
established. In a number of cases, embryonic survival has not been
associated with feeding level (Cole, 1982). Dutt and Chaney (1968)
reported higher embryonic survival in sows fed reduced dietary energy
from mating to d 20 of gestation. However, ranges for feed intake
were too broad (1.25 to 4.1 kg/d) to provide practical information.
Dyck and Strain (1980) confirmed reports of higher embryonic survival
when feed intake was reduced from 2.5 to 1.5 kg/d from mating to d 10
of gestation. However, conception rates were reduced in gilts fed
less from mating to d 30 of gestation. As reviewed by Christenson
(1986), continuous ad libitum feeding of gilts before breeding and
during early gestation increased embryonic mortality in comparison to
pigs on restricted feeding (Robertson et al., 1951b; Self et al.,
1955; Gossett and Sorenson, 1959; Haines et al., 1959; Sorenson et
al., 1961). However, a more recent study of nutritional effects on
embryonic survival indicated that actual embryo numbers present were
similar between groups (Den Hartog and Van Kempen, 1980). Other
researchers failed to confirm an effect of high energy intake on
early embryonic survival in multiparous sows (McGillivray et al.,
1964; Christenson and Zimmerman, 1966; Heap et al., 1967; Toplis et
al., 1983). Toplis et al. (1983) indicated that differences in
embryonic survival previously reported following increased feed
intake were primarily found in primiparous sows and may result from
"flushing" and increased ovulation rate (Anderson and Melampy, 1972;
Den Hartog and Van Kempen, 1980). It is not clear by what
mechanism(s) dietary energy levels exert their effects on embryonic


53
survival in swine other than through increased ovulation rate. Bazer
et al. (1968) demonstrated that rates of embryonic survival of gilts
fed ad libitum for 14 d prior to breeding were reduced not due to
embryo viability or overcrowding, but rather to some uterine factor
which limited litter size. In trials in which embryonic survival was
decreased, reduced concentrations of progesterone in plasma may be
part of the cause. Increased feed or protein intake during early
gestation in dairy cows or gilts has been associated with decreased
concentrations of progesterone in plasma (Jordan and Swanson, 1979;
Dyck et al., 1980).
Evaluating embryonic mortality between d 20 to 30 of gestation
may lead to improper recommendations. Etienne et al. (1983) reported
levels of embryonic mortality of 18 to 33%. However, at d 105,
differences between treatments for fetal mortality were reversed, and
thus, there were no net differences. In summary, nutritional effects
on embryonic survival are not clear. Few studies have led to
conclusive results, so recommendations other than avoiding severe
deficiencies or excesses during early gestation are difficult.
Christenson (1986) recommended that producers restrict feed after
mating, in part, to reduce feed costs and also to decrease embryonic
death losses.
Recently, through a series of cooperative experiments, (F. W.
Bazer and M. T. Zavy, personal communication) effects of
supplementing gestation diets with riboflavin were observed during
early gestation. Endogenous riboflavin increases in uterine
flushings of cyclic and pregnant gilts between d 6 and 8 after onset
of estrus and then decreases to undetectable levels by d 11.


54
Exogenous riboflavin increased levels of riboflavin in uterine
flushings. Pregnant gilts receiving 100 rag riboflavin per day on d 4
to 10 of gestation had increased numbers of live embryos, higher
embryonic survival and greater allantoic fluid volumes at d 30. In a
subsequent trial with 48 control and 51 riboflavin treated
primiparous sows, total number of piglets and piglets alive at birth
tended (P < .11, P < .09, respectively) to be higher and piglets
alive at d 21 and 42 were greater (P < .05). At d 21 and d 42, total
weight of piglets was greater for riboflavin fed sows.
Effects of Nutrition During Mid- or Late-Gestation on Piglet Birth
Weight and Survival
Numerous authors have reported effects of severe feed deprivation
during late gestation (Pond et al., 1968a,b; 1986; Ezekwe and Opoku,
1986; Speer, 1982). Speer (1982) reviewed evidence that low protein
(.5 to 2%), protein-free diets or complete inanition resulted in no
adverse effects on embryonic/fetal development or litter size,
although birth weights were in some cases decreased. Pond et al.
(1986) demonstrated that primiparous gilts can maintain pregnancy
during feed restriction. Primiparous sows were restricted to
one-third of the recommended (NRC, 1979) feed allowance from d 84
through d 108 of gestation. Although effects on fetuses warrant
further research (Pond et al., 1986), litter size was not affected
and piglet birth weight was decreased by 13% in gilts fed the
restricted level (.6 kg/d) (Pond et al., 1986). These results
confirm previous reports by Pond et al. (1968a,b; 1969) in which
protein free diets were fed for various intervals during gestation
and pregnant gilts utilized body stores of nutrients to meet fetal
demands. Recently, Ezekwe and Opoku (1986) demonstrated that feed


55
deprivation (complete starvation for 7 or 14 d prior to farrowing)
did not cause permanent growth retardation of progeny. Litter size,
birth weight, weaning weight, mortality at birth and survival to
weaning of piglets were not altered by starvation of sows. Thus,
feed deprivation for short periods may reduce feed costs. However,
long term effects or effects in the subsequent reproductive phase
were not determined. In other studies, severe protein and(or) energy
restriction during both gestation and lactation decreased the number
of sows returning to estrus after weaning, increased the interval to
estrus and decreased ovulation rates (Holden et al., 1968; Svajgr et
al., 1972; Pike and Boaz, 1972; Hovell and MacPherson, 1977).
Amounts of protein required during gestation are greatly
influenced by the level of protein available during the subsequent
lactation. Mahan and Mangan (1975) indicated that sows fed 9, 13 or
17% protein diets during gestation performed similarly during
lactation if lactation protein levels were adequate. When 18%
protein lacation diets were supplied, no differences in sow or litter
performance were detected. However, if 12% protein was fed during
lactation, litter weights increased most for sows fed the higher
protein levels during gestation. Mahan (1977) reported no difference
in litter size between sows fed gestation/lactation diets of 14/15
versus 8.5/20 percent protein. However, milk production was less for
the 8.5/20% fed sows. Greenhalgh et al. (1977) fed either 9, 11, 13
or 15% protein during gestation followed by 13 or 17% protein during
lactation. Number of total and live piglets born increased, but not
significantly, with ingestion of greater protein during gestation.
Greenhalgh et al. (1980) indicated no difference in piglet weight or


56
litter size at birth due to diets containing 9 or 11% protein during
gestation followed by 13, 15, 17 or 19% protein during lactation.
Feeding either 9 or 15% protein during gestation and 12, 16 or 20%
protein during lactation increased average piglet weight and number
of piglets born, but differences were not significant (NCR-42
Committee on Swine Nutrition, 1978). In summary, sows can withstand
protein deprivation during pregnancy without adverse effects on
litter size at birth. This may be due to the greater ability of
pregnant versus nonpregnant sows to retain nitrogen
(Salmon-Legagneur, 1965; Heap and Lodge, 1967). However, results are
controversial for the effects of long term protein deprivation on
litter size and piglet weight at birth. In addition, protein
deprivation may decrease milk production of sows, but not if adequate
nutrients are supplied during lactation. O'Grady (1985) indicated
that there is agreement that reproductive performance (number, weight
and composition of piglets born/litter) is maximized when 140 to 180
g crude protein/sow is provided during pregnancy and amino acid
requirements are met. Estimated requirements for lysine vary from .4
to .65% of the diet. Estimates of requirements for other amino acids
during pregancy are also available (Cole, 1982; NRC, 1979). Because
different energy sources have different amino acid values and(or)
digestibilities, levels of protein and specific amino acids required
will vary (Maxwell et al., 1987).
Substantial evidence indicates that piglet survival during
lactation is positively correlated with piglet birth weight. Hall et
al. (1984) clearly demonstrated the importance of piglet birth weight
on survival in a study representing over 10,000 pigs. For piglets


57
averaging .45, .68, .91, 1.14, 1.36 or 1.59 kg at birth, the survival
rates (%) were 16, 39, 59, 74, 86 and 95%, respectively. Therefore,
during the last trimester of gestation, researchers have attempted to
increase fetal fat reserves and(or) piglet weight by altering the
diet and(or) metabolism of sows. Swine are born with extremely
limited energy stores in the form of adipose tissue lipids (Mersmann,
1974). Ramsay et al. (1987) reported that central endocrine
regulation has an important function in the development of porcine
fetal adipose tissue metabolism. On d 45 of gestation, spinal
cautery or decapitation was performed in fetuses within one horn,
with the other horn serving as a control. Fetuses were removed on d
110 of gestation and subcutaneous adipose tissue was incubated to
assess metabolic responses to insulin on glucose oxidation or
lipolytic response induced by norepinephrine (NE) bitartrate and
measured by glycerol release. Only decapitated fetal adipose tissue
demonstrated an insulin stimulation of glucose oxidation and
lipogensis. However, NE stimulated lipolysis in fat from cauterized
and control, but not decapitated fetuses. Ramsay et al. (1987)
concluded that the absence of a NE-stimulated lipolytic response in
decapitated fetal tissue demonstrated that central endocrine
regulatory factors control fetal adipose tissue lipolysis.
Furthermore, they indicated that fetal pig adipose tissue is a
consequence of beta-receptor development in response to systemic
hormones controlled by central endocrine regulatory factors. The
inability of spinal cautery to alter glucose metabolism or
responsiveness to insulin stimulation in fetal adipose tissue
indicated that central neural mechanisms did not affect glucose


58
metabolism in fetal adipose tissue. Rather, changes in adipose
tissue of decapitated pigs reflected changes in fetal endocrinology.
Kasser et al. (1983) suggested that the absence of or decrease in
insulin-anatognistic hormones in decapitated pigs during gestation
permitted devlopment of insulin sensitivity in fetal adipose tissue.
Furthermore, Walton and Etherton (1986) reported that GH antagonized
insulin sensitivity of swine adipose tissue. Martin et al. (1985)
found that decapitatation decreased GH concentrations which would
alter insulin responsiveness or receptor concentrations. Either
factor resulted in increased body lipid deposition in decapitated
fetuses (Kasser et al., 1983). Therefore, promotion of fetal lipid
storage may depend on the ability to stimulate or inhibit release of
central endocrine regulatory factors (Ramsay et al., 1987). This
fact should be considered when attempting to increase fetal energy
reserves during gestation.
In a series of experiments, Cline and co-workers reported that ad
libitum feeding with or without 5% soybean oil from d 105 of
gestation until parturition did not alter survival of piglets from
birth to weaning (Massarotti and Cline, 1984; Sterling and Cline,
1986; Lima and Cline, 1987). However, ad libitum feeding and soybean
oil inclusion in the diet increased milk production and heavier
weaning weights of piglets were sometimes detected. Cromwell et al.
(1982) increased feed intake (1.82 to 3.18 kg/d) of sows from d 90
until term and reported increased (+.05 kg) average piglet weight and
greater piglet survival (85.4 vs 87.8%). However, Lewis and Reese
(1986) summarized results of numerous experiments and reported little
or no benefit of additional feed intake late in gestation on piglet


59
survival. They concluded that when piglet birth weights average
greater than 1.4 kg, they will not likely be increased by dietary
factors. Cromwell (1980) presented results of increased energy
intake of sows from over 5000 litters indicating that piglet birth
weights increased by approximately .02 and .05 kg in gilt and sow
litters, respectively for each additional .05 kg of feed consumed.
Although it is desirable to increase birth weights of piglets, it
is necessary to increase sow feed comsumption greatly to elicit small
increases in piglet birth weights. Most researchers recommend
pregnancy weight gains of 10 to 40 kg (O'Grady, 1985). Since, as
indicated previously, maternal weight gains during pregnancy are
deleterious during the subsequent lactation, an optimum level of feed
intake for both fetal and maternal weight gains should be used.
Feeding levels should be adjusted for age, body condition, ambient
temperature, housing, expected low average birth weights and current
feed costs. Diets for gestating sows (with BW of 140 kg) are
recommended to provide 25 Mega Joules (MJ) digestible energy (DE)/d,
e.g., 1.8 kg/d of a corn soybean meal diet.
In addition to providing more energy by increasing overall
consumption, researchers have reported beneficial effects of adding
fat to diets of sows during late gestation and(or) lactation (see
Pettigrew, 1981; Moser, 1985). Moser and Lewis (1980) summarized
results of numerous experiments, performed in the 1970s and 1980s,
which evaluated effects of fat added to sow diets on piglet
survival. Type of fat (corn oil, soybean oil, tallow, lard), level
of fat (2 to 40%) and number of days of feeding fat (5 to 135)
varied. As reviewed by Moser (1985), almost all data indicated that


60
fat content in colostrum and milk of sows was increased in sows fed
fat. Controversial results were obtained for piglet survival and
litter size at weaning. However, Moser and Lewis (1980) reported
little or no benefit of dietary fat on litter size at birth and
average piglet weight at birth or weaning when data from all
experiments were summarized and weighted for total number of litters
in each experiment. A 0.3 piglet increase in litter size at weaning
was detected. This 0.3 piglet/litter improvement would offset feed
cost increases due to dietary fat (Moser, 1985). However, Moser
(1985) emphasizes that some experiments detected little or no
response to dietary fat on litter size. He also indicated that the
type of dietary fat is relatively unimportant although animal fats
are usually less expensive. Herds with 80% piglet survival will have
increased piglet survival more often than herds with greater than 80%
preweaning survival rates. Cieslak et al. (1983) reported that
survival rates were 10% higher for piglets that weighed 700 to 1100
gm at birth when sows were fed gestation diets supplemented with
fat. Survival of piglets that weighed greater than 1100 gm was not
affected significantly by maternal diet. Results of other studies
confirmed that there is a greater response to added fat under
conditions that predispose to low birth weights (Seerley et al.,
1974; Boyd et al., 1978a; Seerley et al., 1981). Based on previous
results, Moser (1985) suggested that a minimum of 7.5% fat should be
added and indicated that little advantage is afforded with more than
15% fat. Furthermore, he stated that it is more beneficial to add
fat either in late gestation or lactation rather than during both
periods. This is in agreement with Pettigrew (1981) who suggested


61
that at least 1 kg of fat should be fed to the sow by feeding a diet
with 10% added fat for at least 7 d prior to farrowing.
Fat supplementation can enhance piglet survival in at least two
ways. First, fetal liver glycogen is elevated (Boyd, 1978b; Seerley
et al., 1974) and piglets tend to have higher blood glucose
concentrations for up to 24 h after birth (Seerley et al., 1974; Boyd
et al., 1978b; 1981; Parsons, 1979). Second, greater milk yield and
milk fat resulting from maternal dietary fat consumption provide a
greater opportunity for newborn piglets to obtain energy (see Moser,
1985). Thus, providing fat to sows during late gestation may be a
practical way to enhance survival.
Effects of Manipulating Sow Metabolism During Gestation on Piglet
Survival and Growth
In addition to altering dietary components, changes in sows'
metabolism have been induced to make nutrients more available to the
fetus. Hausman et al. (1982) induced diabetes in sows on d 78 of
gestation or fasted sows during the last 20 d of gestation. Piglets
from diabetic and fasted sows had more subcutaneous adipose tissue,
but fetal weights did not differ due to treatment. Kasser et al.
(1982) reported that glucose concentrations in maternal blood were
higher after diabetes was induced. In addition, fetuses from
diabetic sows had higher insulin and triiodothyronine and lower
growth hormone and glucagon concentrations in circulation. Survival
rates of piglets fasted for 47 to 60 h were greater in litters of
diabetic or fasted sows in comparison to litters of control sows.
Piglets from sows with diabetes induced by streptozotocin were
reported to have higher liver glycogen and lipid content in
comparison to controls (Ezekwe et al., 1984). Ezekwe et al. (1984)


62
also reported a positive correlation between the severity of maternal
diabetes and body fat of piglet carcasses. Replacement of 15% of the
metabolizable energy in diets of sows with either 1,3 butanediol or a
mixture of acetate and lactate (1:1 molar) during the last 24 h of
gestation did not alter piglet birth weight (Spence et al., 1985).
However, increased liver glycogen, total glucogen/gm BW and ability
to maintain blood glucose levels during a 36 h fast were detected in
piglets from sows fed either the synthetic ketogenic, butanediol, or
the actetate-lactate diets.
Spence et al. (1984a) examined effects of exogenous growth
hormone injected (sc) at a dose of 24 IU/d from d 100 of gestation
through d 21 of lactation. No difference was reported for glucose or
insulin in maternal plasma, but plasma free fatty acids in GH-treated
sows were elevated two to 2.5-fold. Spence et al. (1984b) reported
that glycogen levels were higher, but not significantly, in piglets
from sows injected with GH. However, fasted piglets from sows
treated with GH had higher plasma glucose. Fat concentrations in
colostrum increased on d 13 of lactation for sows treated with GH,
but were not different on d 20. Milk yields at 2 wk were not differ
ent due to treatments, but were 15% higher at 3 wk of lactation for
sows receiving GH. Feed intake decreased by 22% and backfat loss was
greater for GH-treated sows. Spence et al. (1984b) suggested that
the adverse effect of GH may be due to lipolytic effects. Kveragas
et al. (1986) injected (sc) GH at a dose of 20 IU/d for 21 d prior to
parturition. Both glucose and insulin in plasma were elevated in
treated sows, suggesting insulin resistance. Free fatty acids were
also greater in plasma of sows receiving GH. Piglets from treated


63
sows had greater concentrations of blood glucose following fasting,
more total body lipids at birth and increased concentrations of free
fatty acids in plasma. No differences due to treatment were detected
for birth weight, number born alive or dead or survival of piglets to
d 21 of lactation. Kveragas et al. (1986) reported that a
diabetogenic state was induced in gestating sows as indicated by the
higher concentrations of plasma glucose. Furthermore, a treatment x
diet interaction was detected, so the authors indicated that dietary
energy source should be considered when evaluating effects of
exogenous GH. Injection of GH can be fatal in sows. One sow died 3
d after treatment, while three sows died within hours after or before
parturition and exhibited respiratory distress. Thus, the proper
dosage of GH for sows during gestation and lactation warrants further
investigation.
Control and Initiation of Parturition
There are numerous reviews concerning parturition in swine
(Dziuk, 1979; First et al., 1982; Taverne, 1982; Bazer and First,
1983; First and Lohse, 1984; Guthrie, 1985) and factors influencing
piglet survival (Leman et al., 1979; Dziuk, 1979). Similar to other
reproductive processes, events at parturition can reduce potential
litter size. At least six percent of piglets are born dead (Randall,
1972; Sprecher et al., 1974; Leman et al., 1979). Furthermore, the
last piglet in each uterine horn has less than a 50% chance of
survival, according to Bevier and Dziuk (1976). Leman et al. (1979)
indicated that 20 to 25% of piglets died before weaning and that most
of this loss occurred during the first 3 days of the piglets' lives.
Furthermore, the incidence of stillbirths and perinatal deaths


64
increased as litter size increased and as the duration of parturition
increased (Leman et al., 1979). Randall (1972) concluded that piglet
survival at birth was mainly influenced by fetal hypoxia. Temporary
hypoxia during farrowing may cause permanent damage, since English
and Smith (1975) reported that piglets dying before 21 days post
partum had higher blood lactate at birth than those that survived.
By understanding mechanisms controlling parturition, ways of reducing
neonatal death losses may be developed (First et al., 1982; Bazer and
First, 1983). For example, more precise methods of pharmacologically
inducing parturition may be developed. The presence of an attendant
during parturition to assist with difficult deliveries (Hammond and
Matty, 1980) or to resuscitate piglets (Milosavljevic et al., 1972)
has been reported to save up to one additional piglet per litter. In
addition, some potential benefits of controlling time of paturition
precisely are: (1) more efficient use of farrowing facilities; (2)
occurence of births during regular working hours; (3) efficient
cross-fostering of piglets; (4) better synchronization of estrus in
sows after weaning, and (5) more uniform age and weight of piglets in
litters (Guthrie, 1985).
Hormonal changes leading to birth involve final maturation of the
fetus, termination of pregnancy, expansion of the birth canal,
synthesis of milk and the ability to eject milk (Bazer and First,
1983) Because pregnancy is maintained in the presence of functional
CL in pigs, regression of CL and loss of progesterone is the primary
requirement for parturition (First, 1979; First et al., 1982).
However, the exact nature of the initial signal for parturition and
its mode of action are not certain (First et al., 1982). It is


65
somewhat ironic that a product (estrogen) of the conceptus is
required for establishment and maintenance of pregnancy (Bazer and
Thatcher, 1977); a product of the conceptus also initiates
parturition (First et al., 1982). Cortisol clearly causes increased
PGF resulting in regression of CL. How this is accomplished has not
been determined but a proposed mechanism will be reviewed later
(First et al., 1982).
The fetal brain is required for initiation of parturition, since
decapitated (Stryker and Dziuk, 1975; Coggins and First, 1977) or
hypophysectomized (Bose et al., 1974) pig fetuses will not initiate
parturition. Furthermore, increased glucocorticoid production by the
fetal adrenal is crucial to induction of parturition. Adrenal
atrophy in fetal pigs due to hypophysectomy (Bose et al. 1974) or
decapitation (Stryker and Dziuk, 1975) prevents parturition at term.
In sheep, fetal adrenalectomy blocks initiation of parturition (Drost
and Holm, 1968; Liggins, 1969). Administration of dexamethasone to
fetuses (North et al., 1973) or the sow (North et al., 1973; First
and Staigmiller, 1973; Huhn et al., 1976; Coggins and First, 1977;
Huhn et al., 1978; Huhn and Kiupel, 1979) induces parturition which
is followed by live birth and milk ejection. In addition, exogenous
ACTH administration to pig fetuses during the last 10 d of gestation
will cause fetal adrenal cortex hypertrophy and subsequent premature
parturition (Bose, 1973). The porcine fetal adrenal undergoes
hyperplasia and this increases its ability to synthesize
glucocorticoids late in gestation (Bose, 1973; Fevre et al., 1975;
Dvorak, 1972; Lohse and First, 1981). At d 113, the relative
proportion of cortisol in comparison to corticosterone production


66
increases in the fetal adrenal (Lohse and First, 1981). These data
and additional information reviewed by First et al. (1982) suggest
that the increased adrenal cortex weight, due to increased mitosis is
responsible for increased cortisol production from d 89 to 105.
However, the following increase in cortisol (d 105 to 113) is
believed to be due to changes in steroid ratio (First et al., 1982).
The mechanism by which the fetal brain controls the fetal adrenal
has not been defined (First et al., 1982). First et al. (1982)
suggested that control of adrenal cortisol production by the fetal
pituitary may not be the only way in which the fetal brain regulates
the initiation of parturition. First et al. (1982) indicated that,
via an action of the fetal brain, receptors for glucocorticoids must
be developed to allow cortisol to induce parturition. The placenta
may be the target organ for glucocorticoid action prior to
parturition as suggested for other species (Linzell and Heap, 1968;
Anderson et al., 1975; Flint et al., 1975). In rabbits, when fetuses
were removed on or before d 25 of gestation, parturition at term did
not occur and could not be induced by dexamethasone. However, when
fetuses were removed on or after d 26, placentae were delivered on
the expected day of parturition (d 32) (Chiboka et al., 1977). In
pigs, however, live or dead fetal tissue must be present for
pregnancy to be maintained (Chiboka et al., 1976). Whatever the
precise mechanism is, it is believed that glucocorticoids induce
parturition by increasing PGF secretion from the uterus which results
in luteolysis (Nara and First, 1978; 1981a). How fetal cortisol
increases uterine PGF synthesis and how the fetal brain regulates the
adrenal are not known.


67
Based on available evidence, First et al. (1982) proposed the
following sequence of events which lead to parturition in pigs. The
fetal hypothalamus stimulates ACTH production from the fetal
pituitary. Then either a hypothalamic factor or ACTH stimulates the
adrenal cortex to release cortisol. Cortisol or another factor of
hypothalamic origin then acts on the placenta. By some mechanism,
the placenta stimulates uterine PGF production. This may involve
increased 17-alpha-hydroxylase due to cortisol stimulation and
hydroxylase-induced estradiol production which in turn increases PGF
production. Prostaglandins can increase posterior pituitary oxytocin
secretion (Ellendorff et al., 1979) or stimulate progesterone and
relaxin secretion from the CL (Sherwood et al., 1976). In addition,
PGF increases oxytocin receptors allowing for an increased pulsing of
oxytocin and PGF. Then, the combined effects of oxytocin, PGF and
declining progesterone result in myoraetrial contractions, while
relaxin dilates the cervix to facilitate delivery of the piglets. It
is possible that the maternal central nervous system provides the
final signal for initiation of parturition in sows (Guthrie, 1985).
Once signalled to begin, parturition proceeds via coordinated
rhythmic contractions of uterine smooth muscle, involuntary
contractions of abdominal muscles and softening or opening of the
birth canal (First and Lohse, 1984). In pigs, myometrial activity
during late gestation consists of irregular episodes of prolonged
activity in those uterine segments containing a fetus, while those
parts of the uterus which are unoccupied by a conceptus are
relatively inactive (Taverne et al., 1979a). Oxytocin is low (1.3
uU/ml plasma) at this time (Forsling et al., 1979), although oxytocin


68
receptors are present in the pig uterus during late gestation (Soloff
and Swartz, 1975). Not until 9 to 4 h before birth, does myometrial
activity increase in all parts of the uterus. This increase in
activity of the myometrium occurs when concentrations of oxytocin
increase in peripheral plasma. The release of oxytocin seems to be
related to a lower progesterone:estrogen ratio, due to decreasing
progesterone and increasing estrogen (Forsling et al., 1979). In
addition, the frequency of uterine contractions during delivery is
positively correlated with oxytocin concentrations (Taverne et al.,
1979a). First and Lohse (1984) indicated that uterine contractions
are likely initiated by increased intracellular calcium in myometrial
smooth muscle and by formation of gap junctions. Gap junctions
provide low resistance coupling for communication between cells
(Peracchia, 1980). An increase in intracellular free calcium causes
formation of a calcium-calmodulin complex. This complex binds to and
activates myosin light-chain kinase, which phosphorylates myosin, and
thus allows myosin to interact with actin and cause contraction
(Adelstein and Eisenberg, 1980). Although the factors regulating
calcium flux and gap juntion formation are not well understood (Bazer
and First, 1983), prostaglandins may play a role. Prostaglandins
liberate calcium from intracellular binding sites and thus effect
tonic contraction. In addition, prostaglandins cause slow membrane
depolarization that increases the frequency of phasic contractions
(Liggins, 1979). The PGF may cause release of oxytocin in swine as
well (Ellendorff et al., 1979). As reviewed by Bazer and First
(1983) and First and Lohse (1984), oxytocin lowers the threshold for


69
initiation of potential activity and also directly influences the
rate of calcium influx.
Multiple implantation of intrauterine catheters (Zerobin, 1968)
or surface electrodes in swine (Taverne et al., 1979b) provided
evidence that myometrial contractions in all segments of the uterine
horn are synchronized during delivery. These contractions were
initiated at both ends of the uterine horn and subsequently
propagated in either a tubocervical or cervicotubal direction.
Contraction waves returned in an opposite direction upon reaching the
end of the horn (Taverne et al., 1979c; Taverne, 1982). However,
cervicotubal contractions stopped when the horn was empty and seemed
related to the presence of piglets close to the cervix. Taverne
(1982) suggested that this mechanism shortens the distance travelled
by succeeding piglets and prevents piglets from "piling up" near the
cervix. At the cervix, placental attachments could be dissociated
and cause fetal anoxia and death. In support of this idea, piglets
dying during birth are predominantly the last ones born (Randall,
1972) and usually the last piglet in each horn (Bevier and Dziuk,
1976). Although myometrial smooth muscle contractions are
synchronized, expulsion of piglets from the two uterine horns is
random (Dziuk and Harmon, 1969; Taverne et al., 1977).
In addition to uterine contractions, distension and softening of
cervical connective tissue must occur (Bazer and First, 1983; First
and Lohse, 1984). Little is known about the mechanism of cervical
softening in domestic animals (Bazer and First, 1983). However, the
involvement of relaxin on cervical distension before parturition has
been demonstrated in swine (Kertiles and Anderson, 1979; Nara et al.,


70
1982). Sherwood (1982) reviewed structure, source and function of
relaxin in swine. The principle source of relaxin in swine is CL
(Fevold et al., 1930; Hisaw and Zarrow, 1948; Nara et al., 1982).
The CL store and concentrate relaxin throughout pregnancy (Anderson
et al., 1973a,b; Kendall et al., 1978; Fields and Fields, 1985), but
this is not dependent upon conceptuses, since CL of hysterectomized
gilts also accumulate relaxin through d 124 (Anderson et al.,
1982a). Unmated gilts with CL prolonged by exogenous estrogen
(pseudopregnant) also produce and accumulate relaxin in their CL
(Anderson et al., 1973b). Relaxin is secreted or released by luteal
cells of CL (Belt et al., 1971; Kendall et al., 1978) as sustained
surges starting approximately 2 d prior to birth. Maximum values for
relaxin in maternal plasma are at 14 to 22 h prior to parturition
(Sherwood, 1982). The mode of relaxin release is not clear, but
there is evidence that secretion or release of relaxin is induced by
PGF directly (Sherwood et al., 1979; Nara and First, 1981b) or
indirectly through PGF-induced oxytocin release and subsequent
oxytocin action on relaxin secretion. There is some evidence that
timing of relaxin release may be dependent upon lifespan of CL
(Anderson et al., 1982a). Felder et al. (1986) reported that abrupt
shifts in both relaxin and progesterone secretion on d 111 to 113 in
hysterectomized and pregnant gilts. Thus, conceptus/fetal tissues
are not required for the surge of relaxin release coincident with
decreased progesterone. They also suggested that autonomous
regulation within the ovary or from the central nervous system and
pituitary gland may control relaxin and progesterone secretion. In a
recent study, Taylor and Clark (1988) provide evidence that relaxin


71
inhibits its own release from porcine luteal cells. Thus,
autoregulation may restrain relaxin secretion until the initiation of
labor. In a previous study, Taylor and Clark (1987) suggested that
prostacyclin may act alone or in combination with other prostanoids
to cause relaxin release in the pregnant pig.
Dilatation of the cervix is prematurely induced by injection of
relaxin in late pregnant gilts (Kertiles and Anderson, 1979).
Furthermore, removal of CL on d 110 of pregnancy results in difficult
delivery and a prolonged period of parturition. Relaxin replacement
to gilts without CL led to premature delivery, but short duration of
parturition with cervical dilatation (Kertiles and Anderson, 1979).
Zarrow et al. (1956) reported that relaxin caused dilatation of the
cervix, increased water content and depolymerization of cervical
glycoproteins when injected into estrogen-treated ovariectomized
nonpregnant gilts. Nara et al. (1982) found that in the absence of
the source of relaxin, delivery was prolonged and there was a high
frequency of stillborn piglets. Exogenous relaxin decreased the
duration of parturition and increased the frequency of live births
comparable to that for normal ovarian intact gilts. In addition to
inducing cervical distension, relaxin may also prevent premature
labor during late pregnancy by suppressing uterine contractions
(Porter, 1979; Taverne et al., 1979b). In summary, relaxin is
involved in cervical distensibility in swine. However, the effects
of relaxin are dependent upon prior exposure to estrogen or
progesterone followed by estrogen (Sherwood, 1982). The possibility
exists that estrogen, progesterone, prostaglandins, oxytocin and


72
other hormones are also involved in cervical distension (First and
Lohse, 1984; Sherwood, 1982).
Since pharmacological induction of parturition can benefit
management schemes and potentially decrease losses at birth,
protocols have been developed. Administration of exogenous PGF or
one of its analogues, alone, or in combination with oxytocin, is the
most effective and widely accepted method used today.
Chantaraprateep et al. (1986) reported a high number of live piglets
per litter in sows given 175 ug estrumate, a PGF analogue, on d 111
to 113 of gestation (im or iv). The authors attributed the live
piglet advantage to the presence of an attendant. Although birth
weights were less for treated sows, differences were not detected for
individual piglet weaning weights. As First and Bose (1979)
indicated, the advantage of PGF or its analogue is that these
compounds induce normal parturition, as well as, parturition-related
events including initiation of lactation and expulsion of the
placenta (First and Bose, 1979). When administered after d 110 of
gestation, most experiments show no significant difference between
treated and control sows in duration of labor, frequency of piglets
stillborn, birth weight and survival to weaning or weaning weight, as
reviewed by First et al. (1982). There is a slightly greater birth
weight for piglets from control sows, however. The doses of PGF used
in these studies ranged from 7.5 to 12.5 mg/sow (im) (Ehnvall et al.,
1976; Backstrom et al., 1976; King et al., 1979; Hagner et al., 1979;
Huhn et al., 1980). It is critical that parturition not be induced
prior to d 110 since birth weights and piglet survival will be
significantly reduced (First and Lohse, 1984).


73
When oxytocin is given after injection of PGF, delivery occurs in
approximately 27.2 + 2 h and variation in time of delivery is
significantly reduced compared to when PGF is given alone (Welk and
First, 1979). Dial et al. (1987) attempted to determine the optimal
dose and interval between PGF and oxytocin. They based their study
on the fact that although oxytocin administration 16 to 24 h after
PGF administration is effective in initiating parturition within 3 to
6 h, uterine intertia increases (Holtz et al., 1983; Dial, 1984; Welp
et al., 1984). Thus, increased perinatal mortality can result due to
the interrupted delivery. In one trial, sows were given 20 U
oxytocin 16, 20, or 24 h after PGF (Lutalyse) injection (10 mg on d
112, 113 or 114 d of gestation). There was a tendency for
intrapartum complications to be less frequent with the greatest
interval between injections. However, the results indicated that
synchrony of farrowing was greatest when the interval between
injections was reduced. Similarly, although degree of synchrony
increased with 30 U of oxytocin in comparison to lower doses, the
incidence of problems requiring manual intervention also rose.
Another approach to induce parturition in swine involves the use
of epostane, a competitive inhibitor of 3B-hydroxysteroid
dehydrogenase (3B-HSD) (Martin et al., 1987). On d 109 of gestation,
sows received either oral doses or subcutaneous injections of
epostane on a body weight basis. Farrowing occurred 31 to 77 h
later, depending on the dose. With the higher doses, farrowing
occurred within 31 to 33 h. The duration of farrowing, proportion of
piglets born live, birth weights, weaning weights, proportion of
piglets born live that were weaned and interval from weaning to first


74
postpartum estrus were not influenced by treatment. The major
influence of epostane was suggested to be through its action on
3B-HSD and subsequent removal of progesterone. Martin et al. (1987)
concluded that inhibitors of 3B-HSD could be successfully used to
induce farrowing without adversely affecting the sow or litter.
Another method to induce parturition has been reported by Guthrie
et al. (1987). Their method was developed in an attempt to reduce
the incidence of spontaneous farrowing. First et al. (1982) reported
that only 50 to 60% of sows actually begin delivery during a 10 h
interval on the expected day of parturition, because some sows farrow
before the scheduled injection of PGF. By feeding an orally active
progesterone agonist, altrenogest, early unscheduled farrowings can
be prevented (Varley et al., 1985). Therefore, Guthrie et al. (1987)
combined the advantages of altrenogest to delay parturition and PGF
to induce parturition. Oral administration of altrenogest twice
daily on four days beginning on d 109 or 110 prevented early
parturition in all sows. Injection of PGF had no adverse effects
except on lactation in 3 of 62 sows and did successfully induce
parturition. Therefore, Guthrie et al. (1987) concluded that the
combination of altrenogest followed by PGF allows better control of
the time of farrowing. However, they suggest addition of compounds
such as oxytocin or relaxin to their protocol may reduce variation in
time from administration of PGF to birth of the first piglet and
duration of parturition.
In summary, factors associated with parturition are being
elucidated and utilized to manipulate initiation of farrowing to the
advantage of the producer. However, additional experiments may lead


75
to more optimal doses of "inducing" agents and times for
pharmacological intervention.
Physiology and Characteristics of Lactation in Swine
As reviewed by Collier et al. (1984), a classic example of both
homeostasis and homoerhesis is the "redirection of nutrient flow that
occurs at parturition as site of maternal delivery of nutrients to
offspring shifts from placental transfer in the uterus to milk
synthesis, secretion and removal at the mammary gland." Lactation
provides piglets with nutrition and passive immunity against
pathogenic infections and is dependent upon: (1) supply and uptake of
metabolites from blood; (2) amount of secretory tissue present and
(3) stimuli for milk removal. Because all milk precursors are
derived from blood, blood flow to mammary glands as a precentage of
cardiac output increases during lactogenesis (Linzell, 1974) thereby
increasing nutrient delivery to and uptake by mammary glands. In
addition, adipose tissue adapts to demands of lactation under
homeorhetic regulation by mobilizing fatty acids (see Collier et al.,
1984). Four separate stages of lactation include: (1) mammary growth
(mammogenesis); (2) inititiation of copious milk secretion
(lactogenesis); (3) maintenance of milk secretion and (4) weaning
(mammary gland involution) (Hartmann et al., 1984).
Although it is essential that adequate fetal and prepuberal
mammary gland development occur, this review will only consider
pregnant and lactating sows. Hormones known to stimulate mammary
gland growth in swine are estrogens, progesterone and prolactin
(DeHoff et al., 1986); however, general metabolic hormones, e.g.,
insulin, thyroid hormones and corticoids, also affect mammogenesis.


76
Kensinger et al. (1982) indicated that the majority of mammary duct
growth of sows occurs prior to d 60 and Hartmann et al. (1984)
indicated this growth begins around d 45. Concentrations of
circulating progesterone and prolactin remain fairly constant, while
estradiol-17B increases as lobulo-alveolar development is initiated
and concentrations of mammary DNA and RNA increase (Hacker and Hill,
1972; Cowie et al., 1980; Kensinger et al., 1982). Lobulo-alveolar
development occurs between d 60 and 105, with the fastest rate of
mammogenesis occuring between d 75 and 90 (Kensinger et al., 1982).
Lyons (1958) indicated that estradiol, GH and adrenal steroids are
required for duct growth, while progesterone and prolactin, in
addition to the previous hormones, are required for lobulo-alveolar
growth, and prolactin and adrenal steroids are necessary for milk
secretion.
Lactogenesis occurs in two stages: (1) stage I, which occurs
between d 90 to 105 in pigs, is associated with increased synthesis
of fatty acids, distension of alveoli and fat droplet accumulation in
epithelial cells and (2) stage II, extending from d 112 of gestation
through parturition, which is associated with increased
concentrations of RNA and additional increases in production of fatty
acids and CO2 (Kensinger et al., 1982). In sows, alveolar
secretions begin to accumulate about 2 d prior to parturition (Cross
et al., 1958) and, normally, mammary secretion can only be expressed
within a few hours prior to parturition. Lactogenesis (stage II) has
been described by numerous researchers as the time when milk can
first be expressed; however, as Hartmann et al. (1984) suggest,
analysis of lactose may be a more sensitive indicator for the onset


77
of lactation (Willcox et al., 1983). Two theories regarding the
mechanism for the onset of lactogenesis are: (1) mammary glands are
released from inhibition by progesterone or (2) positive stimuli of
prolactin and glucocorticoids act upon the mammary gland (Kuhn, 1977;
Fulkerson, 1979; Cowie et al., 1980). Administration of progesterone
delays onset of lactation until its withdrawal (Gooneratne et al.,
1979; Taverne et al., 1982). However, it is likely that progesterone
withdrawal at parturition is not solely responsible for lactogenesis,
but is coupled to stimulatory effects of prolactin and cortisol
(Hartmann et al., 1984). In addition, declining concentrations of
relaxin may be required for lactogenesis (Cowie, 1969), as reviewed
by Hartmann et al. (1984). Tucker (1985) stated that the minimum
requirement for lactogenesis involves secretion of prolactin,
adrenocorticotrophic hormone (which stimulates secretion of
glucocorticoids), and estrogens and decreased progesterone. Cortisol
induces differentiation of rough endoplasmic reticulum and the Golgi
appartus of epithelial cells during midpregnancy in mice, which
permits prolactin to induce synthesis of milk proteins (Tucker,
1985) Prolactin controls expression of the casein gene and other
genes, and its effects are amplified by insulin and glucocorticoids
and inhibited by progesterone (Tucker, 1985). Growth hormone appears
to act by partitioning available energy away from body tissues toward
milk production (Forsyth, 1986). Improper hormonal stimulation has
been implicated in development of mastitis-metritis-agalactia, which
results in partial or complete failure of lactation (Martin and
Threlfall, 1970).


78
Because alterations in milk composition cause changes in body
composition and growth of piglets (Williams, 1976), composition of
milk may be manipulated by dietary or pharmacological means to
advantageously influence piglet survival. Fat, protein and lactose
constitute approximately 60, 22 and 18%, respectively, of total
energy content in sow milk (Hartmann et al., 1984). Synthesis of
milk fat occurs in cytosolic secretory cells, and lipids accumulate
into droplets in vesicular cells of the basal cytoplasm which move to
the apex of cells and are then extruded (Cowie, 1984). Proteins in
milk are synthesized in endoplasmic reticulum, pass into the Golgi
apparatus where caseins undergo phosphorylation, form micelles within
vesicles and move to the cell apex for membrane fusion and subsequent
discharge of vesicle contents into the alveolar lumen (Cowie, 1984).
Lactose synthesis occurs in the Golgi in association with proteins.
The final step in lactose synthesis involves lactose synthase which
is made up of two proteins: (1) alpha-lactalburain which is
synthesized in endoplasmic reticulum and (2) galactosyl-transferase
which is synthesized in the Golgi (Cowie, 1984). Lactose synthesis
produces equimolar H^PO^ intracellularly and, in order to
neutralize H+, net anion transport occurs (Jenness, 1986). Jenness
(1986) indicated that lactose synthesis and associated anion
transport regulate swelling of Golgi vesicles which, along with rate
of passage of vesicles through cells, determines volume of milk
(aqueous) secreted. Secreted protein is diluted to its final
concentration in Golgi vesicles and dilution of fat globules occurs
in alveoli (Jenness, 1986). Since volume is regulated by lactose
synthesis, fat and protein content are inversely correlated with


79
content of lactose in milk (Davies et al., 1983). Functions of
lactose and fat include supplying energy, while protein is a source
of amino acids for growth (Jenness, 1986). The B-l,4-galactosidic
link of lactose promotes calcium absorption and, since specific
enzymes are required to hydrolyze this bond, it may prevent
intestinal fermentation (Jenness, 1986).
Linzell et al. (1969) and Spincer et al. (1969) estimated that
mammary glands of sows utilize 50 and 31%, respectively, of glucose
entering mammary circulation and glucose is the major source of milk
lactose, glycerol and mammary CO2 (Linzell et al., 1969). Although
acetate has been demonstrated to be preferentially utilized as a
substrate, it is present in low concentrations in plasma of pigs, and
therefore, glucose utilization predominates (Linzell et al., 1969;
Spincer et al., 1969; Bauman et al., 1970). Furthermore, although
glucose and acetate can be use to synthesize fatty acids de novo,
fatty acids derived from plasma triglycerides are the major source of
fatty acids in milk (Hartmann et al., 1984). Free amino acids in
plasma give rise to milk proteins. More complete reviews of
biosynthesis of milk are available (Mepham, 1983; Larson, 1985;
Jenness, 1985).
Maternal antibodies secreted into colostrum and absorbed intact
by piglets during the first 24 h after birth (Lecce and Morgan, 1962)
are critical, since piglets are born agammaglobulinaemic.
Accumulation of immunoglobulins in colostrum occurs rapidly over the
last 2 d of pregnancy, and most of these are derived from maternal
serum (Bourne and Curtis, 1973). Colostrum contains trypsin
inhibitor (Jensen and Pedersen, 1979) which protects immunoglobulins


80
from intestinal proteolysis. Concentrations of all immunoglobulins
in mammary secretions fall rapidly during the first 24 h after
parturition (Curtis and Bourne, 1971). As reviewed in a separate
section, piglets are extremely susceptible to hypoglycemia (Edwards,
1972), so during the first few hours post-partum, intake of colostrum
is critical. Although colostrum contains 586 to 628 kJ energy/100 ml
(Salmon-Legagneur and Guegen, 1962), its energy is limited since it
contains immunoglobulins which will be absorbed intact and not
contribute to energy. Differences in composition of milk and
colostrum are due to the rapid decline in immunoglobulins and casein
during the first few days after parturition and increased
concentrations of lactose (Brent et al., 1973). Klobasa et al.
(1987) reported that concentrations of IgG, IgM and IgA in colostrum
declined by 50% during the first 12 h after parturition. Since
immunoglobulins, especially IgG, are the predominant proteins in
colostrum, total protein content during the first 12 h of lactation
also declined by nearly 50%. Total solids concomitantly declined
during the first day of lactation; however, fat and lactose content
increased at this time. At birth, composition of sows' colostrum was
25.6% total solids, 5.0% fat, 3.1% lactose, 15.7% total protein and
14.3% whey protein. In contrast, at 21 d of lactation, composition
of milk was estimated to be 18.7% total solids, 6.6% fat, 5.8%
lactose, 5.2% total protein and 2.8% whey protein (Klobasa et al.,
1987)', which agrees with estimates of milk composition obtained on d
22 of lactation by White and Campbell (1984). Similar composition of
sows' milk (percent by weight) has been reported by others to be
81.2% water, 6.8% fat, 2.8% casein, 2.0% whey protein, 5.5% lactose


81
and 1.0% ash, which would supply approximately 102 kcal energy/g of
milk (Jenness and Sloan, 1970). Long (1961) estimated concentrations
(g/100g) of ash, fat, lactose, and protein in milk of sows with
values of .6, 8.2, 4.8, and 5.8, respectively.
Hartmann et al. (1984) indicated that with increased litter size
from highly selected sows and decreased neonatal deaths in
technologically sophisticated piggeries, "milk production is now one
of the most important factors limiting piglet growth and, ultimately,
pig production." Lewis et al. (1978) concluded that variability in
milk yield among sows accounts for approximately 33% of the
variability in weight gain of piglets. Milk yield is determined by
epithelial cell number and by secretory activity of cells (Forsyth,
1986) Regulation of milk yield is influenced by suckling intensity
of piglets postpartum (Blaxter, 1961) and possibly by prepartum
factors. For example, Elsley (1971) demonstrated that milk yield of
sows is related to litter size, but it is not clear whether this
regulation is entirely due to suckling and milk removal or whether
development during pregnancy may be involved (see Forsyth, 1986).
However, greater fetal numbers were not associated with additional
increases in mammary development (Kensinger et al., 1980). Milk
yield can be assessed by: (1) differences in piglet weights or sow
weights before and after suckling (Braude, 1954; Lewis et al., 1978);
(2) milking sows by hand or machine at intervals following oxytocin
injection (Hughes and Hart, 1935; Hartmann and Pond, 1960; Linzell et
al., 1969); (3) isotope dilution (Yang et al., 1980) and (4) isotope
transfer (See Oftedal, 1984). Estimates of daily milk yield of sows
between d 7 and 28 of lactation range from 5 to 13 kg/d (White and


82
Campbell, 1984; White et al., 1984a; Coffey et al., 1987). English
et al. (1982) and White and Campbell (1984) detected greatest milk
yield at approximately 3 wk of lactation. Yield during an 8 wk
lactation has been estimated to average 5.8 kg/d (Smith, 1952; Barber
et al., 1955; Smith, 1959; Hartman et al., 1962). Peak yields
occurred between the third and fifth wk and yields slowly declined by
the ninth or 10th wk (Allen and Lasley, 1960). Thus, early weaning
can result in the inability of sows to reach peak production. Yield
is also influenced by parity; yield increases from the first to third
lactation (Smith, 1959; Van Spaendonck, 1967). In addition, sows in
good condition produce more milk than thin sows even when thin sows
are fed extra energy during early lactation (Klaver et al., 1981).
As previously mentioned, milk yield is a linear function of rate of
blood flow to mammary glands (Kronfeld, 1969). Increasing
photoperiod from 8 to 16 h per d increased milk production by 20%,
litter weight at 21 d by 13% and piglet survival by 10% (Mabry et
al., 1982).
Suckling is required to maintain lactation; unsuckled mammary
glands involute rapidly (Cross et al., 1958; Martin et al., 1978).
Suckling maintains lactation, in part, through its stimulation of
prolactin (Bevers et al., 1978), a necessary hormone for maintenance
of lactation (Schams, 1976). During lactation, concentrations of
prolactin in serum are between 3 and 8 ng/ml compared to 1 to 2 ng/ml
after weaning (Bevers et al., 1978; Mulloy and Malven, 1979).
Administration of bromocryptine, a dopamine agonist, inhibits
prolactin secretion and prevents milk secretion in swine. In
addition to its requirement for milk synthesis, suckling behavior


83
is required for milk ejection through stimulation of oxytocin
release. It is generally accepted that a discrete release of
oxytocin is responsible for milk flow at each suckling (Cross,
1977). However, relaxin may help regulate the duration of milk
release (Afele et al., 1979). Milk is ejected from alveoli by
myoepithelial cell contractions in response to oxytocin which leads
to increased intramammary pressure (Cowie, 1984). Estimates of
suckling frequency vary from 12 to 18 times per 24 h (Hughes and
Varley, 1980) to once every 55 to 65 min for 2 to 3-wk-old piglets
(Whittemore and Fraser, 1974).
Influence of Nutrition on Sow Performance During Lactation
Nutrition of sows during lactation is designed to maximize milk
production and minimize body weight and fat losses. However,
nutrition during lactation also impacts short- and long-term post-
weaning reproductive efficiency (see Britt et al., 1985). Nutrient
requirements and composition of the diet during lactation are
influenced by nutrient intake during gestation, weight and condition
of the sow at onset of lactation, as well as milk yield and
composition which are influenced by litter size, seasonal or
temperature variations and stage and duration of lactation. In
addition, O'Grady (1985) indicated that energy and protein allowances
for lactation must be related to expected life of sows and, if
multiple litters are expected, allowances must permit maintenance of
body fat reserves. If protein intake is inadequate (O'Grady and
Hanrahan, 1975), sows will draw upon their own reserves to meet
demands for secretion of milk proteins and consequently lose
weight. Often, long term effects of nutrition and weight loss


84
during lactation on sow productivity have not been investigated.
Numerous reviews have addressed nutritional needs of lactating sows
(Cole, 1982; O'Grady, 1985; Aherne and Kirkwood, 1985; Britt, 1986).
Relative to those of pregnancy, nutritional requirements to meet
the demands of milk production are high (Cole, 1982). Energy
consumption of sows during lactation influences: (1) litter size
weaned; (2) days to estrus after weaning and (3) subsequent litter
size (Lewis and Reese, 1986). Evaluating effects of increased
energy, specifically, is difficult in numerous experiments, because
greater intakes of all nutrients occurred. In addition, carry-over
effects of energy and(or) feed intake during gestation influence
energy intake during lactation and vice versa (Salmon-Legagneur and
Rerat, 1962). Sows that consume the most feed during pregnancy lose
the most weight during lactation (Salmon-Legagneur and Rerat, 1962;
Sterling and Cline, 1986). However, if feed intake is increased
during the latter part of pregnancy (d 105 of gestation through
lactation), lactational performance may be improved without having a
detrimental effect on sow weight loss (Sterling and Cline, 1986).
Mahan and Mangan (1975) provided evidence of an interaction between
protein level fed thoughout gestation and voluntary intake of gilts
during lactation. If high levels of dietary protein (18%) were
supplied during lactation, feed intake during lactation was
independent of dietary protein level fed during gestation. However,
if a 12% crude protein diet was fed during lactation, feed intake
during lactation was linearly related to level of protein fed during
gestation. Results obtained over three or four reproductive cycles
by O'Grady and Hanrahan (1975) confirmed those findings. Results of


85
a larger study indicated that it may be most beneficial to production
to feed diets (13% crude protein and .6% lysine) which provide
similar protein levels during pregnancy and lactation (Greenhalgh et
al., 1977).
Quality and quantity of milk produced are the two major factors
influencing dietary protein requirements during lactation. Cole
(1982) indicated that milk yield is affected by litter size and stage
of lactation which, in turn, affects the amount of energy required
for lactation. Changes in milk composition are most evident early in
lactation when production changes from colostrum to milk. Protein
content of milk declines over the first 10 to 14 d and fat production
increases during the first 3 d. Thereafter, secretion of milk
protein gradually increases and fat synthesis decreases (see Cole,
1982) While milk yield influences the amount of nutrients required,
plane of nutrition influences milk production especially during the
first 3 wk of lactation (Lodge, 1972). O'Grady (1985) indicated that
the greatest requirement for dietary protein is within the first 2 wk
of lactation. Research comparisons and recommendations have been
complicated because length of lactation periods have varied from two
to eight weeks in available literature. O'Grady (1985), for example,
calculated dietary protein requirements after consideration of
protein in milk and milk yield, as well as estimated feed intake and
stage of lactation.
Litter size weaned was increased only slightly when metabolizable
energy (ME) [>14 Mcal/(sow d)] intake during lactation was
increased for sows ranging in parity from 1 to 4 and lactation
periods of 4 to 8 wk (Elsley et al., 1968; Hitchcock et al., 1971;


86
O'Grady et al., 1973; Adam and Shearer, 1975; Reese et al., 1982a;
King and Williams, 1984a). When litter size is increased, greater
energy consumption by sows may be accompanied by greater milk yields
due to sows consuming higher levels of energy. Shurson et al. (1986)
reported that greater energy intake due to inclusion of 10% fat in
the lactation diet increased litter size (8.9 vs 8.4) and litter
weight (56.1 vs 48.9 kg) at 21 d of age. Sow milk yield was
increased by 13.1% for sows consuming fat and this may have been
responsible for increased litter size at weaning. Sterling and Cline
(1986) indicated that ad libitum feeding in late gestation (d 105 to
farrowing) followed by ad libitum feeding of a diet containing 5%
soybean oil during lactation improved milk yield. Feed intake during
lactation and birth weight of piglets were not influenced by ad
libitum feeding of diets containing soybean oil. In spite of
improved milk yields for sows fed ad libitum diets containing soybean
oil, number of piglets born alive was less for ad libitum fed sows.
Nelssen et al. (1985a) utilized 146 primiparous sows to
investigate effects of intakes of 10, 12, or 14 Meal ME/(sow d)
during a 28 d lactation. Sow weight and backfat loss decreased
linearly as energy intake increased. No differences in litter size
at d 14 or at weaning were detected. However, on d 14, pig weights
increased (P < .05) and litter weights tended (P = .13) to increase
linearly as energy intake of sows increased. At weaning, pig weights
and litter weights increased (P < .05) as energy intake of sows
increased. The authors concluded that intakes of 10 Meal ME/(sow
d) decreased sow and litter performance, while little difference in
performance was detected from feeding 12 or 14 Meal ME/(sow d).


87
Therefore, NRC (1979) recommendations of 12.8 Meal ME/(sow d)
appear to be adequate for lactating sows. However, carry-over
effects to subsequent farrowings were not determined. Dulohery et
al. (1986a,b) reported effects of increased energy during lactation
[8 vs 16 Meal ME/(sow d)] and subsequent postweaning [5.75 vs
11.5 Meal ME/(sow d)] intervals on sow and litter performance in
first and second parity sows during 21 d lactations. Litter weight
gain and pig weaning weights were increased and sow weights and
backfat losses were reduced by increased dietary energy.
Seerley et al. (1974) were the first to report that
supplementation of sow diets with lipids (corn oil) had beneficial
effects on piglet performance. Piglet survival to d 21 was increased
by adding corn oil to sows' diets from d 109 through parturition due,
in part, to increased glycogen stores for piglets at birth.
Subsequently, numerous researchers reported that adding fat to sow
diets during late gestation and early lactation improved survival
rates for newborn pigs (Moser and Lewis, 1980; Pettigrew, 1981;
Moser, 1985). Milk yield and(or) composition is improved by addition
of lipids to sow diets (Friend, 1974; Kruse et al., 1977; Coffey et
al., 1982). There is evidence that addition of fat to sow diets
confers advantages on piglet survival that are not obtained when
equivalent amounts of ME are from other energy sources. However,
piglet survival in response to fat supplementation has been varied
and somewhat inconsistent.
Moser (1984) reported that addition of fat to lactation diets of
sows increased ME intake an average of 6.5% over standard lactation
diets. In sow herds which consume an average of 3.0 kg/d of a


Full Text

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81,9(56,7< 2) )/25,'$



REPRODUCTIVE EFFICIENCY OF SWINE AS INFLUENCED BY
FEEDING FRUCTOSE DURING LACTATION OR
GLUTATHIONE DURING EARLY GESTATION
By
WENDY JO CAMPBELL
A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL
OF THE UNIVERSITY OF FLORIDA IN
PARTIAL FULFILLMENT OF THE REQUIREMENTS
FOR THE DEGREE OF DOCTOR OF PHILOSOPHY
UNIVERSITY OF FLORIDA
1988

The author dedicates this dissertation to all of the swine who so
enthusiastically cooperated during this project while receiving such
little recognition.

ACKNOWLEDGEMENTS
The professional guidance, time, and patience of Dr. Fuller W.
Bazer are gratefully acknowledged. The author also extends
appreciation to Dr. W. C. Buhi, Dr. R. M. Shireman, Dr. D. C. Sharp
and Dr. W. W. Thatcher for their advice, encouragement and efforts
throughout this program. For providing the author with a listening
ear and helping hand, sincere gratitude is extended to Dr. J. H.
Brendemuhl who often helped motivate the author. Appreciation is
also extended to Dane Bernis for mixing diets and for providing both
practical and humorous information, and to him and his wife, Lynda,
for their friendship. To other faculty members who were helpful, the
author extends her gratitude for their concern during her education.
The author has been blessed with numerous friends who often
assisted with projects and elevated the quality of her life. For
example, F. and A. Fliss have been a constant source of encouragement
and assistance. Likewise, for the cooperation of her laboratory
companions, C. Ashworth, M. Murray, J. Dore, J. Vallet, K. Young, J.
Harney, D. Dubois, M. Dones-Smith, M. Mirando, T. Ott, L. Smith and
their spouses and(or) friends, the author is grateful. Thanks is
also extended to W. Grubaugh, Dr. K. Bachman, Dr. C. J. Wilcox, Dr.
R. Miller and P. Miles for their technical assistance. Without the
help of L. Joe Padgett and K. Corbett, work at the swine unit would
have been unbearable. The friendship of L. and R. Lawrence, M.
iii

McGuire, A. Williams, B. and M. Schwingel, T. Dawson, K. Bailey, S.
and V. Williams, P. and R. Miles, S. Black, J., D. and B. Yates and
T. and S. TenBroeck will be remembered long after the completion of
this dissertation.
The author extends deep appreciation to J. Weithenauer, for
providing a comfortable home when the author's husband got tired of
her and for unending humor and encouragement. For their constant
love and support, the author will be forever indebted to her family.
Lastly and certainly not the least, the author expresses heartfelt
gratitude to her husband, Donnie Ray, for his blend of affection and
humor without which the author would have had less of a reason to
pursue her goals.
IV

TABLE OF CONTENTS
Page
ACKNOWLEDGEMENTS iii
LIST OF TABLES viii
LIST OF FIGURES x
ABSTRACT xi
CHAPTERS
I INTRODUCTION 1
II REVIEW OF THE LITERATURE 4
//¿Introduction: Reproductive Efficiency 4
Control of the Estrous Cycle in Swine 7
Maternal Recognition of Pregnancy and Factors Associated
with the Establishment of Pregnancy 16
Embryonic/Fetal Mortality 28
Effects of Nutrition or Manipulation of Metabolism of Sows
During Gestation on Embryonic Survival, Litter Size and
Sow and Litter Performance During Lactation 50
¡/Influences of Nutrition Prior to Breeding or During Early
Gestation on Embryonic Survival 52
Effects of Nutrition During Mid- or Late-Gestation on
Piglet Birth Weight and Survival 54
(/Effects of Manipulating Sow Metabolism During Gestation
on Piglet Survival and Growth 61
Control and Initiation of Parturition 63
Physiology and Characteristics of Lactation in Swine. ... 75
✓Influence of Nutrition on Sow Performance During Lactation. 83
i/Influence of Nutrition on Post Weaning Sow Performance. . . 92
Lactation 92
Post Weaning 101
✓Factors Influencing Piglet Survival 103
Factors Associated with Anestrous During and After
Lactation in Sows 107
Metabolism of Glutathione 116
Functions of Glutathione 126
Previous Research Associating Glutathione With Factors
Affecting Embryonic Growth 142
Metabolic Influences of Dietary Fructose 148
Occurence and Utilization 148
General Physiological Roles of Fructose 149
V

Influences of Fructose in Swine in Comparison to
Other Species 150
Digestion, Absorption and Transport 157
General Metabolism 159
Implications in Diabetes 164
Glucose Tolerance as Affected by Dietary Fructose .... 166
Effects on Other Glucoregulatory Hormones 173
Effects on Lipogenesis and Blood Lipids 175
Effects on Uric and Lactic Acid Production 179
Effects on Mineral Status 180
Effects on Amino Acid Absorption 181
Effects on Ethanol Metabolism 181
Previous Research Designed to Assess Effects of Fructose
on Sow and Litter Performance 183
III EFFECTS OF SUPPLEMENTAL GLUTATHIONE IN GESTATION DIETS OF
GILTS ON FACTORS ASSOCIATED WITH EARLY EMBRYONIC
SURVIVAL 196
Introduction 196
Materials and Methods 198
Results 201
Discussion 201
IV EFFECTS OF MATERNAL CONSUMPTION OF FRUCTOSE DURING LACTATION
ON SOW AND LITTER PERFORMANCE DURING LACTATION, INTERVAL
FROM WEANING TO ESTRUS AND METABOLIC INDICES IN PLASMA. . 207
Introduction 207
Materials and Methods 210
Animals, Dietary Treatments and Collection of
Performance Data 210
Catheterization and Blood Collection Protocol 214
Glucose Tolerance Test • 215
Processing of Blood Samples 215
Assay Procedures for Plasma Samples 216
Fructose 216
Growth hormone 216
Glucose 216
Nonesterified fatty acids 217
Insulin 217
Assay Procedures for Milk Samples 218
Milk fat 218
Lactose 218
Protein 218
Statistical Analyses 218
Results 221
Litter Performance 221
Litter size 221
Average piglet weight 221
Litter weight 224
Sow Performance 224
Sow weight change and feed consumption during
lactation 224
Postweaning interval to estrus 227
Milk yield 227
Milk composition 227
VI

Plasma Constituents 231
Fructose 231
Glucose 235
Insulin 237
Nonesterified fatty acids 246
Growth hormone 251
Response to glucose infusion 251
Discussion 257
V SUMMARY AND CONCLUSIONS 276
LITERATURE CITED 280
BIOGRAPHICAL SKETCH 354
vi i

LIST OF TABLES
Table Page
3-1 COMPOSITION OF THE GESTATION DIET (PERCENT BASIS) 199
3-2 EFFECTS OF DIETARY GLUTATHIONE ON FACTORS ASSOCIATED
WITH EARLY EMBRYONIC MORTALITY/CONCEPTUS DEVELOPMENT
AND METABOLISM OF GLUTATHIONE 202
4-1 COMPOSITION OF GESTATION DIET (PERCENT BASIS) 211
4-2 DIETARY COMPOSITION OF TREATMENTS DURING LACTATION .... 213
4-3 LITTER SIZE (LSMEANS) FOR EACH DIETARY TREATMENT BY
WEEK (WK) AND PARITY 222
4-4 AVERAGE PIGLET WEIGHT (LSMEANS) FOR EACH DIETARY
TREATMENT BY WEEK (WK) AND PARITY 223
4-5 LITTER WEIGHT (LSMEANS) FOR EACH DIETARY TREATMENT BY
WEEK (WK) AND PARITY 225
4-6 SOW WEIGHT CHANGE (LSMEANS) FOR EACH DIETARY TREATMENT
BY WEEK (WK) AND PARITY 226
4-7 AVERAGE (MEAN+SE) YIELD, CONTENT AND COMPOSITION OF MILK
FROM SOWS ON D 18 AND 22 OF LACTATION 230
4-8 PRE- AND POST-PRANDIAL MEAN ± SE CONCENTRATIONS
(MG/100 ML) OF FRUCTOSE IN PLASMA OF SOWS FED FRUCTOSE
OR DEXTROSE BY DAY 232
4-9 ANALYSIS OF REGRESSION CURVES OF CONCENTRATIONS OF
FRUCTOSE IN PLASMA 236
4-10 PRE- AND POST-PRANDIAL MEAN + SE CONCENTRATIONS
(MG/100 ML) OF GLUCOSE IN PLASMA OF SOWS FED FRUCTOSE
OR DEXTROSE BY DAY 238
4-11 ANALYSIS OF REGRESSION CURVES OF CONCENTRATIONS OF
GLUCOSE IN PLASMA 241
4-12 PRE- AND POST-PRANDIAL MEAN ± SE CONCENTRATIONS
(uU/10 ML) OF INSULIN IN PLASMA OF SOWS FED FRUCTOSE OR
DEXTROSE BY DAY 242
VÍ i i

4-13 ANALYSIS OF REGRESSION CURVES OF CONCENTRATIONS OF
INSULIN IN PLASMA 245
4-14 PRE- AND POST-PRANDIAL CONCENTRATIONS (uEQ/L) OF
NONESTERIFIED FATTY ACIDS IN PLASMA AVERAGED OVER THE SIX
SAMPLING DAYS BY TREATMENT 247
4-15 ANALYSIS OF REGRESSION CURVES OF CONCENTRATIONS OF
NONESTERIFIED FATTY ACIDS IN PLASMA 250
4-16 PRE- AND POST-PRANDIAL LSMEANS ± SE CONCENTRATIONS (NG/ML)
OF GROWTH HORMONE IN PLASMA OF 14 SOWS SAMPLED ON D 27
OF LACTATION 252
4-17 CONCENTRATIONS (MEAN ± SE) OF GLUCOSE AND INSULIN IN
PLASMA PRE- AND POST-INFUSION OF GLUCOSE 260
IX

LIST OF FIGURES
Figure Page
4-1 Percentage of sows that returned to estrus 229
4-2 Concentrations of fructose in plasma after ingestion of
Dextrose or HFCS 234
4-3 Concentrations of glucose in plasma after ingestion of
Dextrose or HFCS 240
4-4 Concentrations of insulin in plasma after ingestion of
Dextrose or HFCS 244
4-5 Concentrations of nonesterified fatty acids in plasma
after ingestion of Dextrose or HFCS 249
4-6 Concentrations of glucose in plasma in response to
glucose infusion for each day and treatment 254
4-7 Concentrations of insulin in plasma in response to
glucose infusion for each day and treatment 256
4-8 Glucose clearance for each treatment and day 259
X

Abstract of Dissertation Presented to the Graduate School
of the University of Florida in Partial Fulfillment of the
Requirements for the Degree of Doctor of Philosophy
REPRODUCTIVE EFFICIENCY OF SWINE AS INFLUENCED BY
FEEDING FRUCTOSE DURING LACTATION OR
GLUTATHIONE DURING EARLY GESTATION
By
Wendy Jo Campbell
August, 1988
Chairman: Fuller W. Bazer
Major Department: Animal Science
Supplemental glutathione (GSH) was fed to gilts on d 2 through 29
in a corn soybean meal-based diet; 0 (n = 5) or 10 (n = 5) mg GSH/kg
body weight (BW) per d. Embryonic survival, uterine, placental and
embryo weights, activities of glutamic-oxalacetic and glutamic
pyruvic transaminase in plasma, number of corpora lútea, number of
live embryos and total embryos and allantoic fluid and amnionic fluid
volumes were not influenced (P > .05) by dietary GSH on d 30.
In a second experiment, 45 multiparous (M) and 36 primiparous (P)
crossbred sows were fed, on a metabolic BW basis, from d 0 though d
28 of lactation, isonitrogenous and isocaloric corn-soybean
meal-based diets containing either 28% high fructose corn syrup or
22% dextrose (D). Plasma of sows fed fructose (F) contained: (1)
lower (P < .05) concentrations of glucose (G) postprandially; (2)
lower (P < .05) insulin preprandially and (3) higher (P < .05) F pre-
and post- prandially. Concentrations of growth hormone (GH) and
XI

nonesterified fatty acids in plasma and response to G challenge were
not altered (P > .05) by treatment. However, postprandially, GH in
plasma of P sows tended (P = .09) to be greater than for M sows.
Milk yield was not altered by treatment. Milk from D sows had higher
(P < .05) concentrations of lactose and milk from F sows had more (P
< .05) fat. Treatment did not affect (P > .05) weight loss of sows
or the postweaning interval to estrus. However, P sows lost more (P
< .05) weight than M sows and produced milk with greater (P = .06)
concentrations of protein. Litter size (LS) was higher (P < .05) for
sows fed F, and F had a greater effect (P < .05) over time on litter
weight than D. However, weights of piglets and litters at weaning
were similar (P > .05) between treatments. Sows fed F have lower
concentrations of G in plasma initially, but conversion of F to G
results in similar performance except for a slight advantage for F on
piglet survival.
Xll

CHAPTER I
INTRODUCTION
Reproductive efficiency in swine is not represented by any one
trait but rather the net sum of animal performance during various
stages of reproductive life. Reproductive efficiency is partially
determined by embryonic survival during gestation and by performance
of sows and their litters during lactation. These two major areas
greatly influence number and weight of piglets weaned for that
interval. However, another relevant factor is reproductive
performance of sows after weaning which influences number of piglets
produced per year. Various factors impact upon reproductive
performance of swine. One of the more important elements required
for production is nutrition; however, its specific interaction with
reproduction is not well defined. Because producers can easily
implement new feeding regimes, it is an area through which knowledge
gained through research can yield rapid benefits. Objectives of this
dissertation were to clarify effects of specific dietary ingredients
on embryonic survival and lactational and rebreeding performance in
swine.
In the first experiment, specific objectives were to determine
effects of supplementation of glutathione (GSH) in diets during early
gestation on factors associated with conceptus development and
embryonic survival. Because up to one-third of potential piglets are
lost due to embryonic mortality during gestation, factors associated
with survival are relevant. In swine and other species in which
1

2
multiple offspring are born, it is intriguing that certain embryos
survive while others perish within the same uterine environment.
This has led to the suggestion that embryos which survive are able to
more effectively compete for nutrients, growth factors or conceptus-
endometrial contact and(or) secretions during early blastocyst
expansion. Glutathione has been associated with numerous
physiological events. Most relevant is its apparent involvement in
in vitro growth of the ovum and stimulation of ovum growth and
uterine proliferation in rabbits. Concentrations of GSH also
increase in pig conceptuses during early growth and differentiation.
Therefore, it was hypothesized that exogenous GSH may provide
additional stimuli for growth in conceptuses and, if so, allow less
advanced embryos to survive. Since dietary ingredients provide the
most practical method of adminstering exogenous compounds, GSH was
incorporated into diets of gestating swine. Objectives included
evaluating effects of dietary GSH on embryonic survival, weights of
uteri, embryos and placentae, numbers of corpora lútea and live, dead
and total embryos, activities of glutamic-oxaloacetic and glutamic-
pyruvic transaminase and volumes of allantoic and amnionic fluid.
Measurements were obtained at d 30 of gestation, because most
embryonic losses occur prior to this time.
Milk production of sows is one of the primary factors limiting
piglet growth. In addition, primiparous sows often experience
anestrus after weaning which can decrease number of piglets born per
sow per year. Therefore, it is of interest to determine the optimum
and cost-effective dietary composition which will alter metabolism of
sows to allow maximum milk production while not hindering subsequent

3
reproductive performance after weaning. For numerous reasons,
effects of replacing part of the dietary energy source of sows with
high fructose corn syrup (HFCS) during gestation and(or) lactation
have been inconclusive. However, promising effects of dietary
fructose were reported on milk production of sows during lactation
and weights of litters at weaning, while negative effects on sow
weight change during lactation may be detrimental during the
postweaning interval to estrus. These effects have not been
confirmed and have been controversial. Effects of ingestion of
fructose in numerous species often depends upon other dietary
ingredients, metabolic status of animals prior to experimentation and
duration of fructose consumption. In some studies fructose resulted
in increased concentrations of insulin and glucose in plasma, while
opposite effects have been reported following other experiments.
Therefore, objectives of one aspect of this study were to further
evaluate effects of replacing part of the dietary energy source of
lactating sows with high fructose corn syrup and dextrose.
Production traits of interest were: (1) litter size and litter weight
gain throughout a 4 wk lactation; (2) sow milk production, weight
loss and interval to estrus after weaning; (3) plasma metabolic
indices, including concentrations of glucose, fructose, growth
hormone, insulin and nonesterified fatty acids in plasma pre- and
post-prandially and (4) response to glucose challenge.

CHAPTER II
REVIEW OF THE LITERATURE
Introduction: Reproductive Efficiency
Factors affecting reproduction in pigs and management
considerations to enhance their reproductive efficiency have been
reviewed (Johnson, 1984; Terqui and Legault, 1984; Dziuk and Bellows,
1983; Yen et al., 1987). As Johnson (1984) indicated: "reproductive
efficiency is a function of age at puberty, fertility (the percentage
of breeding herd females that conceive), fecundity (the number of
offspring per pregnancy) and offspring survival to weaning." Terqui
and Legault (1984) stated that the number of offspring weaned per dam
is one of the best estimate of reproductive efficiency in all species
and that this has been called "numerical productivity." In swine,
numerical productivity (P ) of sows can be expressed as [0'(1 -
em)(l - pm)/I] x 365, where "0" is ovulation, rate, "em" is embryonic
mortality rate from ovulation to parturition, "pm" is mortality rate
from birth to weaning and "I" is the interval between successive
parturitions in days. Terqui and Legault (1984) indicated that "I"
represents the interval from weaning to fertilization in lactating
sows. They suggested that numerical productivity should also include
age at first parturition (m^) and the interval between last
parturition and culling of the female (m2). Therefore, their
estimate of productivity would be: P' = [N x 0‘(1 - em)(l -
pm)]/[m-^ + (N - 1) x I + m2] x 365, where "N" represents the
average number of reproductive cycles at culling. Although
4

5
reproductive efficiency can be defined in numerous ways, e.g., "Sow
Productivity Index" (Yen et al., 1987), all methods estimate number
of pigs produced within the sow's reproductive life. Goals of
producers include maximizing piglets per litter and litters per sow
per year. Factors which influence reproductive efficiency include
genetics, environmental conditions, e.g., photoperiod, temperature,
social interactions, and nutrition.
Age at puberty has moderate heritability (.30) in swine
(Cunningham et al., 1974) and is influenced most by environmental
factors. Tess et al. (1983) determined that the most important
economic consideration in reproductive efficiency of swine is number
of live pigs per litter at birth. This can be influenced by
ovulation and fertility rates, embryonic mortality and losses at
parturition. Although ovulation rate can be increased by selection
(Cunnigham et al., 1979) or administrations of exogenous hormones
(Webel and Day, 1982), it is balanced by decreased embryonic survival-
(Cunningham et al., 1979). Fertility is not a major problem in swine
with the exception of summer or heat-induced infertility (Wetteman
and Bazer, 1985), which can be overcome to a large degree with proper
management. Likewise, parturition is not a major complication in
swine, but can be successfully induced (First and Lohse, 1984) to
increase management efficiency; however, it has limited usefulness
for decreasing the interval between farrowings. Genetic selection
for reproductive efficiency has limited potential, due to low
heritabilities for reproductive traits (Johnson, 1984; Terqui and
Legault, 1984) and other production traits are important in meat
producing animals. Nutritional factors may be exploited to maximize

6
reproductive efficiency. However, optimum nutritional regimens for
the various stages of sows reproductive cycles have not been
determined. Supplementation of certain nutrients, e.g., riboflavin,
during gestation may increase embryonic/fetal survival to term (F. W.
Bazer and M. T. Zavy, personal communication). Manipulation of the
metabolic status of sows during gestation by dietary or
pharmacological agents which induce a diabetic state may increase
fetal energy reserves and enhance survival at birth (Britt, 1986).
Nothing is more vital to neonatal piglets than availability of
immunoglobulins and energy from colostrum at birth. Therefore,
nutrition during gestation and(or) lactation has a significant
influence on piglet survival and growth by influencing milk
production. Similarly, nutritional status influences weight loss and
body condition of sows and, therefore, their ability to rebreed after
weaning which, in turn, affects the interval between parturition.
Scientists are continually searching for factors which will
enhance reproductive efficiency. These approaches enhance our
understanding of physiological mechanisms associated with
reproduction and suggest management protocols to enhance reproductive
efficiency. Nutrition is definitely not a solitary factor, but as
innovative goals are realized, larger litters will be produced and
nutritional requirements will need to be modified to complement
advances in other disciplines that maximize reproductive efficiency
in swine. This review summarizes our knowledge of factors affecting
reproductive efficiency in swine.

7
Control of the Estrous Cycle in Swine
Estrous cyclicity in all mammalian species is dependent upon
proper interactions between the components of the hypothalamic-
pituitary-gonadal axis and the uterus (Anderson, 1974b). Appropriate
morphological modifications and altered secretory functions of these
reproductive tissues allow the sexually mature female pig to display
polyestrous activity (Anderson, 1974b) under domestic conditions and
to complete one estrous cycle approximately every 21+3 days
(Anderson, 1974b; Sorenson, 1979). Although the pig is not a
seasonal breeder, seasonal variation does exist (Ledwitz-Rigby and
Rigby, 1987; Claus and Weiler, 1985). Numerous reviews concerning
reproductive physiology of swine have been published (Anderson,
1974b; Hansel and Convey, 1983; Foxcroft and Van de Wiel, 1982).
This review is not intended to describe mechanisms associated with
follicular growth, intrafollicular communication, selection of
ovulatory follicles, ovulation and other specific events. Rather,
this review is to provide a general overview of the reproductive
biology of female pigs.
The 21-day-estrous cycle in swine is commonly divided into four
phases: estrus, metestrus, diestrus and proestrus (Anderson, 1974b).
The female is sexually receptive to a boar for approximately 24 to 66
h during estrus and the first day of "estrus" is referred to as day
(d) 0 of the estrous cycle. At estrus, concentrations of estrogen,
follicle stimulating hormone (FSH) and progesterone in plasma are low
(Anderson, 1974b). Approximately 38 to 42 h after onset of estrus,
multiple Graffian follicles, selected by a yet undefined mechanism,
ovulate. Ovulation itself results from a complex physiological

8
cascade of events (Murdoch, 1985) initiated primarily by the
ovulatory surge of luteinizing hormone (LH). The LH surge is induced
by the positive feedback of estrogen produced from growing follicles
on the hypothalamic-pituitary axis. Concentrations of LH in plasma
decline rapidly following the LH surge. Metestrus begins as the
female ceases to be sexually receptive and is characterized by low
levels of estrogen, FSH and LH, but increasing concentrations of
progesterone in plasma produced by developing corpora lútea (CL).
During diestrus (d 3 to 4 though d 15 to 16), progesterone secretion
is maximal while concentrations of LH, FSH and estrogen in plasma
remain low. In nonpregant pigs, the CL begin to regress between d 15
to 16 due to prostaglandin F 2-alpha (PGF) secretion by the uterus.
Therefore, progesterone secretion by CL declines and there is
initiation of the proestrous phase. Simultaneously, preovulatory
follicles begin to develop and produce estrogen so that
concentrations in plasma peak around d 18. The elevated estrogen
levels decline to low levels before the subsequent estrous period
begins, but are elevated sufficiently to initiate the ovulatory surge
of LH and initiate a new estrous cycle. Some of these events will
now be discussed in more detail. The luteal phase (diestrus),
terminated by the mechanism of luteolysis, the early follicular
phase, late follicular phase and pre-ovulatory period (proestrus and
estrus) and the periovulatory period (including the early luteal
phase (metestrus) will be discussed in this order as suggested by
Foxcroft and Van de Wiel (1982).
Maintenance of luteal function and thus, continued progesterone
production (Foxcroft and Van de Wiel, 1982), blocks the final stages

9
of follicular growth and steroidogenesis and controls the length of
the estrous cycle. A rise in progesterone generally occurs on d 3 to
4 of the estrous cycle (Van de Wiel et al., 1981). Although the
pattern of secretion may be altered by season (Perotti et al., 1979),
progesterone secretion, as measured in the ovarian vein (Gomes et
al., 1965), is maximal on d 10 to 12, declines slowly to d 13 to 15
and then falls rapidly. However, Masuda et al. (1967) reported
maximal progesterone production on d 8 in the ovarian vein. It is
possible that pigs can sequester progesterone in body fat and return
progesterone into the circulation after luteolysis resulting in a
latent fall in progesterone, and thus, longer effects of progesterone
on the hypothalamic-pituitary axis (Foxcroft and Van de Wiel, 1982).
Whether there is a physiological requirement for a luteotrophin other
than LH in swine is not clear. Prolactin has been demonstrated to
stimulate progesterone secretion by luteinized pig granulosa cells
(Veldhuis et al., 1980) and isolated luteal cells in vitro
(Gregoraszczuk, 1983; Grinwich et al., 1983). Recently, Bramley and
Menzies (1987) characterized receptor numbers for prolactin in the
porcine corpus luteum. Prolactin receptors were low during the
periovulatory and early luteal period, increased in the mid-luteal
phase and declined in the late luteal phase. In pregnant swine, as
gestation advanced, prolactin receptor concentrations in CL
increased. It is known that exogenous estrogens elevate plasma
progesterone levels, prolong CL lifespan (Ford et al., 1982) and
stimulate progesterone production by porcine granulosa cells in vitro
(Goldenburg et al., 1972). However, whether estrogen and prolactin

10
play necessary and direct luteotrophic roles endogenously is not
certain.
Luteolysis in pigs is strongly associated with production of PGF
by the uterus (see Bazer et al., 1982). Moeljono et al. (1976, 1977)
proposed that PGF is the luteolysin in swine and reported increasing
PGF levels in utero-ovarian vein plasma coincident with luteal
regression (Gleeson et al., 1974; Moeljono et al., 1976; Ford et al.,
1982) . Exogenous PGF was luteolytic in gilts in which CL were
maintained beyond their normal life span by estradiol treatment
(Kraeling et al., 1975) or hysterectomy (Moeljono et al., 1976).
However, PGF can only exert a luteolytic effect after d 12 (Diehl and
Day, 1974; Moeljono et al., 1976). To reach the ovary,
prostaglandins produced by the uterus can be transferred to the
ovarian artery and possibly into the lymphatic circulation (Kotwica,
1980). Since exogenous gonadotropins cannot maintain CL of the cycle
in the presence of an intact uterus (Anderson, 1966) , it is suggested
that PGF inactivates some component of the LH stimulatory mechanism
that is effective in maintaining luteal function in hysterectomized
females. Thus, PGF overrides the luteotrophic effect of LH by
blocking the LH-adenylate cyclase pathway. It appears that a loss of
LH-receptor mediated mechanisms within luteal tissue results in the
decline in progesterone synthesis (Foxcroft and Van de Wiel, 1982).
Evidence of coincident increases in prolactin and decreases in
progesterone (Van de Wiel et al., 1981) and indications that
prolactin inhibits progesterone secretion by porcine granulosa cells
(Rolland et al., 1976), have led to speculation that prolactin plays
a role in luteolysis. However, the initial fall in progesterone and

11
increases in estradiol and prolactin occur simultaneously, so it is
difficult to establish exact cause and effect relationships.
However, the majority of literature indicates that PGF is the
luteolysin which, in the absence of a conceptus, overrides
luteotrophic effects of LH and(or) prolactin (see Bazer et al., 1982;
Moeljono et al., 1976).
Resumption of follicular growth and production of estrogens are
initiated following luteolysis. The factor responsible for
initiating onset of increased estrogen production by follicles during
the late luteal/early follicular phase of the cycle is not known.
Whether progesterone blocks ovarian follicular development directly
(thus, removal of progesterone may involve removal of an inhibitory
influence on intra-ovarian factors necessary for initiation of late
follicular growth) or by acting on the hypothalamic-pituitary axis to
inhibit an appropriate pattern of LH:FSH production is not clear.
Whatever the exact mechanism, as the luteal phase ends, certain large
follicles which had previously begun development have increased: (1)
granulosa LH receptor numbers (100 X); (2) LH-stimulated cAMP
production; (3) ability of granulosa cells to secrete progesterone
and convert androgen to estrogens and (4) responsiveness to FSH to
stimulate androgen aromatization in granulosa cells (Anderson et al.,
1979; Leung et al., 1979; Schwartz-Kripner and Channing, 1979).
These changes may be similar to those proposed for rats (Armstrong
and Dorrington, 1977; Richards et al., 1978). Foxcroft and Van de
Wiel (1982) suggest that these follicular responses involve estrogen-
dependent changes in receptors for LH and FSH in granulosa cells and
induction of aromatase enzymes intracellularly. This would allow for

12
LH-induced increases in androgen production by theca cells followed
by increases in aromatization of androgens to estrogens by granulosa
cells. It is important to note that, unlike sheep and cows, pig
granulosa cells produce estradiol in the absence of detectable
androgens. This is possibly due to stored androgens of thecal origin
in the granulosa cells (Evans et al., 1981). Additionally, porcine
thecal cells, as well as granulosa cells, can aromatize androgens to
estradiol. Although the exact mechanism is not clear, Graffian
follicles develop and estrogen production increases in the early
follicular phase. As a result, during the late follicular phase and
pre-ovulatory period, concentrations of circulating estrogens are
elevated between d 18 to 20 (Van de Wiel et al., 1981). Estrogens
exert a positive feedback on the hypothalamus in pigs (Edwards, 1980)
and, in vivo, the pre-ovulatory surge of LH and FSH occurs
approximately 50 to 55 h after the rise in estrogens. However, the
rise in estradiol initially results in suppression of episodic LH
release and, later, inhibition of FSH production which results in low
gonadotrophin levels immediately prior to their surge (Vandalem et
al., 1979; Foxcroft, 1978; Van de Wiel et al., 1981). The rise in
plasma LH and its characteristic preovulatory surge 40 to 48 h prior
to ovulation, with a duration of approximately 20 h concident with
the onset of estrus, has been confirmed by numerous researchers
(Liptrap and Raeside, 1966; Niswender et al., 1970; Henricks et al.,
1972; Rayford et al., 1971; Parvizi et al., 1976; Vandalem et al.,
1979; Edwards, 1980; Van de Wiel et al., 1981). However, the
relationship between the onset of behavioral estrus and timing of the
LH surge is variable (Foxcroft et al., unpublished data in Foxcroft

13
and Van de Wiel, 1982). Van de Wiel et al. (1981) reported maximum
LH levels of 6 ng/ml during the LH surge versus 3 ng/ml associated
with tonic secretion of LH during the luteal phase. Thus, the LH
surge of the pig is not characterized by a discrete LH surge, but one
of rather long duration (Foxcroft and Van de Wiel, 1982). The
response of FSH to estradiol positive feedback is variable. However,
it appears that estrogen directly induces a surge of FSH release
(Elsaesser and Foxcroft, 1978; Edwards, 1980) concident with the LH
surge, but of lower magnitude. As a result of the LH surge,
luteinization of the theca and granulosa cells occurs, estradiol
production declines rapidly, progesterone synthesis gradually
increases and ovulation occurs (Catt et al., 1979; Hunzicker-Dunn et
al., 1979). The requirement of the FSH surge for these phenomena is
questionable (Edwards, 1980), since periovulatory events have been
observed in early weaned sows which did not experience an FSH surge.
Ovulation generally occurs near the end of d 2 of the estrous
cycle when LH levels are low and FSH levels are high (Rayford et al.,
1974; Vandalem et al., 1979; Edwards, 1980; Van de Wiel et al.,
1981) . Whether this rise in FSH is due to removal of inhibin at the
time of ovulation (Channing, 1979) or declining estradiol (Edwards,
1980) is not certain. Foxcroft and Van de Wiel (1982) suggest that
inhibin would specifically regulate FSH secretion. Furthermore,
whether or not the increase in FSH is important for recruitment of
follicles destined to ovulate during the subsequent estrous period
has not been resolved for pigs. Increasing concentrations of
progesterone in the postovulatory period are associated with a
decline in FSH (Vandalem et al., 1979; Edwards, 1980, Van de Wiel et

14
al., 1981), and simultaneously, development of episodic LH release
with increasing amplitude and decreasing frequency. Wilfinger (1974)
and Van de Wiel et al. (1981) also reported increased prolactin
secretion at this time with no known role, but with a possible
function in expression of behavioral estrus. Although numerous
patterns of hormonal secretion have been characterized, the exact
mechanism(s) responsible for follicular recruitment have not been
defined.
Attempts to control length of the luteal or follicular phase of
the cycle pharmacologically to facilitate management of labor and
increase reproductive efficiency have led to inconsistent results
(for review, see Webel and Day, 1982; Day, 1984). Currently, the
most promising approach towards effective regulation of the estrous
cycle in swine involves the use of synthetic steroids with progesta¬
tional activity, e.g., altrenogest. Altrenogest has been effective
in synchronizing estrus to a 4-day period in approximatly 95% of
gilts which have already exhibited estrus by administering altreno¬
gest (15 to 20 mg/day) orally for 18 consecutive days (Redmer and
Day, 1981). Other regimens and doses have been tested (see Webel,
1978; Webel and Day, 1982; Day, 1984), and treatment of young gilts
with altrenogest appears to be a potentially useful management tool.
Genetic selection, pharmacological agents and elevating the
nutritional plane of energy (flushing) (Anderson and Melampy, 1972;
Den Hartog and Van Kempen, 1980; Dziuk and Bellows, 1983) prior to
ovulation have all been utilized to increase ovulation rates in
gilts. It is firmly established that increased feed or energy intake
prior to mating will increase ovulation rate, and the optimum intake

15
period has been reported to be in excess of 11 d (Den Hartog and Van
Kempen, 1980) or as little as 8 to 10 d (Anderson and Melampy,
1972). However, whether flushing increases ovulation rate beyond
normal expectations, or reverses nutritional inhibition due to
previous low levels of feeding is not certain (Anderson and Melampy,
1972). For a review of management recommendations (genetic,
nutritional and age considerations) of gilts aimed at improving
ovulation rates refer to Christenson (1986) or Aherne and Kirkwood
(1985).
The mechanism whereby increased dietary energy elevates ovulation
rate is not known. However, neither increased dietary energy or
exogenous insulin is necessarily accompanied by changes in
gonadotropins or estradiol (Cox et al., 1987). Cox et al. (1987)
suggest the increased ovulation rate induced by diet and insulin may
be due to recruitment of more follicles or lessening of atresia, thus
providing more preovulatory follicles. Direct effects of insulin on
the ovaries have been reported, including promotion of progesterone
production by granulosa (May and Schomberg, 1981) and luteal cells
(Ladenheim et al., 1984) in culture, and androstenedione production
by thecal cells (Barbieri et al., 1983). In addition, insulin and
insulin receptors have been identified in the vicinity of
gonadotropin releasing hormone-producing neurons (Havrankova et al.,
1978) in the hypothalamus. The effects of high energy and insulin on
LH secretion were not clear in the study of Cox et al. (1987). In
experiment 1, both dietary energy and insulin were positively related
with number of LH pulses and ovulation rate. However, in experiment
2 no treatment differences were detected. In a separate report by

16
Flowers et al. (1986), FSH and LH were positively influenced by
flushing between 2 and 5 d prior to estrus.
Thus, the effects of flushing and of insulin are not well
defined, but any or all components of the hypothalamo-hypophyseal-
ovarian axis may be affected by insulin (Cox et al., 1987). Since
increased ovulation rate is accompanied by decreased embryonic/fetal
survival (Johnson et al., 1985), it may be more practical to select
for larger litters and attempt to reduce prenatal and postnatal
losses in pigs rather than attempt to increase ovulation rates.
Maternal Recognition of Pregnancy
and Factors Associated with the Establishment of Pregnancy
Under normal conditions, the luteolysin (presumed to be PGF; see
Bazer et al., 1982) in the pig causes regression of the CL, beginning
around d 15 in nonpregnant pigs. This allows for recurrent estrous
cycles. However, should the female become pregnant, the developing
conceptuses must signal their existence to the uterine endometrium in
order to maintain functional CL and endometrial development and
secretory activity which will permit a gestation period of 114 to 115
d to follow. As reviewed by Bazer et al. (1982), the conceptus is
believed to initiate luteostatic mechanisms via the production of
estrogens (also see Flint et al., 1979a). The exocrine-endocrine
theory (Bazer and Thatcher, 1977) suggests that under the influence
of estrogen produced by the conceptuses, PGF and other components of
endometrial origin, including necessary histotrophic factors, are
directed into the uterine lumen (exocrine direction) (Marengo et al.,
1986). This prevents release of the luteolysin towards the uterine
vasculature (endocrine direction). Thus, establishment and
maintenance of pregancy are initiated.

17
Probably the single most important requirement for establishment
of pregnancy is maintenance of CL. Loss of CL function at any stage
of gestation leads to abortion within 24 to 36 h (Belt et al., 1971)
since CL are required for progesterone production. Concentrations of
progesterone in maternal plasma during pregnancy reach 30 to 40 ng/ml
on d 12 to 14, decline to 10 to 25 ng/ml by d 25 (Guthrie et al.,
1974; Robertson and King, 1974; Knight et al., 1977), and remain
fairly constant until d 100. Then, progesterone levels decline
gradually prior to parturition at which time they decrease abruptly
to <1 ng/ml. However, DeHoff et al. (1986) reported that concentra¬
tions of progesterone peak at d 45 (35 ng/ml), decline at d 60 and
then remained farily constant until a rapid periparturient decrease.
The CL of pigs appear to be autonomous until d 14, and then
require only basal LH support until d 40 to 50. After that time, a
possible role for prolactin in CL maintenance has been suggested (see
Heap et al., 1973). However, based on later studies (Whitacre and
Threlfall, 1981; R. R. Kraeling, unpublished data, cited by Bazer et
al., 1982), it appears that prolactin may not be necessary for CL
maintenance after d 70 of gestation. Recently, Bramley and Menzies
(1987) suggested that prolactin may be luteotrophic during pregnancy
as indicated by increasing numbers of prolactin receptors as gesta¬
tion advances. Whatever the luteotropic agents may be, it is impera¬
tive that they function properly to ensure successful pregnancy.
Following fertilization, embryos move through the oviducts and
into the uterine horns at about the 4-cell stage, approximately 48 h
after ovulation (Hunter, 1974). Transport through the oviduct is
entirely a maternal function involving flow of secretions, movement

18
of cilia, peristaltic contractions, and the actions of gonadal
steroids and prostaglandins (Hunter, 1974). Pig embryos fail to
develop beyond the early blastocyst stage if confined to the oviduct
(Murray et al., 1971; Pope and Day, 1972). Therefore, it is a
requirement that the embryos reach the uterine environment.
Having passed through the oviduct, porcine embryos temporarily
are free to move throughout the uterus (Dziuk et al., 1964), but are
actively undergoing morphological changes. Niemann and Elsaesser
(1986) suggested that estradiol-17B is necessary for
morula-blastocyst transformation in vitro and that the effect is
mediated through specific binding sites. Niemann and Elsaesser
(1986) tested in vitro effects of withdrawing estradiol on
development of porcine morula using an antiestrogen or an antiserum
to estradiol. These compounds reduced rate of blastocyst formation,
and this reduction could be partially reversed by addition of
estradiol-17B to the culture medium. In a subsequent study, Niemann
and Elsaesser (1987) confirmed that estradiol-17B is a potentially
important factor in morula-blastocyst transformation in vitro. The
effects of estrone on transformation were less evident. Whether in
vitro effects of estradiol on transformation is physiologically
relevant remains to be determined.
Embryos reach the blastocyst stage by d 5 and hatch from the zona
pellucida between d 6 and 7. After hatching, blastocysts expand from
0.5 to 1 mm diameter to 2 to 6 mm diameter on d 10. Then, between d
10 to 12, blastocysts undergo the most rapid elongation phase,
changing from spherical (3 to 10 mm diameter), to tubular (10 to 50
mm long) and filamentous (>100 mm long) forms, resulting in lengths

19
of 700 to 1000 mm by d 16 of pregnancy (Perry and Rowlands, 1962;
Anderson, 1978). Geisert et al. (1982a) reported that initial
elongation (from 9-10 mm to 100-200 mm) is due to remodeling of
existing trophectoderm. The final elongation (100-200 mm to
800-1,000 mm; d 14 to 16) involves cellular hyperplasia. Albertini
et al. (1987) have begun to investigate the role of actin
cytoskeleton reorganization during premiplantation development of pig
embryos from d 1 through d 8 of gestation. Their experiment was
based on the premise that actin filaments may be involved in
contractile events during compaction (Johnson and Maro, 1984) and
differentiation of trophectoderm (Lehtonen and Bradley, 1980; Reima
and Lehtonen, 1985). Although inconclusive, their results suggest
that actin is important in mechanisms responsible for blastocyst
elongation. Failure of blastocyst elongation can lead to embryonic
death early in gestation or submaximal placental development (Perry
and Rowlands, 1962; Knight et al., 1977).
Although, pig embryos are initially freely mobile, elongated
conceptuses cannot undergo further spacing so they lie end-to-end
along the length of the uterine horns in preparation for
implantation. Spacing of spherical conceptuses is a necessary
requirement since they must compete for a limited amount of
endometrial surface area to obtain support from the endometrial
secretions during placentation. Scheerboom et al. (1987) measured
uterine motility in sows during the estrous cycle and early
pregnancy. They suggested that increased frequency of myoelectrical
complexes (episodes of activity and subsequent interval of
inactivity) may be involved in the process of intra-uterine migration

20
of conceptuses. The interval between myoelectrical complexes
decreased on d 12 of gestation. They also reported that myometrial
activity of low magnitude and high frequency was present during d 8
to 9 of gestation. Pope et al. (1982b) had previously indicated that
contractions of the myometrium are involved in the process of embryo
spacing. Pope et al. (1982b) suspended uterine strips in baths,
during the period of intrauterine migration (d 12 of gestation), and
showed increased myometrial activity in comparison to uterine strips
excised on d 6 to 9 of gestation.
In a subsequent study, Pope et al. (1986a) attempted to examine
the process of intrauterine migration of porcine embryos by studying
a model involving migration of estradiol- and cholesterol-releasing
beads in útero. The presence of estradiol-releasing beads resulted
in activity that induced adjacent beads (estradiol and cholesterol
beads) within the uterus to migrate posteriorly from the uterine
tips. However, cholesterol releasing-beads failed to migrate as far
as estradiol-impregnated beads. The possibility that adjacent
embryos migrate as a result of activated myometrial function was
examined in a second experiment. The results were not clear, but
estradiol release locally tended to induce a random distribution of
cholesterol- impregnated beads. In a third experiment (Pope et al.,
1986a), however, estradiol tended to induce anterior migration when
cholesterol-containing beads were placed at the base of the uterine
horn. Pope et al. (1986a) could not conclude whether the uterus was
responding differentially depending on the site of estrogenic action
or whether the anterior, posterior migrations were due to random
intermixing. None-the-less, it appears that estrogen is involved in

21
embryo migration and the waves of uterine contractions. However,
Scheerboom et al. (1987) suggested the myometrial activity is
dependent on ovarian hormones and independent of the blastocyst
because of similar responses in cyclic and pregnant gilts.
Pig conceptuses are known to produce estrogens while undergoing
elongation (Flint et al., 1979a). In addition, Fischer et al. (1985)
demonstrated that estradiol production is initiated by large (7 mm)
spherical conceptuses and then estrone and estradiol are produced by
tubular conceptuses in amounts greater than are produced by d 12
filamentous conceptuses. Fischer et al. (1985) also demonstrated
that [ H]-progesterone could be converted to estrogens. Their
results agree with data obtained from analyses of uterine flushings
and uteroovarian vein plasma for estrogens. In addition, Fischer et
al. (1985) reported that both the conceptus and pregnant endometrium
converted progesterone to estrogens. The initial increase in
estrogen content in uterine flushings (Geisert et al., 1982b) occurs
when conceptuses reach approximately 10 mm in diameter (late
spherical, d 11.5), which coincides with the time of maternal
recognition of pregnancy (Dhindsa and Dziuk, 1968; Bazer and
Thatcher, 1977; Flint et al., 1979a) and just precedes initiation of
trophectoderm elongation. Based on measurements of estrone sulfate
in maternal plasma, estrogen production by pig conceptuses is
triphasic with the first peak occurring between d 10 to 12 (Stoner et
al., 1981). Maternal estrone sulfate increases from d 16 (60 pg/ml)
to d 30 (3 ng/ml) (Robertson and King, 1974; Stoner et al., 1981),
decreases to d 46 (35 pg/ml), increases slightly to d 60, and then
increases steadily to parturition (3 ng/ml) (Robertson and King,

22
1974). Knight et al. (1977) reported the same pattern for
unconjugated estrone and estradiol in peripheral and uterine vein
plasma and amniotic and allantoic fluids. However, Kensinger et al.
(1986) reported higher estradiol values than Knight et al. (1977) and
concentrations similar to Robertson and King (1974). Robertson et
al. (1985) measured estrogens in fetal fluids and maternal blood and
urine and confirmed previous estimates. DeHoff et al. (1986) also
reported patterns of estradiol, estrone and their sulfated forms
similar to those described above. In addition, Robertson et al.
(1985) suggested that the second rise in estrogen concentrations (d
30) reflects estrogen synthesis by the fetus rather than the
trophoblast. Kensinger et al. (1986) and Knight et al. (1977)
indicated that conjugated estrogens at d 30 and during late pregnancy
are primarily of feto-placental origin. Furthermore, during the last
third of gestation, maternal concentrations of estrogen sulfate and
estrone are directly affected by the number of conceptuses present.
According to the exocrine-endocrine theory (Bazer and Thatcher,
1977) , failure of conceptuses to produce adequate estrogens can
result in regression of CL and loss of pregnancy, since PGF will be
allowed to be secreted in an endocrine direction. That estrogens
themselves and not prostaglandin E-^ or E2 are responsible for
movement of PGF into the uterine lumen was demonstrated by Marengo et
al. (1986).
While, conceptuses are undergoing extensive remodelling and
initiating steroid synthesis, the endometrium is actively preparing
for gestation. Similar to conceptuses, the uterine horns and
endometrium elongate (Perry and Rowlands, 1962) from 190 cm on d 3 to

23
a length of 360 cm at d 13 to 18. Some aspects of early embryonic
development have been reviewed by Allen (1984) and Bazer and First
(1983). On approximately d 13 of gestation, porcine conceptuses
begin physical attachment, seen histologically as discrete areas of
cell-to-cell contact, which is maintained by the adhesive properties
of endometrial gland exocrine secretions (Crombie, 1970).
Although the mechanism(s) involved in attachment of blastocysts
to the uterine epithelium is not well understood, Morgan et al.
(1987a,b) suggested that estrogen is involved. Morgan et al. (1987a)
speculated that ultrastructural and biochemical changes occur in the
plasmalemma of the uterine surface epithelium in response to estrogen
for blastocyst attachment. Schlafke and Enders (1975) previously
suggested that attachment is likely mediated by such changes in the
plasma membrane surface of the trophoblast and uterine specific
epithelium. Alteration of protein and polysaccharide composition
occurs on the apical surface of the rabbit endometrium at the time of
implantation (Anderson et al., 1986). Alterations of glycoprotein
coatings on both the trophoblast and epithelial cell plasma membrane
have been suggested by other researchers to be responsible for close
apposition necessary for interdigitation of microvilli (Enders and
Schlafke, 1974; Jenkinson and Searle, 1977).
Keys et al. (1986) utilized a technique involving systemic
injection of Evans blue and localization of endometrial fluorescence
to determine extravascular content of the dye, and thus, endometrial
vascular permeability in the pig. Only in pregnant gilts, at d 12 of
gestation, was a well-defined area of endometrial fluorescence
detected. The response appeared in conjunction with blastocyst

24
elongation and was consistently confined to areas of conceptus
membranes. The coincidence of increased uterine vascular
permeability at the site of attachment and elevated blood flow,
suggest enhanced transport of nutrients toward the conceptus and
movement of conceptus- induced products into the maternal
circulation. Furthermore, it appears that embryonic factors act in a
localized manner to increase uterine vascular permeability
selectively during attachment. Histamines (Dey and Johnson, 1980),
prostaglandins, e.g., PGE (Davis et al., 1983) and estrogens (King
and Ackerley, 1985) of conceptus origin have all been suggested to be
involved in this response (Keys et al., 1986).
From d 16, a microvillous attachment develops between trophoblast
and endometrial epithelium and extends rapidly to cover almost the
entire chorion by d 22 (Bjorkman, 1965). Expansion and development
of the allantois rapidly occurs between d 18 and 30 of gestation.
Fetal and maternal surfaces undergo complex folding to increase
surface area, and areolae develop on the chorioallantois at points
where endometrial glands open into the uterine lumen. Additional
folding of the chorion occurs in each areolus to increase surface
area and to allow for uterine gland secretions to accumulate
(Crombie, 1970). Fusion of chorion and allantois occurs between d 30
and d 60 of pregnancy, and by d 60 to 70, placental development is
complete. Because placentation in the pig is superficial with no
invasion of maternal uterine endometrium, transfer of histotroph from
the endometrial surface occurs at least through the second trimester
of gestation (Bazer and First, 1983). Maintenance of pregnancy
requires successful development of the placenta, so the embryo-fetal

25
units can receive nutrients, wastes can be removed and the conceptus
will be protected from the maternal immune system.
Because of the noninvasive nature of placentation in the pig, it
is likely that a high proportion of the nutrients of the trophoblast
are secreted by endometrial glands and surface epithelium (Amoroso,
1952; Dantzer et al., 1981). Numerous reviews of uterine secretions
during pregnancy and blastocyst-endometrial interactions are
available (Bazer and First, 1983; Flint et al., 1982; Bazer and
Roberts, 1983; Bazer et al., 1986; Roberts and Bazer, 1988).
Fazleabas et al. (1985) demonstrated that, depending upon the
physiological purpose of a protein, some proteins (uteroferrin) are
secreted by uterine gland epithelium, while other proteins (plasmin
inhibitor) are secreted by the surface epithelium. Thus, the pig
epithelium is regionally differentiated. In addition, results of
Fazleabas et al. (1985) confirmed previous reports (Knight et al. ,
1973, 1974a,b) that uterine secretory proteins are under
progestational control. Furthermore, while secretion of proteins by
the pregnant uterus is induced by progesterone, estradiol modulates
the magnitude of secretion of progesterone - induced proteins.
Included among the list of endometrial secretory proteins,
induced at least partially by progesterone (Knight et al., 1973) and
produced in early pregnancy (Zavy et al., 1977), are three enzymes:
uteroferrin, lysozyme and leucine aminopeptidase. These enzymes have
been shown to accumulate in allantoic fluid after d 30 of pregnancy
(Bazer et al., 1975; Roberts et al., 1976). Based on
immunoflourescent studies, these and certain other compounds of
endometrial origin can pass into the fetus via the chorio-allantoic

26
areolae (Chen et al., 1975). Uteroferrin is involved in the
transport of iron from uterine glands to the conceptus (Roberts and
Bazer, 1980; Bazer et al., 1981b; Ducsay et al., 1986). Other
transport proteins such as retinol and retinoic acid binding
proteins, hydrolytic enzymes and regulatory proteins have been found
in uterine secretions of ovariectomized pigs injected with
progesterone. A high content of riboflavin in uterine flushings has
been reported during the initial period of blastocyst expansion
(Moffatt et al., 1980; Murray et al., 1980). Riboflavin appears to
increase embryonic survival when administered orally during early
gestation (F. W. Bazer and M. T. Zavy, personal communication).
Glucose, fructose and ascorbic acid are also found in uterine
flushings and increase in the pregnant uterus as gestation progresses
(Zavy et al., 1982). Thus, the allantoic fluid of pigs contains
substantial quantities of nutrients, including proteins detected in
uterine flushings, glucose, fructose, water, minerals, electrolytes
and vitamins (see Bazer et al., 1981a). The placental areolae appear
to transport these nutrients to the fetus, by fluid-phase pinocytosis
(Friess et al. , 1981) or by an active transport process, e.g., water
and glucose, in order for a successful gestation to occur. So, the
allantois and amnion do not simply play a passive role in protection
of the fetus and expansion of the chorioallantoic membranes. Because
of the roles and composition of the fetal fluids, they are active in
the mechanisms associated with embryonic survival (see Bazer and
First, 1983). Thus, cooperative interactions of the endometrium and
placenta are required for the developing embryo/fetus to receive
adequate nutritional/metabolic support.

27
In addition to requirements for maintenance of pregnancy,
maternal immunological tolerance of the antigenically dissimilar
conceptus must occur (for review, see Koch, 1985) . Although the
conceptus possesses antigens on its surface which are accessible to
and frequently elicit responses from the maternal immune system,
pregnancy normally progesses with no adverse effects. Although the
mechanism of immunological tolerance is not well defined, Beer and
Billingham (1979) suggested that the following events occur during
pregnancy: (1) excess antigen shedding by trophoblast may lead to
blocking of T and B cell immune responses; (2) antigen-antibody
complex production during pregnancy may block T and B cell immune
response and (3) suppressor T lymphocyte production may be enhanced
during pregnancy. Data of Murray et al. (1978) suggest that uterine
secretions of pigs contain an immunosuppressive factor. Masters et
al. (1983) indicated that a large glycoprotein (Mr>660,000) secreted
by pig blastocysts may coat the conceptus and prevent maternal
lymphocytes from recognizing conceptus antigens. Recently, Murray et
al. (1987) identified a high molecular weight glycoprotein
(MW>660,000) purified from d 16 porcine conceptus culture medium that
had potent immunosuppressive effects. This was evidenced by
suppression of phytohemagglutinin and mixed lymphocyte-induced
blastogenesis of lymphocytes. In addition, the authors suggested
that this high molecular weight glycoprotein caused immunosuppressive
effects on anticonceptus immune responses by the mother while leaving
the systemic immune system unaffected.
As mentioned previously, pregnancy usually progresses with no
adverse affects from the antigenic incompatability. In some cases,

28
antigenic disparity might be advantageous for implantation and
continued intrauterine development (Gill and Repetti, 1979). Several
investigators have reported that number of conceptuses, placental
weights and fetal growth rates are higher in allogeneic versus
syngeneic matings (Billington, 1964; James, 1965, 1967; Beer and
Billingham, 1974; Beer et al., 1975).
In summary, numerous interactions between the conceptus and
maternal endometrium are required to assure proper growth,
implantation, nutritional support and immunological acceptance of the
conceptus. In spite of all the mechanisms designed to assure
maintenance of pregnancy, as will be reviewed in the next section,
the incidence of embryonic mortality is high in pigs.
Embrvonic/Fetal Mortality
Litter size is determined by ovulation rate, fertilization rate,
conceptus deaths during gestation and fetal deaths during the
perinatal period. Although ovulation rate can be increased by
nutritional means (Anderson and Melampy, 1972; Den Hartog and Van
Kempen, 1980; Dziuk and Bellows, 1983), greater embryonic death
losses during gestation generally occur so that litter size at birth
changes very little (Legault, 1978). In addition, as the incidence
of ovulation is increased via genetic selection or by gonadotropic
induction, less viable ova are produced (Koenig et al., 1986).
Developing hyperprolific lines such as Meishan pigs have led to
larger litters (Legault et al., 1981). However, an extensive system
of backcrossing with sows of more desirable growth and carcass traits
is required to enhance overall production successfully (Legault and
Caritez, 1983). In addition, the availability of hyperprolific

29
animals is limited. Heritability estimates of live pigs per litter
at birth range from .1 to .18 (Young et al., 1976; Legault; 1983).
Thus, selection for ovulation rate or litter size is not completely
practical. Therefore, the primary focus of this discussion will
concern embryonic mortality.
The majority of pregnancy wastage occurs before or during
embryogenesis and is referred to as embryonic mortality (Flint et
al., 1982). Rates of embryonic mortality, calculated by counting
embryos and using numbers of CL as a measure of the number of eggs
ovulated, usually range from 20 to 45% (see Flint et al., 1982). In
a study utilizing superovulated cows, some follicles were observed to
rupture and luteinize, but oocytes were not released (Monniaux et
al. , 1983). Furthermore, fertility rates as well as the quality of
follicles and ovulations can also contribute to higher embryonic
mortality (see Terqui and Legault, 1984). Therefore, the number of
CL may not always represent the number of eggs shed (Terqui and
Legault, 1984) and embryonic mortality may be over-estimated.
However, in pigs, embryonic mortality estimates are usually in good
agreement with the number of CL and substantial loss due to embryonic
mortality does occur (Flint et al., 1982).
Numerous factors are associated with embryonic loss, including
chromosomal aberrations (Bishop, 1964). Based on karyotypes of
blastocysts recovered from pig uteri, McFeely (1967) and Day and
Polge (1968) suggested that 8 to 12% of fertilized eggs are abnormal
due primarily to polyspermy (which is likely to be lethal). Van der
Hoeven et al. (1985) indicated that this high percentage of
chromosomal abnormalities has not been confirmed. In agreement with

30
Van der Hoeven et al. (1985), Boyd (1965) reported that genetic
abnormalities account for only a small percentage (0 to 4%) of
embryonic mortality in domestic animals. Most losses due to
chromosomal abnormalities were reported to occur after d 10 (McFeely,
1967). Van der Hoeven et al. (1985) reported the karyotypes of 3- or
4-day-old pig embryos after short in vitro culture and confirmed that
a low frequency of chromosomal abnormalities exists in pig
conceptuses. This was true for both 10-day-old pig blastocysts
(Dolch and Chrisman, 1981) and 3- or 4-day-old embryos in which
hatching had not yet taken place (Van der Hoeven et al., 1985). Of
115 embryos cultured (3 to 4-day-old embryos), 80 were judged to be
of normal karyotypes. In contrast, Koenig et al. (1986) reported
25.1% of ova (8 to 32 h post-ovulation) are chromosomally abnormal.
Percentages of immature ova (70% of which never resumed meiosis)
ranged from 8.2 to 15.7%. Thus, Koenig et al. (1986) estimated that
a substantial portion of embryonic loss in swine could be accounted
for by chromosomal abnormalities and(or) ovulation of immature ova.
It is probable that certain boars (Perry and Rowlands, 1962) and
inbreeding (Squires et al., 1952; Rampacek et al., 1975) are
associated with greater losses due to genetic factors. As indicated
by Bazer and First (1983) , because the genotype of the fetus and its
membranes is determined by both the dam and sire genotypes,
production of protein and steroid hormones by the placenta will be
unique. Since these hormones influence conceptus development and
survival in útero, certain sire-dam matings will have higher levels
of fertility and larger litter sizes. However, the effectiveness of
genetic selection for prolificacy in pigs at this time is limited

31
(for review see, Bichard and David, 1985; Johnson et al., 1985,
Legault, 1985).
Genes affecting early embryonic development have been identified
by Goldbard and Warner (1982). They reported that an H-2 associated
gene, named Ped (preimplantation embryo development) controlled
either fast or slow embryonic development in mice. Warner et al.
(1984) speculated that a slower rate of development was associated
with more embryonic mortality and indicated that this was true for
outbred strains of mice (e.g., CF1, a strain in which a population of
mixed morulas and blastocysts often indicates morulas are moribund)
(C. Warner, unpublished observations cited in Warner et al., 1984).
Furthermore, Warner et al. (1984) speculated that the Ped gene may be
biologically critical. For example, they raised the possibility that
more advanced pig embryos are the ones that survive to birth. In
addition, they wished to pursue whether domestic species have a
homologue to the mouse MHC associated Ped gene. Warner et al. (1986)
have since demonstrated the presence of MHC antigens on 2 to 4 cell
stage and blastocyst stage pig embryos. In addition, Conley et al.
(1987) reported that litters from either sows or boars with the d
haplotype were larger than for all other matings. The authors
concluded that although ovulation rate was higher in SLA sows
(swine MHC, haplotype d), an additional effect of the d haplotype on
embryonic survival was indicated by a significant effect of paternal
genotype on litter size. Thus, the Ped gene initially detected in
mice appears to be present in pigs as well. Recently, Warner et al.
(1988) indicated that the Ped gene product may be the Qa-2 antigen.
In addition, they indicated that although there is no known function

32
for any of the Q-region genes, Qa-2 antigens would be expected to be
expressed on preimplantation embryos possessing Qa-2a alleles but
not Qa-2^ alleles (Warner et al., 1987). Strains of mice
expressing the Qa-2 antigen produce embryos with the slow Ped allele
(Warner et al., 1988). Precisely how the Ped gene regulates
embryonic growth and(or) maternal immunological tolerance remains to
be determined.
It is recognized that pubertal gilts have greater embryonic
losses than multi-estrous pigs (Warnick et al., 1951; MacPherson et
al. , 1977). Uterine capacity does not appear to be the contributing
factor. Up to d 30 of gestation, the gilt can accommodate
approximately twice as many fetuses as are normally present (Dziuk,
1968; Rampacek et al., 1975). Archibong et al. (1987) determined
that changes in the ratio of systemic levels of estrogen and
progesterone may be related to early embryonic mortality in gilts
bred at pubertal estrus. Embryonic survival in the study by
Archibong et al. (1987) was 78.1 vs 95.4% on d 15 and 66.7 vs 89.4%
on d 30 of gestation in gilts bred at the first vs the third estrus,
respectively. Although serum estrogen and progesterone were not
significantly different, the ratio of progesterone:estrogen was
higher on d 15 (439 vs 210) and d 30 (597 vs 179), but lower on d 3
(187 vs 444) of gestation for gilts bred at their first or third
estrus, respectively. It is possible that the low
progesterone:estrogen ratio on d 3 may have altered uterine secretory
activity and resulted in early embryonic death. The higher steroid
ratios at d 15 and 30 are probably due to a reduced number of
surviving conceptuses and reduced estrogen production by the placenta

33
after d 12 of gestation. Although further investigation will be
required, the altered steroid ratios may be involved in embryonic
loss in gilts.
It is well known that progesterone is required for the
establishment and maintenance of pregnancy in the pig. Furthermore,
it has been suggested that a deficiency of progesterone leads to
embryonic loss. Although it is generally assumed that the maternal
hormone profile is always appropriate for establishment of pregnancy,
Ashworth et al. (1984) suggest that naturally occurring levels of
progesterone can be inappropriate and as a result embryonic loss
occurs. Because of this, experiments have been conducted utilizing
progesterone supplementation as a protective measure (Flint et al.,
1982). Results have been inconsistent. Heap et al. (1984) suggest
that progesterone therapy reduces early embryonic loss in certain
circumstances, e.g., high environmental temperatures. However, Heap
et al. (1984) indicate that designing the appropriate dose and time
frame for supplementation is difficult because of the lack of
knowledge of the ways that progesterone supports early embryonic
survival. In addition, Heap et al. (1984) emphasize that it is not
yet known whether progesterone plays an obligatory or a permissive
role. These authors attempted to clarify the role of progesterone in
embryonic survival by utilizing passive immunization against
progesterone in early pregnancy in mice and reported multiple actions
of the antibody (Heap et al., 1984). When anti-progesterone
monoclonal antibody was given repeatedly to BALB/c mice as five daily
injections from the day of mating, implantation was blocked in all
six mice. Furthermore, few of the embryos of treated dams progressed

34
to the blastocyst stage and there was no indication of delayed
implantation. No remnants of degenerating conceptuses were detected
at autopsy on d 30 after copulation. The authors indicated that the
primary effect of the antibody was to arrest cleavage of embryos.
This effect was stated to occur during activation of the embryonic
genome. Based on these findings, Heap et al. (1984) stated that
progesterone production in the first 3 d after fertilization is
essential for normal embryonic development. Furthermore, they
indicated that one effect of progesterone is to provide a tubal
environment in which the embryos can develop at normal rates. Their
work is supported by results of Cline et al. (1977) who found that
estrogen dominated females had embryos with retarded development.
However, if progesterone was also supplied, embryonic development
proceeded at a normal rate. Thus, the possibility remains, as
indicated by Ashworth et al. (1984), that insufficient progesterone
production due to inadequate CL function can lead to increased
embryonic losses.
Other researchers have taken the approach that a combination of
exogenous progesterone and estrone will have a more beneficial effect
than progesterone alone on embryonic survival (Sheridan et al.,
1986). Knight et al. (1973) established that a 2000:1 ratio of
progesterone:estrogen was effective in inducing a synergistic effect
on uterine protein secretion in pigs. Although Knight et al. (1974a)
did not find a significant effect on embryonic survival following
steroid injections from d 4 to 15 of gestation, mean placental weight
and allantoic fluid volume increased when measured at d 40 of gesta¬
tion. Knight et al. (1974b) also demonstrated a negative effect of

35
doses higher than 50 mg progesterone and 25 ug estradiol per 45.4 kg
BW on uterine protein secretions. Since then, Wildt et al. (1976)
and de Sa et al. (1981) reported increased litter size following
combined injections of progesterone and estrone between d 14 to 23
and d 16 to 17 of gestation, respectively. However, since primarily
multiparous sows were in the treated group and primiparous were in
the control group, these results may be misleading. Recently,
Sheridan et al. (1986) reported results of administration of proges¬
terone (25 mg) and estrone (12.5 ug) on both d 16 and 17 or on either
d 16 or 17 of gestation. Gestation length was reduced and litter
sizes were larger at birth for steroid-treated sows. However, subse¬
quent litter size at weaning and interval from weaning to rebreeding
were not altered by treatment. Their results support the theory that
injection of progesterone and estrone at a 2000:1 ratio in
quanitities less than 50 mg progesterone and 25 ug estrone/45.4 kg BW
will effectively decrease embryonic mortality. Although Sheridan et
al. (1986) did not determine uterine secretory response or placental
growth in response to exogeneous steroid treatment, they suggested
that due to increased protein secretion or placental growth rate
previously reported by Knight et al. (1973), nutrient availability to
embryos increased and embryonic survival was enhanced.
In many countries, a period of lowered fertility exists in the
summer (see Claus and Weiler, 1985). Ledwitz-Rigby and Rigby (1987)
suggest that part of the decreased reproductive capacity of pigs in
summer may be due to decreased capacity for follicular development
within the ovary as a result of an altered endocrine signal. They
suggest that granulosa cell responsiveness to signals is altered by

36
photoperiod and(or) heat (such as decreased FSH; Mauget, 1982) which
results in a their decreased ability to secrete progesterone.
Conception rate is decreased in summer and tends to be elevated in
autumn and winter (Keindorf and Plescher, 1981; Britt et al., 1983;
Dobao et al., 1983; Mattioli et al., 1983). Mattioli et al. (1983)
and Love (1981) reported that a higher incidence of embryonic loss
occurs in the summer months (June-September). Problems due to timing
of artificial insemination or mating may be responsible for reduced
conception rates. It is known that duration of estrus is prolonged
during the summer (Signoret, 1967; Nauk and Sekrii, 1983). Reduced
farrowing rates due to embryonic loss has been reported (Stork, 1979;
Mattioli et al., 1983) with the highest incidence of abortions
detected in September/October for sows mated between June and
September. Litter size is higher after mating in autumn and winter
compared to summer (Tomes and Nielsen, 1979; Bevier and Backstrom,
1980; Keindorf and Plescher, 1981; Dobao et al., 1983; Mattioli et
al., 1983; Noguera et al., 1983; Aalbers et al., 1984). According to
Bevier and Backstrom (1980) and Mattioli et al. (1983), litter size
for sows mated in the summer is usually reduced by 1 piglet or more
compared to that for sows mated in autumn or winter. Concentrations
of progesterone in early pregnancy (dlO to 60) are lower (21.5 vs
32.4 to 40.3 ng progesterone/ml plasma) in August-September than in
all other months (Beilanski and Kremer, 1983). Seasonal influences
on the weaning-to-estrus interval may be removed by imposing
conditions of decreased photoperiod in summer (Claus et al., 1984).
However, effects of reduced photoperiod on litter size, embryonic
mortality and conception rates have not been reported. It appears

37
that sensitivity to photoperiodic stimuli present in wild pigs
(Mauget, 1982) may not have disappeared completely in domestic pigs
(Claus and Weiler, 1985). However, Claus and Weiler (1985) indicate
that interactions between photoperiod and embryonic/fetal survival
need to be clarified. In addition, this author suggests that effects
now attributed to photoperiod are also due, in part, to temperature
variations.
Environmental factors such as elevated ambient temperature are
also known to influence embryonic mortality (Wettemann et al., 1984;
Wettemann and Bazer, 1985). Although the following discussion deals
with effects of heat stress, it is relevant to the overall discussion
on embryonic mortality. For example, altered endocrine function in a
non-heat stressed sow may also lead to the loss of embryos. Thus, an
overall understanding of factors associated with embryonic survival
can be gained by studying this model.
Wettemann et al. (1984) indicated that heat stress of male swine
results in a decrease in fertilization rate. Furthermore, increased
embryonic mortality occurs when gilts are artificially inseminated
with extended and stored semen from heat stressed boars. However,
when heat stressed boars are naturally mated, conception rate, but
not litter size, is altered (Wettemann et al., 1976, 1979). Heat
stress of gilts prior to breeding did not influence ovulation rate or
embryonic survival (Edwards et al., 1968). However, heat stress
during the intervals from 1 to 15 days (Edwards et al., 1968) or 0 to
8 days (Omtvedt et al., 1971) after breeding reduced conception rate
and litter size when measured at d 30. Kreider et al. (1978)

38
reported that plasma progesterone increased and estradiol decreased
following heat stress of gilts from estrus until d 8 of gestation.
When gilts were exposed to elevated ambient temperatures from d 8
to 16 after breeding, decreased conception rates and reduced litter
size were detected at d 30 of gestation (Omtvedt et al., 1971). In
addition, Omtvedt et al. (1971) suggested that the implantation
period may be the most susceptible to heat stress. Wettemann et al.
(1984) reported effects of heat stress between d 8 to 16 after
breeding on concentrations of progesterone, corticoids and estradiol
in plasma. Luteal function, as measured by progesterone production,
was not altered between days 9 through 28 of pregnancy by heat stress
in those gilts that maintained preganancy. However, in heat
stressed, nonpregnant gilts on d 13 to 19 after estrus, concentra¬
tions of progesterone were reduced in comparison to nonpregnant
control gilts and all pregnant gilts. Yet, by d 25, progesterone in
plasma of heat stressed, pregnant gilts had not decreased to
concentrations usually present at d 25 of pregnancy. Wettemann et
al. (1984) suggested that prolonged luteal regression occurred in
these gilts following maternal recognition of pregnancy and subse¬
quent embryonic mortality. Polge et al. (1966) previously reported
an extended luteal phase and estrus on approximately d 26 after
breeding in gilts with less than 4 embryos on d 12 of pregnancy.
Concentrations of estradiol in plasma in gilts heat stressed from
d 8 to 16 after breeding were greater compared to control nonpregnant
and all pregnant gilts on d 10 to 12 after estrus. Thus, the
increase in estradiol preceeded the decrease in progesterone.
Wettemann et al. (1984) suggested that because the increase in

39
estradiol occurred in heat stressed gilts prior to the normal
initiation of blastocyst synthesis of estrogens, improper timing of
steroidogenesis may have caused detrimental effects on conceptus
development.
Support for this theory has been generated by Morgan et al.
(1987a). Exogenous estradiol treatment on d 9 of pregnancy resulted
in advanced uterine secretory response. This was evidenced as
increased calcium, protein and acid phosphatase levels in uterine
flushings of pregnant gilts unilaterally hysterectomized on d 11.
Following removal of the remaining uterine horn on d 12, increased
protein and acid phosphatase and decreased calcium and PGF were
reported in the estradiol- treated gilts. However, in a second
experiment (Morgan et al., 1987a), exogenous estradiol followed by
hysterectomy at d 16 revealed no differences in calcium, PGF or
protein and decreased acid phosphatase. Blastocysts were fragmented
and degenerating on d 16 in these estradiol- treated gilts, although
they appeared normal in the previous trial at d 12. Collectively
these data suggest that early estradiol exposure in the uterus
advances uterine secretory response and, although blastocyst
elongation occurs, blastocysts fail to survive to d 16. Geisert et
al. (1987) previously indicated that loss of progesterone support was
not responsible for embryonic mortality observed in estradiol-
treated gilts. In addition, estradiol is not directly embryocidal
(Pope and First, 1985) since gilts maintain pregnancy when estrogen
is administered after d 11. Therefore, Morgan et al. (1987a) suggest
that failure of blastocyst attachment is the result of premature
estradiol action on uterine secretions and(or) surface proteins.

40
Thus, as Wettemann et al. (1984) suggested, alteration of the
hormonal sequence which influences the endometrium is detrimental to
embryonic survival.
Wettemann et al. (1984) also studied the response to exogenous
adrenocorticotropin hormone (ACTH) in heat stressed (from d 8 through
d 16 after breeding) versus control pregnant and nonpregnant gilts.
Concentrations of corticoids and progesterone (during the first 2 h
after ACTH) were reduced in heat stressed nonpregnant gilts. Marple
et al. (1972) previously reported that gilts and barrows exposed to
elevated ambient temperatures had increased ACTH concentrations in
plasma. The combined results suggest that heat stress may alter
adrenal steroid secretion. Wettemann et al. (1984) indicate that
endogenously, excessive ACTH may have the same effect on steroids as
seen following exogenous ACTH treatment. Therefore, altered adrenal
activity may decrease embryonic survival either by lowering
concentrations of necessary steroids or by stimulating greater
production of steroids which have detrimental effects. Two lines of
evidence support their suggestion. First, Tilton et al. (1972)
reported that adrenalectomy may prevent embryonic mortality induced
by heat stress of sheep. Secondly, Howarth and Hawk (1968) reported
that injection of ewes with hydrocortisone acetate resulted in
decreased embryonic survival.
Wettemann et al. (1984) also reported the effects of heat stress
from d 8 through d 16 after breeding on embryonic and uterine
responses. The amount of embryonic tissue present at d 16 was less
for heat stressed gilts. However, protein synthetic ability, as
measured by amount of labelled leucine incorporated into

41
macromolecules by conceptus tissue, was not altered when
incorporation was adjusted for dry weight of conceptus tissue.
Similarly, on d 16, total protein and PGF content per uterine flush
were similar for heat stressed and control pregnant gilts. In
addition, uterine endometrial function at d 16 after estrus was not
altered by heat stress, as indicated by similar dry weight of tissue
and incorporation of leucine into macromolecules by uterine
explants. Furthermore, steroidogenesis by conceptuses and uteri were
not altered by heat stress, as measured by total amounts of estrogens
in uterine flushes on d 16 after breeding.
Significant effects of heat stress on concentrations of the
metabolite of PGF, 13,14-dihydro-15-keto-prostaglandin (PGFM),
composition of blood gases and blood flow to the uterus were not
detected (Wettemann et al., 1984). However, concentrations of
prolactin in plasma were elevated in gilts exposed to higher ambient
temperature following breeding (d 8 to 16) (Wettemann and Bazer,
1985). The authors indicated that the precise role of these factors
in embryonic mortality was not readily apparent (Wettemann and Bazer,
1985), but could not rule out the possibility of their importance.
Putney et al. (1987) indicated that increased embryonic mortality
in cows may result from alterations in signals between the conceptus
and maternal endometrium necessary for maintenance of pregnancy.
Heat shock (39 C for 6 h; 43 C for 18h) reduced (54.2%) protein
secretion of conceptuses, and in particular, decreased (74.3%)
conceptus secretion of bovine trophoblastic protein-1 in comparison
to control (39 C for 24 h) conceptuses. However, protein secretion
by endometrial explants was not altered. In addition, a 1225%

42
increase in endometrial PGF2a]_p^a secretion was detected in
response to heat shock. Endometrial PGE2 production and secretion
of prostaglandins by conceptus tissue were not significantly
altered. An analagous situation to that for heat shock in the bovine
(Putney et al., 1987) may occur in porcine conceptus-endometrial
interactions in response to heat stress.
Elevated ambient temperatures during d 53 to 61 of gestation did
not influence conception rate, litter size, piglet birth weights or
survival rates (Omtvedt et al., 1971). However, heat stress during
later gestation (d 102 to 110 of gestation) increased fetal mortality
(Omtvedt et al., 1971). Wettemann and Bazer (1985) emphasize that
during late gestation the requirements of the fetal-placental unit
for estrogen, nutrients, and gaseous exchange are great. Therefore,
conditions leading to deficiencies during late gestation may result
in fetal death. In contrast, during mid-gestation, heat stress may
not be detrimental because the fetus is only about 10% of birth
weight and fetal-placental steroidogenic function (Knight et al.,
1977) is minimal compared to late gestation (Wettemann and Bazer,
1985) .
In summary, Wettemann et al. (1984) demonstrated that exposure of
swine to elevated ambient temperature during early gestation leads to
lower conception rates and litter sizes. Wettemann et al. (1984)
emphasized that concentrations of steroid hormones control uterine
secretions (Knight et al., 1973; Bazer, 1975) and can alter transport
of ova, embryos and sperm (Chang, 1966; Hawk and Conley, 1971; Hawk,
1975). Therefore, it is possible that heat stress alters conception
rate or embryonic survival indirectly via the endocrine system or

43
through direct effects on the gametes or embryos (Wettemann et al.,
1984). Although these studies were conducted to determine effects of
elevated ambient temperature, it is possible that factors associated
with embryonic mortality in heat stressed animals may be induced by
other conditions and also result in embryonic loss.
The effects of migration, distribution and spacing of pig embryos
on pregnancy and fetal survival have been reviewed by Dzuik (1985) .
Dziuk (1985) indicated that embryonic survival is not influenced by
uterine space prior to d 30. It is essential that a minimum of 4
conceptuses occupy the uterus at d 12 for pregnancy to be maintained
(Polge et al., 1966). Furthermore, the proportion of the uterus that
is occupied is inversely related to the probability that pregnancy
will continue (Dhindsa and Dziuk, 1968). Proper spacing must occur
prior to d 12 (Dziuk, 1985). Furthermore, prenatal growth and
survival of fetuses is greatly influenced by spacing and migration of
embryos (Webel and Dziuk, 1974; Anderson and Parker, 1976; Pope and
First, 1985). Because some embryos die between d 13 and 40 of
gestation, gaps between fetuses result since attachment takes place
at d 12 (Dziuk, 1985). In addition, the distribution and spacing of
embryos is not apparently uniform thoughout the length of the
uterus. At d 40 of gestation, the greatest space available to each
fetus was at the tip of the horn and near the uterine body, with the
least available space in the middle of each horn (Hentzel et al.,
unpublished results, cited by Dziuk, 1985). Dziuk (1985) suggested
that this spacing results from death and partial resorption of
embryos initially crowded near the uterine body. Although uterine
space available to each embryo had little influence on embryonic

44
survival prior to d 25 to 30, in later gestation (d 70) few fetuses
survived in the crowded segments according to Dziuk (1968). Dziuk
(1985) suggested that optimum conditions for litter size, fetal
growth and survival involve uniform distribution of embryos with each
occupying 20 cm of space. He also emphasized that it is imperative
that migration, spacing and distribution be equitable very early in
gestation to maximize survival.
Koch (1985) discussed immunological implications of pregnancy in
the pig. Because cells of all higher vertebrates possess
histompatibility antigens on their surface, some mechanism has
evolved to allow for immunological acceptance of the conceptus by the
maternal immune system (Koch, 1985). It has been demonstrated that
the uterus is not a privileged site for survival of conceptuses in
various species including the pig, by continued development of
trophoblastic tissue when transplanted to ectopic sites (Samuel,
1971). In pigs, the major histocompatability complex is the swine
lymphocyte antigen (SLA) complex (Vaiman et al., 1970; Viza et al.,
1970). The SLA complex is responsible for discrimination of self and
non-self and must be dealt with for successful pregnancies to occur
in swine. Although spermatozoa, seminal plasma and tissues of the
conceptus represent sources of antigenic material, embryonic tissues
are considered to be the primary immunological challenge (Koch,
1985). One hypothesis proposed to explain the non-rejection of the
feto-placental unit is the masking of transplantation antigens on the
conceptus. A general suppression of the immune response during
pregnancy has also been suggested. In addition, antigenic disparity
between the mother and conceptus in certain circumstances may be

45
beneficial for implantation and continued intrauterine development
(Gill and Repetti, 1979). However, Koch (1985) indicates that the
precise nature of the maternal immune response towards the conceptus
is not known. None - the-less, it is imperative that the proper
immunological relationship exist between the fetus and mother or
embryonic mortality will result.
Ford and Stice (1985) have evidence of interactions between pig
conceptuses and uterus affecting uterine blood flow previously
described by Ford and Christenson (1979) . Results from numerous
studies suggest that pig conceptuses, through catechol estrogen
production, increases arterial distensibility locally, resulting in
increased baseline blood flow to each fetal-placental unit. However,
contractility of the uterine arterial vasculature to adrenergic
agonists or other vasoactive agents is not affected. This allows
conceptuses to maintain locally elevated blood flow required for
their survival. Simultaneously, the maternal system responds to
life-threatening stimuli by transiently rerouting blood flow away
from the uterus and towards other vascular supplies necessary for
maternal survival (Ford and Stice, 1985). A malfunction in this
system could result in embryonic/fetal death.
As reviewed by Bazer and First (1983), the developing conceptus
may, in part, control its own destiny via the synthesis of certain
compounds. It had previously been postulated that litter size is, in
part, limited by the availability of an essential biochemical factor
(Bazer, 1975). Most embryonic mortality in pigs has been reported to
occur prior to d 12 of gestation (Perry and Rowlands, 1962). Bazer
and First (1983) indicate that loss of pregnancy may be a function of

46
conceptus rather than maternal deficiencies. This may explain why
some embryos survive while others die within the same uterine
environment in polytocous species (Bazer and First, 1983). Thus, if
blastocysts do not develop and elongate at an adequate rate, they
fail to produce compounds critical to their own survival (Bazer and
First, 1983).
One of these necessary signals in the pig is estrogen, which is
produced by the pig blastocyst beginning on about d 11 of gestation
(Geisert et al., 1982b). Estrogen is required to ensure CL
maintenance (Bazer and Thatcher, 1977), and nutrient availability
through stimulation of histotroph secretion (Geisert et al., 1982b)
and increased uterine blood flow (Ford and Christenson, 1979) .
Numerous reviews describe substances produced by the endometrium
and blastocyst which may allow interactions between the conceptus and
endometrium required for embryo survival (Flint et al., 1982; Bazer
and Roberts, 1983; Bazer et al., 1986). At this time, there is no
conclusive immunoelectophoretic or chromatographic evidence for
pregnancy-specific endometrial proteins involved in stimulating
blastocyst growth. However, Flint (1981) suggests that blastocyst
estrogens control secretion of endometrial embryotrophic factors
which should be considered further. If growth promoting substances
are secreted by the endometrium, competition for growth factors may
be involved in deciding which embryos are lost (Flint et al., 1982).
Therefore, conceptuses which elongate first may obtain a higher
proportion of available growth-supporting substances and deprive
those elongating later (Flint et al., 1982).

47
There is considerable variation in blastocyst size during the
time of elongation (Anderson, 1978). As reviewed by Wilmut et al.
(1985), relatively retarded embryos are much less likely to survive
than synchronous embryos or embryos advanced by up to 24 h (Webel et
al., 1970; Polge, 1982). Thus, factors that advance embryonic growth
or are inherent in an embryo make the advanced embryo much more»
likely to survive in the uterine environment of a single sow (Wilmut
et al., 1986) .
Pope et al. (1982a) reported that more developed embryos have an
advantage over less developed embryos when a 2 d range in age and
development was tested. More recently, Pope et al. (1986b) examined
this in embryos within a closer range of development. Utilizing
asynchronous superinduction to test the range of blastocyst
development on embryonic survival in swine, Pope et al. (1986b)
reported the following. When the proportion of less developed
embryos within a litter increased, subsequent mortality also
increased during the first 30 d of gestation. Thus, naturally
occurring variation in stage of embryonic development might explain
some of the loss. This is in agreement with conclusion of Wilmut et
al. (1986) who reviewed factors contributing to embryonic loss and
indicated that variation in stage of embryonic development can be
sufficient to prejudice survival in polytocous species. In another
study lending support to this theory, Morgan et al. (1987b) tested
effects of estradiol treatment on d 11 in synchronous and
asynchronous (blastocysts 24 h behind recepient uterus) gilts and
compared to control asynchronous gilts. Embryos were recovered in
uterine flushings on d 14. Only in the asynchronous,

48
estradiol-treated group did blastocysts fail to develop. Acid
phosphatase activity was higher and amount of calcium recovered was
lower in both the asynchronous and synchronous estradiol-treated
gilts. Thus, estradiol advanced uterine secretory activity. Morgan
et al. (1987b) indicated that this effect was embryocidal to embryos
that are behind in their development, since neither asynchrony or
estradiol itself resulted in embryonic loss. Furthermore, results of
Morgan et al. (1987b) indicate that blastocysts left to develop at
their own rate stimulate uterine environmental changes at the onset
of elongation and allow blastocyst development to proceed normally.
Thus, the uterus appears to play a permissive role with blastocysts
regulating appropriate uterine responses (Morgan et al., 1987b).
Morgan and co-workers (1987b) also indicated that immature
blastocysts may not possess receptors to recognize changes in
regulatory proteins of uterine origin either released by the
endometrium or exposed on the uterine surface epithelium after
estrogen stimulation. Therefore, immature blastocysts do not undergo
developmental changes required for survival. In summary, three
possibilities have been suggested to account for embryonic loss in
gilts with advanced uterine secretion due to estradiol
administration: (1) inability of blastocysts to elongate; (2) altered
uterine surface epithelium and (3) a direct embryocidal effect of the
uterine environment. These studies clearly demonstrate that
blastocysts must attain a degree of morphological maturation before
they can respond to and survive in the altered uterine environment
normally induced by estrogen on d 11 to 12 of gestation. Although
these conditions were experimentally induced (Morgan et al., 1987b),

49
there is normally a high degree of variation in morphological
maturity between conceptuses within the same uterus. Failure of
immature conceptuses to survive the change in intrauterine
environment induced by faster developing conceptuses may be a signi¬
ficant factor contributing to embryonic death losses in pigs. When
conceptuses within the same uterus are similar in development, each
may have a greater ability to respond to the uterine environment and
greater chance for survival. Evidence for this was obtained from a
study of conceptus development in prolific Chinese Meishan gilts
(Bazer, 1987). In comparison to less prolific breeds, Meishan have
less variation in conceptus development between d 8 to 14 of gesta¬
tion and rate of development between d 11 and 12 of gestation was
faster. These results suggest that minimizing variation among con¬
ceptuses may be part of the mechanism by which Meishan pigs produce
larger litters. The larger litters do not result from higher ovula¬
tion rates, but factors associated with higher embryonic survival.
In summary, neither fertilization failure (Robertson et al.,
1951a; Squires et al., 1952; Day et al., 1959; Spies et al., 1959;
Perry and Rowlands, 1962) or chromosomal aberrations (McFeeley, 1967;
Lupse, 1973), insufficient luteal development (Webel et al., 1975) or
insufficient uterine space (Webel and Dziuk, 1974) explain all of the
30% loss of potential embryos common to swine. In addition, no
single factor can explain embryonic loss or be manipulated to
adequately alter embryonic survival (Bazer and First, 1983).
Genetic, nutritional, environmental, disease and endocrine factors
all can lead to embryonic/fetal death. In a later section,
nutritional factors affecting embryonic/fetal loss, litter size and
postnatal survival will be reviewed.

50
Effects of Nutrition or Manipulation of Metabolism of Sows
During Gestation on Embryonic Survival. Litter Size
and Sow and Litter Performance During Lactation
Numerous factors must be considered when formulating a gestation
diet, i.e., feeding recommendations for gilts are much different than
those for sows. Gilts are now bred at young ages and leaner pork is
being produced resulting in lower body fat at breeding. Brooks
(1982) suggested that because the loss of body fat of sows during the
first 2 or 3 farrowings is great, either body fat of gilts should be
increased prior to the first farrowing to provide fat for later
depletion or sows should be fed to avoid body fat depletion. Brooks
(1982) indicated that increasing body fat prior to the first
farrowing is not practical for two reasons: (1) increased feed intake
during pregnancy reduced voluntary feed intake during lactation (Dean
and Tribble, 1961; Salmon-Legagneur and Rerat, 1962; Baker et al.,
1969) and (2) among gilts that receive the same gestation allowance
there is a tendency for those which farrow at heavier weights to lose
more weight during lactation (Brooks and Cole, 1973; Brooks and
Smith, 1980). Thus, it is more practical to maintain body fat by
providing adequate feed allowances from the first farrowing onward.
This may reduce the problem of lower ovulation rates frequently
encountered in gilts having become catabolic during lactation
(Brooks, 1982).
Cole (1982) indicated that sows do not reach reproductive
maturity until about their fourth parity. The most prolific period
will extend beyond that. Therefore, nutritional considerations
should be for more than just short-term. Cole (1982) emphasized that
nutrition impacts on reproductive performance of sows in the

51
following ways: (1) short term reproductive performance evaluated by
how nutrition during pregnancy affects litter size, lactation and
weights of piglets and sows at weaning; (2) performance during the
subsequent pregnancy affected by nutrition during lactation and (3)
long term reproductive performance as influenced by nutrition in
early stages of their reproductive lives. Thus, long term plans
should be developed. In general, diets are designed to conserve body
condition during lactation. Since greater weight gains during
pregnancy result in greater losses in lactation, limited weight gains
in pregancy are desirable (see Cole, 1982).
Nutrition of the breeding pig is not the only consideration,
however. Since piglets are born with limited energy reserves, diets
fed during gestation are formulated to increase fetal glycogen
stores. In addition, attempts are being made to reduce embryonic
death losses through altered nutrition. Because of these different
goals, determination of nutrient requirements for sows is difficult.
Lewis and Reese (1986) listed additional factors which make
formulating diets for sows difficult. First, sows reproduce well
during periods of nutrient deficiency by drawing on their own body
reserves. Pregnants sows have considerably greater feed efficiency
than nonpregnant females (Salmon-Legagneur and Rerat, 1962). Second,
large numbers of sows must be utilized to draw conclusions because
variability in reproductive traits is great. Third, carry-over
effects from pregnancy to lactation and to the next gestation must be
considered. None-the-less, nutrient requirements for sows during
gestation are being determined which will allow maximum reproductive
performance.

52
Influences of Nutrition Prior to Breeding or During Early Gestation
on Embryonic Survival
Feeding recommendations during early pregnancy are not well
established. In a number of cases, embryonic survival has not been
associated with feeding level (Cole, 1982). Dutt and Chaney (1968)
reported higher embryonic survival in sows fed reduced dietary energy
from mating to d 20 of gestation. However, ranges for feed intake
were too broad (1.25 to 4.1 kg/d) to provide practical information.
Dyck and Strain (1980) confirmed reports of higher embryonic survival
when feed intake was reduced from 2.5 to 1.5 kg/d from mating to d 10
of gestation. However, conception rates were reduced in gilts fed
less from mating to d 30 of gestation. As reviewed by Christenson
(1986), continuous ad libitum feeding of gilts before breeding and
during early gestation increased embryonic mortality in comparison to
pigs on restricted feeding (Robertson et al., 1951b; Self et al.,
1955; Gossett and Sorenson, 1959; Haines et al., 1959; Sorenson et
al., 1961). However, a more recent study of nutritional effects on
embryonic survival indicated that actual embryo numbers present were
similar between groups (Den Hartog and Van Kempen, 1980) . Other
researchers failed to confirm an effect of high energy intake on
early embryonic survival in multiparous sows (McGillivray et al.,
1964; Christenson and Zimmerman, 1966; Heap et al., 1967; Toplis et
al., 1983). Toplis et al. (1983) indicated that differences in
embryonic survival previously reported following increased feed
intake were primarily found in primiparous sows and may result from
"flushing" and increased ovulation rate (Anderson and Melampy, 1972;
Den Hartog and Van Kempen, 1980). It is not clear by what
mechanism(s) dietary energy levels exert their effects on embryonic

53
survival in swine other than through increased ovulation rate. Bazer
et al. (1968) demonstrated that rates of embryonic survival of gilts
fed ad libitum for 14 d prior to breeding were reduced not due to
embryo viability or overcrowding, but rather to some uterine factor
which limited litter size. In trials in which embryonic survival was
decreased, reduced concentrations of progesterone in plasma may be
part of the cause. Increased feed or protein intake during early
gestation in dairy cows or gilts has been associated with decreased
concentrations of progesterone in plasma (Jordan and Swanson, 1979;
Dyck et al., 1980).
Evaluating embryonic mortality between d 20 to 30 of gestation
may lead to improper recommendations. Etienne et al. (1983) reported
levels of embryonic mortality of 18 to 33%. However, at d 105,
differences between treatments for fetal mortality were reversed, and
thus, there were no net differences. In summary, nutritional effects
on embryonic survival are not clear. Few studies have led to
conclusive results, so recommendations other than avoiding severe
deficiencies or excesses during early gestation are difficult.
Christenson (1986) recommended that producers restrict feed after
mating, in part, to reduce feed costs and also to decrease embryonic
death losses.
Recently, through a series of cooperative experiments, (F. W.
Bazer and M. T. Zavy, personal communication) effects of
supplementing gestation diets with riboflavin were observed during
early gestation. Endogenous riboflavin increases in uterine
flushings of cyclic and pregnant gilts between d 6 and 8 after onset
of estrus and then decreases to undetectable levels by d 11.

54
Exogenous riboflavin increased levels of riboflavin in uterine
flushings. Pregnant gilts receiving 100 rag riboflavin per day on d 4
to 10 of gestation had increased numbers of live embryos, higher
embryonic survival and greater allantoic fluid volumes at d 30. In a
subsequent trial with 48 control and 51 riboflavin treated
primiparous sows, total number of piglets and piglets alive at birth
tended (P < .11, P < .09, respectively) to be higher and piglets
alive at d 21 and 42 were greater (P < .05). At d 21 and d 42, total
weight of piglets was greater for riboflavin fed sows.
Effects of Nutrition During Mid- or Late-Gestation on Piglet Birth
Weight and Survival
Numerous authors have reported effects of severe feed deprivation
during late gestation (Pond et al., 1968a,b; 1986; Ezekwe and Opoku,
1986; Speer, 1982). Speer (1982) reviewed evidence that low protein
(.5 to 2%), protein-free diets or complete inanition resulted in no
adverse effects on embryonic/fetal development or litter size,
although birth weights were in some cases decreased. Pond et al.
(1986) demonstrated that primiparous gilts can maintain pregnancy
during feed restriction. Primiparous sows were restricted to
one-third of the recommended (NRC, 1979) feed allowance from d 84
through d 108 of gestation. Although effects on fetuses warrant
further research (Pond et al., 1986), litter size was not affected
and piglet birth weight was decreased by 13% in gilts fed the
restricted level (.6 kg/d) (Pond et al., 1986). These results
confirm previous reports by Pond et al. (1968a,b; 1969) in which
protein free diets were fed for various intervals during gestation
and pregnant gilts utilized body stores of nutrients to meet fetal
demands. Recently, Ezekwe and Opoku (1986) demonstrated that feed

55
deprivation (complete starvation for 7 or 14 d prior to farrowing)
did not cause permanent growth retardation of progeny. Litter size,
birth weight, weaning weight, mortality at birth and survival to
weaning of piglets were not altered by starvation of sows. Thus,
feed deprivation for short periods may reduce feed costs. However,
long term effects or effects in the subsequent reproductive phase
were not determined. In other studies, severe protein and(or) energy
restriction during both gestation and lactation decreased the number
of sows returning to estrus after weaning, increased the interval to
estrus and decreased ovulation rates (Holden et al., 1968; Svajgr et
al., 1972; Pike and Boaz, 1972; Hovell and MacPherson, 1977).
Amounts of protein required during gestation are greatly
influenced by the level of protein available during the subsequent
lactation. Mahan and Mangan (1975) indicated that sows fed 9, 13 or
17% protein diets during gestation performed similarly during
lactation if lactation protein levels were adequate. When 18%
protein lacation diets were supplied, no differences in sow or litter
performance were detected. However, if 12% protein was fed during
lactation, litter weights increased most for sows fed the higher
protein levels during gestation. Mahan (1977) reported no difference
in litter size between sows fed gestation/lactation diets of 14/15
versus 8.5/20 percent protein. However, milk production was less for
the 8.5/20% fed sows. Greenhalgh et al. (1977) fed either 9, 11, 13
or 15% protein during gestation followed by 13 or 17% protein during
lactation. Number of total and live piglets born increased, but not
significantly, with ingestion of greater protein during gestation.
Greenhalgh et al. (1980) indicated no difference in piglet weight or

56
litter size at birth due to diets containing 9 or 11% protein during
gestation followed by 13, 15, 17 or 19% protein during lactation.
Feeding either 9 or 15% protein during gestation and 12, 16 or 20%
protein during lactation increased average piglet weight and number
of piglets born, but differences were not significant (NCR-42
Committee on Swine Nutrition, 1978). In summary, sows can withstand
protein deprivation during pregnancy without adverse effects on
litter size at birth. This may be due to the greater ability of
pregnant versus nonpregnant sows to retain nitrogen
(Salmon-Legagneur, 1965; Heap and Lodge, 1967). However, results are
controversial for the effects of long term protein deprivation on
litter size and piglet weight at birth. In addition, protein
deprivation may decrease milk production of sows, but not if adequate
nutrients are supplied during lactation. O'Grady (1985) indicated
that there is agreement that reproductive performance (number, weight
and composition of piglets born/litter) is maximized when 140 to 180
g crude protein/sow is provided during pregnancy and amino acid
requirements are met. Estimated requirements for lysine vary from .4
to .65% of the diet. Estimates of requirements for other amino acids
during pregancy are also available (Cole, 1982; NRC, 1979). Because
different energy sources have different amino acid values and(or)
digestibilities, levels of protein and specific amino acids required
will vary (Maxwell et al., 1987).
Substantial evidence indicates that piglet survival during
lactation is positively correlated with piglet birth weight. Hall et
al. (1984) clearly demonstrated the importance of piglet birth weight
on survival in a study representing over 10,000 pigs. For piglets

57
averaging .45, .68, .91, 1.14, 1.36 or 1.59 kg at birth, the survival
rates (%) were 16, 39, 59, 74, 86 and 95%, respectively. Therefore,
during the last trimester of gestation, researchers have attempted to
increase fetal fat reserves and(or) piglet weight by altering the
diet and(or) metabolism of sows. Swine are born with extremely
limited energy stores in the form of adipose tissue lipids (Mersmann,
1974). Ramsay et al. (1987) reported that central endocrine
regulation has an important function in the development of porcine
fetal adipose tissue metabolism. On d 45 of gestation, spinal
cautery or decapitation was performed in fetuses within one horn,
with the other horn serving as a control. Fetuses were removed on d
110 of gestation and subcutaneous adipose tissue was incubated to
assess metabolic responses to insulin on glucose oxidation or
lipolytic response induced by norepinephrine (NE) bitartrate and
measured by glycerol release. Only decapitated fetal adipose tissue
demonstrated an insulin stimulation of glucose oxidation and
lipogensis. However, NE stimulated lipolysis in fat from cauterized
and control, but not decapitated fetuses. Ramsay et al. (1987)
concluded that the absence of a NE-stimulated lipolytic response in
decapitated fetal tissue demonstrated that central endocrine
regulatory factors control fetal adipose tissue lipolysis.
Furthermore, they indicated that fetal pig adipose tissue is a
consequence of beta-receptor development in response to systemic
hormones controlled by central endocrine regulatory factors. The
inability of spinal cautery to alter glucose metabolism or
responsiveness to insulin stimulation in fetal adipose tissue
indicated that central neural mechanisms did not affect glucose

58
metabolism in fetal adipose tissue. Rather, changes in adipose
tissue of decapitated pigs reflected changes in fetal endocrinology.
Kasser et al. (1983) suggested that the absence of or decrease in
insulin-anatognistic hormones in decapitated pigs during gestation
permitted devlopment of insulin sensitivity in fetal adipose tissue.
Furthermore, Walton and Etherton (1986) reported that GH antagonized
insulin sensitivity of swine adipose tissue. Martin et al. (1985)
found that decapitatation decreased GH concentrations which would
alter insulin responsiveness or receptor concentrations. Either
factor resulted in increased body lipid deposition in decapitated
fetuses (Kasser et al., 1983). Therefore, promotion of fetal lipid
storage may depend on the ability to stimulate or inhibit release of
central endocrine regulatory factors (Ramsay et al., 1987). This
fact should be considered when attempting to increase fetal energy
reserves during gestation.
In a series of experiments, Cline and co-workers reported that ad
libitum feeding with or without 5% soybean oil from d 105 of
gestation until parturition did not alter survival of piglets from
birth to weaning (Massarotti and Cline, 1984; Sterling and Cline,
1986; Lima and Cline, 1987). However, ad libitum feeding and soybean
oil inclusion in the diet increased milk production and heavier
weaning weights of piglets were sometimes detected. Cromwell et al.
(1982) increased feed intake (1.82 to 3.18 kg/d) of sows from d 90
until term and reported increased (+.05 kg) average piglet weight and
greater piglet survival (85.4 vs 87.8%). However, Lewis and Reese
(1986) summarized results of numerous experiments and reported little
or no benefit of additional feed intake late in gestation on piglet

59
survival. They concluded that when piglet birth weights average
greater than 1.4 kg, they will not likely be increased by dietary
factors. Cromwell (1980) presented results of increased energy
intake of sows from over 5000 litters indicating that piglet birth
weights increased by approximately .02 and .05 kg in gilt and sow
litters, respectively for each additional .05 kg of feed consumed.
Although it is desirable to increase birth weights of piglets, it
is necessary to increase sow feed comsumption greatly to elicit small
increases in piglet birth weights. Most researchers recommend
pregnancy weight gains of 10 to 40 kg (O'Grady, 1985). Since, as
indicated previously, maternal weight gains during pregnancy are
deleterious during the subsequent lactation, an optimum level of feed
intake for both fetal and maternal weight gains should be used.
Feeding levels should be adjusted for age, body condition, ambient
temperature, housing, expected low average birth weights and current
feed costs. Diets for gestating sows (with BW of 140 kg) are
recommended to provide 25 Mega Joules (MJ) digestible energy (DE)/d,
e.g., 1.8 kg/d of a corn soybean meal diet.
In addition to providing more energy by increasing overall
consumption, researchers have reported beneficial effects of adding
fat to diets of sows during late gestation and(or) lactation (see
Pettigrew, 1981; Moser, 1985). Moser and Lewis (1980) summarized
results of numerous experiments, performed in the 1970s and 1980s,
which’ evaluated effects of fat added to sow diets on piglet
survival. Type of fat (corn oil, soybean oil, tallow, lard), level
of fat (2 to 40%) and number of days of feeding fat (5 to 135)
varied. As reviewed by Moser (1985), almost all data indicated that

60
fat content in colostrum and milk of sows was increased in sows fed
fat. Controversial results were obtained for piglet survival and
litter size at weaning. However, Moser and Lewis (1980) reported
little or no benefit of dietary fat on litter size at birth and
average piglet weight at birth or weaning when data from all
experiments were summarized and weighted for total number of litters
in each experiment. A 0.3 piglet increase in litter size at weaning
was detected. This 0.3 piglet/litter improvement would offset feed
cost increases due to dietary fat (Moser, 1985). However, Moser
(1985) emphasizes that some experiments detected little or no
response to dietary fat on litter size. He also indicated that the
type of dietary fat is relatively unimportant although animal fats
are usually less expensive. Herds with 80% piglet survival will have
increased piglet survival more often than herds with greater than 80%
preweaning survival rates. Cieslak et al. (1983) reported that
survival rates were 10% higher for piglets that weighed 700 to 1100
gm at birth when sows were fed gestation diets supplemented with
fat. Survival of piglets that weighed greater than 1100 gm was not
affected significantly by maternal diet. Results of other studies
confirmed that there is a greater response to added fat under
conditions that predispose to low birth weights (Seerley et al.,
1974; Boyd et al., 1978a; Seerley et al., 1981). Based on previous
results, Moser (1985) suggested that a minimum of 7.5% fat should be
added and indicated that little advantage is afforded with more than
15% fat. Furthermore, he stated that it is more beneficial to add
fat either in late gestation or lactation rather than during both
periods. This is in agreement with Pettigrew (1981) who suggested

61
that at least 1 kg of fat should be fed to the sow by feeding a diet
with 10% added fat for at least 7 d prior to farrowing.
Fat supplementation can enhance piglet survival in at least two
ways. First, fetal liver glycogen is elevated (Boyd, 1978b; Seerley
et al., 1974) and piglets tend to have higher blood glucose
concentrations for up to 24 h after birth (Seerley et al., 1974; Boyd
et al., 1978b; 1981; Parsons, 1979). Second, greater milk yield and
milk fat resulting from maternal dietary fat consumption provide a
greater opportunity for newborn piglets to obtain energy (see Moser,
1985). Thus, providing fat to sows during late gestation may be a
practical way to enhance survival.
Effects of Manipulating Sow Metabolism During Gestation on Piglet
Survival and Growth
In addition to altering dietary components, changes in sows'
metabolism have been induced to make nutrients more available to the
fetus. Hausman et al. (1982) induced diabetes in sows on d 78 of
gestation or fasted sows during the last 20 d of gestation. Piglets
from diabetic and fasted sows had more subcutaneous adipose tissue,
but fetal weights did not differ due to treatment. Kasser et al.
(1982) reported that glucose concentrations in maternal blood were
higher after diabetes was induced. In addition, fetuses from
diabetic sows had higher insulin and triiodothyronine and lower
growth hormone and glucagon concentrations in circulation. Survival
rates of piglets fasted for 47 to 60 h were greater in litters of
diabetic or fasted sows in comparison to litters of control sows.
Piglets from sows with diabetes induced by streptozotocin were
reported to have higher liver glycogen and lipid content in
comparison to controls (Ezekwe et al., 1984). Ezekwe et al. (1984)

62
also reported a positive correlation between the severity of maternal
diabetes and body fat of piglet carcasses. Replacement of 15% of the
metabolizable energy in diets of sows with either 1,3 butanediol or a
mixture of acetate and lactate (1:1 molar) during the last 24 h of
gestation did not alter piglet birth weight (Spence et al., 1985).
However, increased liver glycogen, total glucogen/gm BW and ability
to maintain blood glucose levels during a 36 h fast were detected in
piglets from sows fed either the synthetic ketogenic, butanediol, or
the actetate-lactate diets.
Spence et al. (1984a) examined effects of exogenous growth
hormone injected (sc) at a dose of 24 IU/d from d 100 of gestation
through d 21 of lactation. No difference was reported for glucose or
insulin in maternal plasma, but plasma free fatty acids in GH-treated
sows were elevated two to 2.5-fold. Spence et al. (1984b) reported
that glycogen levels were higher, but not significantly, in piglets
from sows injected with GH. However, fasted piglets from sows
treated with GH had higher plasma glucose. Fat concentrations in
colostrum increased on d 13 of lactation for sows treated with GH,
but were not different on d 20. Milk yields at 2 wk were not differ¬
ent due to treatments, but were 15% higher at 3 wk of lactation for
sows receiving GH. Feed intake decreased by 22% and backfat loss was
greater for GH-treated sows. Spence et al. (1984b) suggested that
the adverse effect of GH may be due to lipolytic effects. Kveragas
et al. (1986) injected (sc) GH at a dose of 20 IU/d for 21 d prior to
parturition. Both glucose and insulin in plasma were elevated in
treated sows, suggesting insulin resistance. Free fatty acids were
also greater in plasma of sows receiving GH. Piglets from treated

63
sows had greater concentrations of blood glucose following fasting,
more total body lipids at birth and increased concentrations of free
fatty acids in plasma. No differences due to treatment were detected
for birth weight, number born alive or dead or survival of piglets to
d 21 of lactation. Kveragas et al. (1986) reported that a
diabetogenic state was induced in gestating sows as indicated by the
higher concentrations of plasma glucose. Furthermore, a treatment x
diet interaction was detected, so the authors indicated that dietary
energy source should be considered when evaluating effects of
exogenous GH. Injection of GH can be fatal in sows. One sow died 3
d after treatment, while three sows died within hours after or before
parturition and exhibited respiratory distress. Thus, the proper
dosage of GH for sows during gestation and lactation warrants further
investigation.
Control and Initiation of Parturition
There are numerous reviews concerning parturition in swine
(Dziuk, 1979; First et al., 1982; Taverne, 1982; Bazer and First,
1983; First and Lohse, 1984; Guthrie, 1985) and factors influencing
piglet survival (Leman et al., 1979; Dziuk, 1979). Similar to other
reproductive processes, events at parturition can reduce potential
litter size. At least six percent of piglets are born dead (Randall,
1972; Sprecher et al., 1974; Leman et al., 1979). Furthermore, the
last piglet in each uterine horn has less than a 50% chance of
survival, according to Bevier and Dziuk (1976). Leman et al. (1979)
indicated that 20 to 25% of piglets died before weaning and that most
of this loss occurred during the first 3 days of the piglets' lives.
Furthermore, the incidence of stillbirths and perinatal deaths

64
increased as litter size increased and as the duration of parturition
increased (Leman et al., 1979). Randall (1972) concluded that piglet
survival at birth was mainly influenced by fetal hypoxia. Temporary
hypoxia during farrowing may cause permanent damage, since English
and Smith (1975) reported that piglets dying before 21 days post
partum had higher blood lactate at birth than those that survived.
By understanding mechanisms controlling parturition, ways of reducing
neonatal death losses may be developed (First et al., 1982; Bazer and
First, 1983). For example, more precise methods of pharmacologically
inducing parturition may be developed. The presence of an attendant
during parturition to assist with difficult deliveries (Hammond and
Matty, 1980) or to resuscitate piglets (Milosavljevic et al., 1972)
has been reported to save up to one additional piglet per litter. In
addition, some potential benefits of controlling time of paturition
precisely are: (1) more efficient use of farrowing facilities; (2)
occurence of births during regular working hours; (3) efficient
cross-fostering of piglets; (4) better synchronization of estrus in
sows after weaning, and (5) more uniform age and weight of piglets in
litters (Guthrie, 1985).
Hormonal changes leading to birth involve final maturation of the
fetus, termination of pregnancy, expansion of the birth canal,
synthesis of milk and the ability to eject milk (Bazer and First,
1983). Because pregnancy is maintained in the presence of functional
CL in pigs, regression of CL and loss of progesterone is the primary
requirement for parturition (First, 1979; First et al., 1982).
However, the exact nature of the initial signal for parturition and
its mode of action are not certain (First et al., 1982). It is

65
somewhat ironic that a product (estrogen) of the conceptus is
required for establishment and maintenance of pregnancy (Bazer and
Thatcher, 1977); a product of the conceptus also initiates
parturition (First et al., 1982). Cortisol clearly causes increased
PGF resulting in regression of CL. How this is accomplished has not
been determined but a proposed mechanism will be reviewed later
(First et al., 1982).
The fetal brain is required for initiation of parturition, since
decapitated (Stryker and Dziuk, 1975; Coggins and First, 1977) or
hypophysectomized (Bose et al., 1974) pig fetuses will not initiate
parturition. Furthermore, increased glucocorticoid production by the
fetal adrenal is crucial to induction of parturition. Adrenal
atrophy in fetal pigs due to hypophysectomy (Bose et al. , 1974) or
decapitation (Stryker and Dziuk, 1975) prevents parturition at term.
In sheep, fetal adrenalectomy blocks initiation of parturition (Drost
and Holm, 1968; Liggins, 1969). Administration of dexamethasone to
fetuses (North et al., 1973) or the sow (North et al., 1973; First
and Staigmiller, 1973; Huhn et al., 1976; Coggins and First, 1977;
Huhn et al., 1978; Huhn and Kiupel, 1979) induces parturition which
is followed by live birth and milk ejection. In addition, exogenous
ACTH administration to pig fetuses during the last 10 d of gestation
will cause fetal adrenal cortex hypertrophy and subsequent premature
parturition (Bose, 1973). The porcine fetal adrenal undergoes
hyperplasia and this increases its ability to synthesize
glucocorticoids late in gestation (Bose, 1973; Fevre et al., 1975;
Dvorak, 1972; Lohse and First, 1981). At d 113, the relative
proportion of cortisol in comparison to corticosterone production

66
increases in the fetal adrenal (Lohse and First, 1981). These data
and additional information reviewed by First et al. (1982) suggest
that the increased adrenal cortex weight, due to increased mitosis is
responsible for increased cortisol production from d 89 to 105.
However, the following increase in cortisol (d 105 to 113) is
believed to be due to changes in steroid ratio (First et al., 1982).
The mechanism by which the fetal brain controls the fetal adrenal
has not been defined (First et al., 1982). First et al. (1982)
suggested that control of adrenal cortisol production by the fetal
pituitary may not be the only way in which the fetal brain regulates
the initiation of parturition. First et al. (1982) indicated that,
via an action of the fetal brain, receptors for glucocorticoids must
be developed to allow cortisol to induce parturition. The placenta
may be the target organ for glucocorticoid action prior to
parturition as suggested for other species (Linzell and Heap, 1968;
Anderson et al., 1975; Flint et al., 1975). In rabbits, when fetuses
were removed on or before d 25 of gestation, parturition at term did
not occur and could not be induced by dexamethasone. However, when
fetuses were removed on or after d 26, placentae were delivered on
the expected day of parturition (d 32) (Chiboka et al., 1977). In
pigs, however, live or dead fetal tissue must be present for
pregnancy to be maintained (Chiboka et al., 1976). Whatever the
precise mechanism is, it is believed that glucocorticoids induce
parturition by increasing PGF secretion from the uterus which results
in luteolysis (Nara and First, 1978; 1981a). How fetal cortisol
increases uterine PGF synthesis and how the fetal brain regulates the
adrenal are not known.

67
Based on available evidence, First et al. (1982) proposed the
following sequence of events which lead to parturition in pigs. The
fetal hypothalamus stimulates ACTH production from the fetal
pituitary. Then either a hypothalamic factor or ACTH stimulates the
adrenal cortex to release cortisol. Cortisol or another factor of
hypothalamic origin then acts on the placenta. By some mechanism,
the placenta stimulates uterine PGF production. This may involve
increased 17-alpha-hydroxylase due to cortisol stimulation and
hydroxylase-induced estradiol production which in turn increases PGF
production. Prostaglandins can increase posterior pituitary oxytocin
secretion (Ellendorff et al., 1979) or stimulate progesterone and
relaxin secretion from the CL (Sherwood et al., 1976). In addition,
PGF increases oxytocin receptors allowing for an increased pulsing of
oxytocin and PGF. Then, the combined effects of oxytocin, PGF and
declining progesterone result in myoraetrial contractions, while
relaxin dilates the cervix to facilitate delivery of the piglets. It
is possible that the maternal central nervous system provides the
final signal for initiation of parturition in sows (Guthrie, 1985).
Once signalled to begin, parturition proceeds via coordinated
rhythmic contractions of uterine smooth muscle, involuntary
contractions of abdominal muscles and softening or opening of the
birth canal (First and Lohse, 1984). In pigs, myometrial activity
during late gestation consists of irregular episodes of prolonged
activity in those uterine segments containing a fetus, while those
parts of the uterus which are unoccupied by a conceptus are
relatively inactive (Taverne et al., 1979a). Oxytocin is low (1.3
uU/ml plasma) at this time (Forsling et al., 1979), although oxytocin

68
receptors are present in the pig uterus during late gestation (Soloff
and Swartz, 1975). Not until 9 to 4 h before birth, does myometrial
activity increase in all parts of the uterus. This increase in
activity of the myometrium occurs when concentrations of oxytocin
increase in peripheral plasma. The release of oxytocin seems to be
related to a lower progesterone:estrogen ratio, due to decreasing
progesterone and increasing estrogen (Forsling et al., 1979). In
addition, the frequency of uterine contractions during delivery is
positively correlated with oxytocin concentrations (Taverne et al.,
1979a). First and Lohse (1984) indicated that uterine contractions
are likely initiated by increased intracellular calcium in myometrial
smooth muscle and by formation of gap junctions. Gap junctions
provide low resistance coupling for communication between cells
(Peracchia, 1980). An increase in intracellular free calcium causes
formation of a calcium-calmodulin complex. This complex binds to and
activates myosin light-chain kinase, which phosphorylates myosin, and
thus allows myosin to interact with actin and cause contraction
(Adelstein and Eisenberg, 1980). Although the factors regulating
calcium flux and gap juntion formation are not well understood (Bazer
and First, 1983), prostaglandins may play a role. Prostaglandins
liberate calcium from intracellular binding sites and thus effect
tonic contraction. In addition, prostaglandins cause slow membrane
depolarization that increases the frequency of phasic contractions
(Liggins, 1979). The PGF may cause release of oxytocin in swine as
well (Ellendorff et al., 1979). As reviewed by Bazer and First
(1983) and First and Lohse (1984), oxytocin lowers the threshold for

69
initiation of potential activity and also directly influences the
rate of calcium influx.
Multiple implantation of intrauterine catheters (Zerobin, 1968)
or surface electrodes in swine (Taverne et al., 1979b) provided
evidence that myometrial contractions in all segments of the uterine
horn are synchronized during delivery. These contractions were
initiated at both ends of the uterine horn and subsequently
propagated in either a tubocervical or cervicotubal direction.
Contraction waves returned in an opposite direction upon reaching the
end of the horn (Taverne et al., 1979c; Taverne, 1982). However,
cervicotubal contractions stopped when the horn was empty and seemed
related to the presence of piglets close to the cervix. Taverne
(1982) suggested that this mechanism shortens the distance travelled
by succeeding piglets and prevents piglets from "piling up" near the
cervix. At the cervix, placental attachments could be dissociated
and cause fetal anoxia and death. In support of this idea, piglets
dying during birth are predominantly the last ones born (Randall,
1972) and usually the last piglet in each horn (Bevier and Dziuk,
1976). Although myometrial smooth muscle contractions are
synchronized, expulsion of piglets from the two uterine horns is
random (Dziuk and Harmon, 1969; Taverne et al., 1977).
In addition to uterine contractions, distension and softening of
cervical connective tissue must occur (Bazer and First, 1983; First
and Lohse, 1984). Little is known about the mechanism of cervical
softening in domestic animals (Bazer and First, 1983). However, the
involvement of relaxin on cervical distension before parturition has
been demonstrated in swine (Kertiles and Anderson, 1979; Nara et al.,

70
1982). Sherwood (1982) reviewed structure, source and function of
relaxin in swine. The principle source of relaxin in swine is CL
(Fevold et al., 1930; Hisaw and Zarrow, 1948; Nara et al., 1982).
The CL store and concentrate relaxin throughout pregnancy (Anderson
et al., 1973a,b; Kendall et al., 1978; Fields and Fields, 1985), but
this is not dependent upon conceptuses, since CL of hysterectomized
gilts also accumulate relaxin through d 124 (Anderson et al.,
1982a). Unmated gilts with CL prolonged by exogenous estrogen
(pseudopregnant) also produce and accumulate relaxin in their CL
(Anderson et al., 1973b). Relaxin is secreted or released by luteal
cells of CL (Belt et al., 1971; Kendall et al., 1978) as sustained
surges starting approximately 2 d prior to birth. Maximum values for
relaxin in maternal plasma are at 14 to 22 h prior to parturition
(Sherwood, 1982). The mode of relaxin release is not clear, but
there is evidence that secretion or release of relaxin is induced by
PGF directly (Sherwood et al., 1979; Nara and First, 1981b) or
indirectly through PGF-induced oxytocin release and subsequent
oxytocin action on relaxin secretion. There is some evidence that
timing of relaxin release may be dependent upon lifespan of CL
(Anderson et al., 1982a). Felder et al. (1986) reported that abrupt
shifts in both relaxin and progesterone secretion on d 111 to 113 in
hysterectomized and pregnant gilts. Thus, conceptus/fetal tissues
are not required for the surge of relaxin release coincident with
decreased progesterone. They also suggested that autonomous
regulation within the ovary or from the central nervous system and
pituitary gland may control relaxin and progesterone secretion. In a
recent study, Taylor and Clark (1988) provide evidence that relaxin

71
inhibits its own release from porcine luteal cells. Thus,
autoregulation may restrain relaxin secretion until the initiation of
labor. In a previous study, Taylor and Clark (1987) suggested that
prostacyclin may act alone or in combination with other prostanoids
to cause relaxin release in the pregnant pig.
Dilatation of the cervix is prematurely induced by injection of
relaxin in late pregnant gilts (Kertiles and Anderson, 1979).
Furthermore, removal of CL on d 110 of pregnancy results in difficult
delivery and a prolonged period of parturition. Relaxin replacement
to gilts without CL led to premature delivery, but short duration of
parturition with cervical dilatation (Kertiles and Anderson, 1979).
Zarrow et al. (1956) reported that relaxin caused dilatation of the
cervix, increased water content and depolymerization of cervical
glycoproteins when injected into estrogen-treated ovariectomized
nonpregnant gilts. Nara et al. (1982) found that in the absence of
the source of relaxin, delivery was prolonged and there was a high
frequency of stillborn piglets. Exogenous relaxin decreased the
duration of parturition and increased the frequency of live births
comparable to that for normal ovarian intact gilts. In addition to
inducing cervical distension, relaxin may also prevent premature
labor during late pregnancy by suppressing uterine contractions
(Porter, 1979; Taverne et al., 1979b). In summary, relaxin is
involved in cervical distensibility in swine. However, the effects
of relaxin are dependent upon prior exposure to estrogen or
progesterone followed by estrogen (Sherwood, 1982). The possibility
exists that estrogen, progesterone, prostaglandins, oxytocin and

72
other hormones are also involved in cervical distension (First and
Lohse, 1984; Sherwood, 1982).
Since pharmacological induction of parturition can benefit
management schemes and potentially decrease losses at birth,
protocols have been developed. Administration of exogenous PGF or
one of its analogues, alone, or in combination with oxytocin, is the
most effective and widely accepted method used today.
Chantaraprateep et al. (1986) reported a high number of live piglets
per litter in sows given 175 ug estrumate, a PGF analogue, on d 111
to 113 of gestation (im or iv). The authors attributed the live
piglet advantage to the presence of an attendant. Although birth
weights were less for treated sows, differences were not detected for
individual piglet weaning weights. As First and Bose (1979)
indicated, the advantage of PGF or its analogue is that these
compounds induce normal parturition, as well as, parturition-related
events including initiation of lactation and expulsion of the
placenta (First and Bose, 1979). When administered after d 110 of
gestation, most experiments show no significant difference between
treated and control sows in duration of labor, frequency of piglets
stillborn, birth weight and survival to weaning or weaning weight, as
reviewed by First et al. (1982). There is a slightly greater birth
weight for piglets from control sows, however. The doses of PGF used
in these studies ranged from 7.5 to 12.5 mg/sow (im) (Ehnvall et al.,
1976; Backstrom et al., 1976; King et al., 1979; Hagner et al., 1979;
Huhn et al., 1980). It is critical that parturition not be induced
prior to d 110 since birth weights and piglet survival will be
significantly reduced (First and Lohse, 1984).

73
When oxytocin is given after injection of PGF, delivery occurs in
approximately 27.2 + 2 h and variation in time of delivery is
significantly reduced compared to when PGF is given alone (Welk and
First, 1979). Dial et al. (1987) attempted to determine the optimal
dose and interval between PGF and oxytocin. They based their study
on the fact that although oxytocin administration 16 to 24 h after
PGF administration is effective in initiating parturition within 3 to
6 h, uterine intertia increases (Holtz et al., 1983; Dial, 1984; Welp
et al., 1984). Thus, increased perinatal mortality can result due to
the interrupted delivery. In one trial, sows were given 20 U
oxytocin 16, 20, or 24 h after PGF (Lutalyse) injection (10 mg on d
112, 113 or 114 d of gestation). There was a tendency for
intrapartum complications to be less frequent with the greatest
interval between injections. However, the results indicated that
synchrony of farrowing was greatest when the interval between
injections was reduced. Similarly, although degree of synchrony
increased with 30 U of oxytocin in comparison to lower doses, the
incidence of problems requiring manual intervention also rose.
Another approach to induce parturition in swine involves the use
of epostane, a competitive inhibitor of 3B-hydroxysteroid
dehydrogenase (3B-HSD) (Martin et al., 1987). On d 109 of gestation,
sows received either oral doses or subcutaneous injections of
epostane on a body weight basis. Farrowing occurred 31 to 77 h
later, depending on the dose. With the higher doses, farrowing
occurred within 31 to 33 h. The duration of farrowing, proportion of
piglets born live, birth weights, weaning weights, proportion of
piglets born live that were weaned and interval from weaning to first

74
postpartum estrus were not influenced by treatment. The major
influence of epostane was suggested to be through its action on
3B-HSD and subsequent removal of progesterone. Martin et al. (1987)
concluded that inhibitors of 3B-HSD could be successfully used to
induce farrowing without adversely affecting the sow or litter.
Another method to induce parturition has been reported by Guthrie
et al. (1987). Their method was developed in an attempt to reduce
the incidence of spontaneous farrowing. First et al. (1982) reported
that only 50 to 60% of sows actually begin delivery during a 10 h
interval on the expected day of parturition, because some sows farrow
before the scheduled injection of PGF. By feeding an orally active
progesterone agonist, altrenogest, early unscheduled farrowings can
be prevented (Varley et al., 1985). Therefore, Guthrie et al. (1987)
combined the advantages of altrenogest to delay parturition and PGF
to induce parturition. Oral administration of altrenogest twice
daily on four days beginning on d 109 or 110 prevented early
parturition in all sows. Injection of PGF had no adverse effects
except on lactation in 3 of 62 sows and did successfully induce
parturition. Therefore, Guthrie et al. (1987) concluded that the
combination of altrenogest followed by PGF allows better control of
the time of farrowing. However, they suggest addition of compounds
such as oxytocin or relaxin to their protocol may reduce variation in
time from administration of PGF to birth of the first piglet and
duration of parturition.
In summary, factors associated with parturition are being
elucidated and utilized to manipulate initiation of farrowing to the
advantage of the producer. However, additional experiments may lead

75
to more optimal doses of "inducing" agents and times for
pharmacological intervention.
Physiology and Characteristics of Lactation in Swine
As reviewed by Collier et al. (1984), a classic example of both
homeostasis and homoerhesis is the "redirection of nutrient flow that
occurs at parturition as site of maternal delivery of nutrients to
offspring shifts from placental transfer in the uterus to milk
synthesis, secretion and removal at the mammary gland." Lactation
provides piglets with nutrition and passive immunity against
pathogenic infections and is dependent upon: (1) supply and uptake of
metabolites from blood; (2) amount of secretory tissue present and
(3) stimuli for milk removal. Because all milk precursors are
derived from blood, blood flow to mammary glands as a precentage of
cardiac output increases during lactogenesis (Linzell, 1974) thereby
increasing nutrient delivery to and uptake by mammary glands. In
addition, adipose tissue adapts to demands of lactation under
homeorhetic regulation by mobilizing fatty acids (see Collier et al.,
1984). Four separate stages of lactation include: (1) mammary growth
(mammogenesis); (2) inititiation of copious milk secretion
(lactogenesis); (3) maintenance of milk secretion and (4) weaning
(mammary gland involution) (Hartmann et al., 1984).
Although it is essential that adequate fetal and prepuberal
mammary gland development occur, this review will only consider
pregnant and lactating sows. Hormones known to stimulate mammary
gland growth in swine are estrogens, progesterone and prolactin
(DeHoff et al., 1986); however, general metabolic hormones, e.g.,
insulin, thyroid hormones and corticoids, also affect mammogenesis.

76
Kensinger et al. (1982) indicated that the majority of mammary duct
growth of sows occurs prior to d 60 and Hartmann et al. (1984)
indicated this growth begins around d 45. Concentrations of
circulating progesterone and prolactin remain fairly constant, while
estradiol-17B increases as lobulo-alveolar development is initiated
and concentrations of mammary DNA and RNA increase (Hacker and Hill,
1972; Cowie et al., 1980; Kensinger et al., 1982). Lobulo-alveolar
development occurs between d 60 and 105, with the fastest rate of
mammogenesis occuring between d 75 and 90 (Kensinger et al., 1982).
Lyons (1958) indicated that estradiol, GH and adrenal steroids are
required for duct growth, while progesterone and prolactin, in
addition to the previous hormones, are required for lobulo-alveolar
growth, and prolactin and adrenal steroids are necessary for milk
secretion.
Lactogenesis occurs in two stages: (1) stage I, which occurs
between d 90 to 105 in pigs, is associated with increased synthesis
of fatty acids, distension of alveoli and fat droplet accumulation in
epithelial cells and (2) stage II, extending from d 112 of gestation
through parturition, which is associated with increased
concentrations of RNA and additional increases in production of fatty
acids and CO2 (Kensinger et al., 1982). In sows, alveolar
secretions begin to accumulate about 2 d prior to parturition (Cross
et al., 1958) and, normally, mammary secretion can only be expressed
within a few hours prior to parturition. Lactogenesis (stage II) has
been described by numerous researchers as the time when milk can
first be expressed; however, as Hartmann et al. (1984) suggest,
analysis of lactose may be a more sensitive indicator for the onset

77
of lactation (Willcox et al., 1983). Two theories regarding the
mechanism for the onset of lactogenesis are: (1) mammary glands are
released from inhibition by progesterone or (2) positive stimuli of
prolactin and glucocorticoids act upon the mammary gland (Kuhn, 1977;
Fulkerson, 1979; Cowie et al., 1980). Administration of progesterone
delays onset of lactation until its withdrawal (Gooneratne et al.,
1979; Taverne et al., 1982). However, it is likely that progesterone
withdrawal at parturition is not solely responsible for lactogenesis,
but is coupled to stimulatory effects of prolactin and cortisol
(Hartmann et al., 1984). In addition, declining concentrations of
relaxin may be required for lactogenesis (Cowie, 1969), as reviewed
by Hartmann et al. (1984). Tucker (1985) stated that the minimum
requirement for lactogenesis involves secretion of prolactin,
adrenocorticotrophic hormone (which stimulates secretion of
glucocorticoids), and estrogens and decreased progesterone. Cortisol
induces differentiation of rough endoplasmic reticulum and the Golgi
appartus of epithelial cells during midpregnancy in mice, which
permits prolactin to induce synthesis of milk proteins (Tucker,
1985) . Prolactin controls expression of the casein gene and other
genes, and its effects are amplified by insulin and glucocorticoids
and inhibited by progesterone (Tucker, 1985). Growth hormone appears
to act by partitioning available energy away from body tissues toward
milk production (Forsyth, 1986). Improper hormonal stimulation has
been implicated in development of mastitis-metritis-agalactia, which
results in partial or complete failure of lactation (Martin and
Threlfall, 1970).

78
Because alterations in milk composition cause changes in body
composition and growth of piglets (Williams, 1976), composition of
milk may be manipulated by dietary or pharmacological means to
advantageously influence piglet survival. Fat, protein and lactose
constitute approximately 60, 22 and 18%, respectively, of total
energy content in sow milk (Hartmann et al., 1984). Synthesis of
milk fat occurs in cytosolic secretory cells, and lipids accumulate
into droplets in vesicular cells of the basal cytoplasm which move to
the apex of cells and are then extruded (Cowie, 1984). Proteins in
milk are synthesized in endoplasmic reticulum, pass into the Golgi
apparatus where caseins undergo phosphorylation, form micelles within
vesicles and move to the cell apex for membrane fusion and subsequent
discharge of vesicle contents into the alveolar lumen (Cowie, 1984).
Lactose synthesis occurs in the Golgi in association with proteins.
The final step in lactose synthesis involves lactose synthase which
is made up of two proteins: (1) alpha-lactalburain which is
synthesized in endoplasmic reticulum and (2) galactosyl-transferase
which is synthesized in the Golgi (Cowie, 1984). Lactose synthesis
produces equimolar H^PO^ intracellularly and, in order to
neutralize H+, net anion transport occurs (Jenness, 1986). Jenness
(1986) indicated that lactose synthesis and associated anion
transport regulate swelling of Golgi vesicles which, along with rate
of passage of vesicles through cells, determines volume of milk
(aqueous) secreted. Secreted protein is diluted to its final
concentration in Golgi vesicles and dilution of fat globules occurs
in alveoli (Jenness, 1986). Since volume is regulated by lactose
synthesis, fat and protein content are inversely correlated with

79
content of lactose in milk (Davies et al., 1983). Functions of
lactose and fat include supplying energy, while protein is a source
of amino acids for growth (Jenness, 1986). The B-l,4-galactosidic
link of lactose promotes calcium absorption and, since specific
enzymes are required to hydrolyze this bond, it may prevent
intestinal fermentation (Jenness, 1986).
Linzell et al. (1969) and Spincer et al. (1969) estimated that
mammary glands of sows utilize 50 and 31%, respectively, of glucose
entering mammary circulation and glucose is the major source of milk
lactose, glycerol and mammary CO2 (Linzell et al., 1969). Although
acetate has been demonstrated to be preferentially utilized as a
substrate, it is present in low concentrations in plasma of pigs, and
therefore, glucose utilization predominates (Linzell et al., 1969;
Spincer et al., 1969; Bauman et al., 1970). Furthermore, although
glucose and acetate can be use to synthesize fatty acids de novo,
fatty acids derived from plasma triglycerides are the major source of
fatty acids in milk (Hartmann et al., 1984). Free amino acids in
plasma give rise to milk proteins. More complete reviews of
biosynthesis of milk are available (Mepham, 1983; Larson, 1985;
Jenness, 1985).
Maternal antibodies secreted into colostrum and absorbed intact
by piglets during the first 24 h after birth (Lecce and Morgan, 1962)
are critical, since piglets are born agammaglobulinaemic.
Accumulation of immunoglobulins in colostrum occurs rapidly over the
last 2 d of pregnancy, and most of these are derived from maternal
serum (Bourne and Curtis, 1973). Colostrum contains trypsin
inhibitor (Jensen and Pedersen, 1979) which protects immunoglobulins

80
from intestinal proteolysis. Concentrations of all immunoglobulins
in mammary secretions fall rapidly during the first 24 h after
parturition (Curtis and Bourne, 1971). As reviewed in a separate
section, piglets are extremely susceptible to hypoglycemia (Edwards,
1972), so during the first few hours post-partum, intake of colostrum
is critical. Although colostrum contains 586 to 628 kJ energy/100 ml
(Salmon-Legagneur and Guegen, 1962), its energy is limited since it
contains immunoglobulins which will be absorbed intact and not
contribute to energy. Differences in composition of milk and
colostrum are due to the rapid decline in immunoglobulins and casein
during the first few days after parturition and increased
concentrations of lactose (Brent et al., 1973). Klobasa et al.
(1987) reported that concentrations of IgG, IgM and IgA in colostrum
declined by 50% during the first 12 h after parturition. Since
immunoglobulins, especially IgG, are the predominant proteins in
colostrum, total protein content during the first 12 h of lactation
also declined by nearly 50%. Total solids concomitantly declined
during the first day of lactation; however, fat and lactose content
increased at this time. At birth, composition of sows' colostrum was
25.6% total solids, 5.0% fat, 3.1% lactose, 15.7% total protein and
14.3% whey protein. In contrast, at 21 d of lactation, composition
of milk was estimated to be 18.7% total solids, 6.6% fat, 5.8%
lactose, 5.2% total protein and 2.8% whey protein (Klobasa et al.,
1987)', which agrees with estimates of milk composition obtained on d
22 of lactation by White and Campbell (1984). Similar composition of
sows' milk (percent by weight) has been reported by others to be
81.2% water, 6.8% fat, 2.8% casein, 2.0% whey protein, 5.5% lactose

81
and 1.0% ash, which would supply approximately 102 kcal energy/g of
milk (Jenness and Sloan, 1970). Long (1961) estimated concentrations
(g/100g) of ash, fat, lactose, and protein in milk of sows with
values of .6, 8.2, 4.8, and 5.8, respectively.
Hartmann et al. (1984) indicated that with increased litter size
from highly selected sows and decreased neonatal deaths in
technologically sophisticated piggeries, "milk production is now one
of the most important factors limiting piglet growth and, ultimately,
pig production." Lewis et al. (1978) concluded that variability in
milk yield among sows accounts for approximately 33% of the
variability in weight gain of piglets. Milk yield is determined by
epithelial cell number and by secretory activity of cells (Forsyth,
1986) . Regulation of milk yield is influenced by suckling intensity
of piglets postpartum (Blaxter, 1961) and possibly by prepartum
factors. For example, Elsley (1971) demonstrated that milk yield of
sows is related to litter size, but it is not clear whether this
regulation is entirely due to suckling and milk removal or whether
development during pregnancy may be involved (see Forsyth, 1986).
However, greater fetal numbers were not associated with additional
increases in mammary development (Kensinger et al., 1980). Milk
yield can be assessed by: (1) differences in piglet weights or sow
weights before and after suckling (Braude, 1954; Lewis et al., 1978);
(2) milking sows by hand or machine at intervals following oxytocin
injection (Hughes and Hart, 1935; Hartmann and Pond, 1960; Linzell et
al., 1969); (3) isotope dilution (Yang et al., 1980) and (4) isotope
transfer (See Oftedal, 1984). Estimates of daily milk yield of sows
between d 7 and 28 of lactation range from 5 to 13 kg/d (White and

82
Campbell, 1984; White et al., 1984a; Coffey et al., 1987). English
et al. (1982) and White and Campbell (1984) detected greatest milk
yield at approximately 3 wk of lactation. Yield during an 8 wk
lactation has been estimated to average 5.8 kg/d (Smith, 1952; Barber
et al., 1955; Smith, 1959; Hartman et al., 1962). Peak yields
occurred between the third and fifth wk and yields slowly declined by
the ninth or 10th wk (Allen and Lasley, 1960). Thus, early weaning
can result in the inability of sows to reach peak production. Yield
is also influenced by parity; yield increases from the first to third
lactation (Smith, 1959; Van Spaendonck, 1967). In addition, sows in
good condition produce more milk than thin sows even when thin sows
are fed extra energy during early lactation (Klaver et al., 1981).
As previously mentioned, milk yield is a linear function of rate of
blood flow to mammary glands (Kronfeld, 1969). Increasing
photoperiod from 8 to 16 h per d increased milk production by 20%,
litter weight at 21 d by 13% and piglet survival by 10% (Mabry et
al., 1982).
Suckling is required to maintain lactation; unsuckled mammary
glands involute rapidly (Cross et al., 1958; Martin et al., 1978).
Suckling maintains lactation, in part, through its stimulation of
prolactin (Bevers et al., 1978), a necessary hormone for maintenance
of lactation (Schams, 1976). During lactation, concentrations of
prolactin in serum are between 3 and 8 ng/ml compared to 1 to 2 ng/ml
after weaning (Bevers et al., 1978; Mulloy and Malven, 1979).
Administration of bromocryptine, a dopamine agonist, inhibits
prolactin secretion and prevents milk secretion in swine. In
addition to its requirement for milk synthesis, suckling behavior

83
is required for milk ejection through stimulation of oxytocin
release. It is generally accepted that a discrete release of
oxytocin is responsible for milk flow at each suckling (Cross,
1977). However, relaxin may help regulate the duration of milk
release (Afele et al., 1979). Milk is ejected from alveoli by
myoepithelial cell contractions in response to oxytocin which leads
to increased intramammary pressure (Cowie, 1984). Estimates of
suckling frequency vary from 12 to 18 times per 24 h (Hughes and
Varley, 1980) to once every 55 to 65 min for 2 to 3-wk-old piglets
(Whittemore and Fraser, 1974).
Influence of Nutrition on Sow Performance During Lactation
Nutrition of sows during lactation is designed to maximize milk
production and minimize body weight and fat losses. However,
nutrition during lactation also impacts short- and long-term post-
weaning reproductive efficiency (see Britt et al., 1985). Nutrient
requirements and composition of the diet during lactation are
influenced by nutrient intake during gestation, weight and condition
of the sow at onset of lactation, as well as milk yield and
composition which are influenced by litter size, seasonal or
temperature variations and stage and duration of lactation. In
addition, O'Grady (1985) indicated that energy and protein allowances
for lactation must be related to expected life of sows and, if
multiple litters are expected, allowances must permit maintenance of
body fat reserves. If protein intake is inadequate (O'Grady and
Hanrahan, 1975), sows will draw upon their own reserves to meet
demands for secretion of milk proteins and consequently lose
weight. Often, long term effects of nutrition and weight loss

84
during lactation on sow productivity have not been investigated.
Numerous reviews have addressed nutritional needs of lactating sows
(Cole, 1982; O'Grady, 1985; Aherne and Kirkwood, 1985; Britt, 1986).
Relative to those of pregnancy, nutritional requirements to meet
the demands of milk production are high (Cole, 1982). Energy
consumption of sows during lactation influences: (1) litter size
weaned; (2) days to estrus after weaning and (3) subsequent litter
size (Lewis and Reese, 1986). Evaluating effects of increased
energy, specifically, is difficult in numerous experiments, because
greater intakes of all nutrients occurred. In addition, carry-over
effects of energy and(or) feed intake during gestation influence
energy intake during lactation and vice versa (Salmon-Legagneur and
Rerat, 1962). Sows that consume the most feed during pregnancy lose
the most weight during lactation (Salmon-Legagneur and Rerat, 1962;
Sterling and Cline, 1986). However, if feed intake is increased
during the latter part of pregnancy (d 105 of gestation through
lactation), lactational performance may be improved without having a
detrimental effect on sow weight loss (Sterling and Cline, 1986).
Mahan and Mangan (1975) provided evidence of an interaction between
protein level fed thoughout gestation and voluntary intake of gilts
during lactation. If high levels of dietary protein (18%) were
supplied during lactation, feed intake during lactation was
independent of dietary protein level fed during gestation. However,
if a 12% crude protein diet was fed during lactation, feed intake
during lactation was linearly related to level of protein fed during
gestation. Results obtained over three or four reproductive cycles
by O'Grady and Hanrahan (1975) confirmed those findings. Results of

85
a larger study indicated that it may be most beneficial to production
to feed diets (13% crude protein and .6% lysine) which provide
similar protein levels during pregnancy and lactation (Greenhalgh et
al., 1977).
Quality and quantity of milk produced are the two major factors
influencing dietary protein requirements during lactation. Cole
(1982) indicated that milk yield is affected by litter size and stage
of lactation which, in turn, affects the amount of energy required
for lactation. Changes in milk composition are most evident early in
lactation when production changes from colostrum to milk. Protein
content of milk declines over the first 10 to 14 d and fat production
increases during the first 3 d. Thereafter, secretion of milk
protein gradually increases and fat synthesis decreases (see Cole,
1982) . While milk yield influences the amount of nutrients required,
plane of nutrition influences milk production especially during the
first 3 wk of lactation (Lodge, 1972). O'Grady (1985) indicated that
the greatest requirement for dietary protein is within the first 2 wk
of lactation. Research comparisons and recommendations have been
complicated because length of lactation periods have varied from two
to eight weeks in available literature. O'Grady (1985), for example,
calculated dietary protein requirements after consideration of
protein in milk and milk yield, as well as estimated feed intake and
stage of lactation.
Litter size weaned was increased only slightly when metabolizable
energy (ME) [>14 Mcal/(sow • d)] intake during lactation was
increased for sows ranging in parity from 1 to 4 and lactation
periods of 4 to 8 wk (Elsley et al., 1968; Hitchcock et al., 1971;

86
O'Grady et al., 1973; Adam and Shearer, 1975; Reese et al., 1982a;
King and Williams, 1984a). When litter size is increased, greater
energy consumption by sows may be accompanied by greater milk yields
due to sows consuming higher levels of energy. Shurson et al. (1986)
reported that greater energy intake due to inclusion of 10% fat in
the lactation diet increased litter size (8.9 vs 8.4) and litter
weight (56.1 vs 48.9 kg) at 21 d of age. Sow milk yield was
increased by 13.1% for sows consuming fat and this may have been
responsible for increased litter size at weaning. Sterling and Cline
(1986) indicated that ad libitum feeding in late gestation (d 105 to
farrowing) followed by ad libitum feeding of a diet containing 5%
soybean oil during lactation improved milk yield. Feed intake during
lactation and birth weight of piglets were not influenced by ad
libitum feeding of diets containing soybean oil. In spite of
improved milk yields for sows fed ad libitum diets containing soybean
oil, number of piglets born alive was less for ad libitum fed sows.
Nelssen et al. (1985a) utilized 146 primiparous sows to
investigate effects of intakes of 10, 12, or 14 Meal ME/(sow ' d)
during a 28 d lactation. Sow weight and backfat loss decreased
linearly as energy intake increased. No differences in litter size
at d 14 or at weaning were detected. However, on d 14, pig weights
increased (P < .05) and litter weights tended (P = .13) to increase
linearly as energy intake of sows increased. At weaning, pig weights
and litter weights increased (P < .05) as energy intake of sows
increased. The authors concluded that intakes of 10 Meal ME/(sow •
d) decreased sow and litter performance, while little difference in
performance was detected from feeding 12 or 14 Meal ME/(sow ‘ d).

87
Therefore, NRC (1979) recommendations of 12.8 Meal ME/(sow ' d)
appear to be adequate for lactating sows. However, carry-over
effects to subsequent farrowings were not determined. Dulohery et
al. (1986a,b) reported effects of increased energy during lactation
[8 vs 16 Meal ME/(sow * d)] and subsequent postweaning [5.75 vs
11.5 Meal ME/(sow ‘ d)] intervals on sow and litter performance in
first and second parity sows during 21 d lactations. Litter weight
gain and pig weaning weights were increased and sow weights and
backfat losses were reduced by increased dietary energy.
Seerley et al. (1974) were the first to report that
supplementation of sow diets with lipids (corn oil) had beneficial
effects on piglet performance. Piglet survival to d 21 was increased
by adding corn oil to sows' diets from d 109 through parturition due,
in part, to increased glycogen stores for piglets at birth.
Subsequently, numerous researchers reported that adding fat to sow
diets during late gestation and early lactation improved survival
rates for newborn pigs (Moser and Lewis, 1980; Pettigrew, 1981;
Moser, 1985). Milk yield and(or) composition is improved by addition
of lipids to sow diets (Friend, 1974; Kruse et al., 1977; Coffey et
al., 1982). There is evidence that addition of fat to sow diets
confers advantages on piglet survival that are not obtained when
equivalent amounts of ME are from other energy sources. However,
piglet survival in response to fat supplementation has been varied
and somewhat inconsistent.
Moser (1984) reported that addition of fat to lactation diets of
sows increased ME intake an average of 6.5% over standard lactation
diets. In sow herds which consume an average of 3.0 kg/d of a

88
corn-soybean meal diet, fat supplementation may be a desirable method
of increasing energy intake by lactating sows (Cox et al., 1983a).
However, for sow herds in which consumption is greater than 4.5 kg/d,
fat supplementation (7% added tallow) resulted in only a slight
improvement in litter weights at weaning (Moser et al., 1985a,b).
Thus, addition of dietary fat during lactation is most effective
during periods of hot weather or when feed intake is reduced (Cox et
al., 1983a). Moser (1985) summarized results of numerous experiments
involving supplementation of diets with fat before and(or) after
farrowing. Type of fat varied from corn and soybean oils to tallow
and lard, while level of fat varied from 2 to 40% and the duration of
feeding fat varied from 5 to 135 d. Moser (1985) indicated that
dietary fat was more beneficial during either gestation or lactation,
rather than during both intervals in terms of number of piglets
weaned per litter. Dietary fat during lactation did not benefit
piglet survival as much as when it was consumed during gestation only
or during both gestation and lactation. Piglet survival appears to
be enhanced by increased fat content of colostrum and(or) milk
following dietary fat supplementation for sows.
Nelssen et al. (1985b) indicated that replacement of cornstarch
with tallow was not beneficial in diets for primiparous sows during
lactation when energy intake was restricted. Unlike situations in
poultry where an extracaloric effect of fat was reported (Sibbald et
al., 1962; Vermeersch and Vanschoubroek, 1968; Jensen et all, 1970;
Gomez and Polin, 1974; Whitehead and Fisher, 1975), lactational
performance of sows on a low level of energy intake was not improved
by replacement of carbohydrate with fat on an isocaloric ME basis.

89
Nelssen et al. (1985b) indicated that greater weight loss for sows
fed a tallow containing diet may have been due to poor digestion of
tallow or preferential shunting of fatty acids directly to mammary
gland tissues. Reese et al. (1982a) reported increased, but not
statistically significant, backfat losses for sows fed tallow due to
their increased dependence on body fat to continue to lactate under
conditions of severe energy restriction. Nelssen et al. (1985b)
reported that concentrations of blood urea fell slightly from d 14 to
28 for sows fed constarch, but increased for sows fed tallow. Since
concentrations of urea in plasma provide an index of catabolism of
amino acids, their data indicated that catabolism was more extensive
in sows fed tallow than cornstarch. Nelssen et al. (1985b) suggested
that greater amino acid degradation by sows fed tallow occurred, in
part, because less substrate was available from dietary sources for
lactose synthesis and digestibility was less for tallow. Boyd et al.
(1982) added 8% tallow to lactation diets and increased fat and
solids in milk, milk yield and weaning weights of piglets.
Shurson et al. (1986) reported effects of supplemental fat (10%)
and season in a 2 x 2 factorial arrangement of treatments. For sows
that received fat supplemented diets ad libitum from 1 wk prior to
farrowing thoughout a 28 d lactation period. Weight losses were
unaffected by diet or season; however, birth weights were higher for
piglets born during the summer and sows receiving fat had heavier
litter and individual pig weights at d 21 of lactation. Enhanced
piglet performance was attributed to a 13.1% increase in milk yield
and greater fat concentrations in milk of sows fed fat supplemented
diets.

90
Brendemuhl et al. (1987) examined the combined effects of protein
and energy intake during a 28 d lactation on sow and litter
performance utilizing a 2 x 2 factorial arrangement of protein [380
or 760 g crude protein/(sow ’ d)] and energy [8 or 16 Meal ME/(sow
• d)] intakes. At d 14, piglet weights were not affected by
dietary energy or protein in sow diets. However, at d 28, sows fed
high energy or high protein diets had heavier pigs. Energy level did
not affect litter size or weight at either d 14 or 28. However, at d
28, sows fed high protein diets had heavier litters even though
litter size was smaller. These results agree with those of Elsley et
al. (1968) and Adam and Shearer (1975) who detected increased piglet
weights in litters from sows fed increased dietary energy. However,
results of Brendemuhl et al. (1987) are not supported by those of
others who reported decreased litter weights in sows fed 8 Meal
ME/(sow ' d) (Reese et al., 1982a, b; Nelssen et al., 1985a).
Brendemuhl et al. (1987) reported that weight loss was greater in
both the low protein and low energy fed sows during both the first
and second 2 wk lactation periods. Sows fed low energy diets lost
more backfat during the first and second 14 d intervals. Backfat
losses were not influenced by dietary protein during the first 14 d,
but sows fed high protein diets lost more backfat during the second
14 d interval. Although weight losses for sows fed high energy-low
protein diets and low energy-high protein diets were similar, large
differences in backfat loss were detected, indicating that
composition of weight loss was different. Brendemuhl et al. (1986)
reported effects on carcass composition of the sows when slaughtered
after weaning; protein and energy interactions were detected. Water,

91
protein, fat, ash and total weight of many organs and carcass samples
increased more in response to energy when high levels of dietary
protein were fed. Heart, kidney and liver tissues contained less
protein when sows were fed low levels of dietary protein. More fat
was measured in longissimus muscle, right shoulder and supraspinatus
muscle sections when sows were fed high levels of dietary energy.
The different composition of weight loss may affect milk production
and subsequent reproductive performance.
Body condition of the sow entering lactation influences expected
efficiency of conversion of dietary energy to milk energy (O'Grady,
1985). If sows are fed 25 MJ DE/d in pregnancy, it is recommended
that sows receive an average of 80 MJ DE/d during lactation (based on
an average of three lactations/sow). However, if sows are in a
negative energy balance at onset of lactation, dietary energy
conversion to milk energy is higher (48% versus 32% for sows in a
positive energy balance). Although this appears to be an economic
advantage initially, sows in poor condition will be in a catabolic
state and less dietary energy will be available for maintenance of
the sows energy reserves. Therefore, it is beneficial to feed sows
during gestation so that they will be in a positive energy balance
when entering lactation and maintain adequate body fat reserves.
Noblet and Eteinne (1987) addressed the topic of utilization of
metabolic energy and maintenance requirements for lactating sows by
measuring metabolic and energy balances of litters. Data were used to
estimate maintenance requirements for sows and efficiency of
utilization of energy from food and body reserves for milk
production. The nitrogen balance of the sows was also determined.

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Energy restriction and increased milk production with advanced
lactation increased mobilization of body reserves. Increased weight
loss following energy restrictions was attributed primarily to fat
depletion. However, depletion of muscle represented a rather large
proportion of weight loss, even for sows fed higher energy levels.
Maintenance requirements were calculated to be 109 kcal ME/kg
weight"^"* - d’^. Noblet and Etienne (1987) indicated that
overall efficiency of energy storage during pregnancy and its
mobilization during lactation (68.6 to 70.9%) was similar to that of
direct utilization of ME during lactation.
In addition to energy and crude protein requirements during
lactation, Lellis and Speer (1985) established requirements for
aromatic amino acids during lactation. If natural ingredients are
fed, .75% of the diet should be aromatic amino acids. Similarly,
Lellis and Speer (1983) addressed the issue of nutrient balance for
lactating sows fed supplemental fat. Guidelines for requirements are
available (NRC, 1979); however, most fail to consider interactions
between dietary components, parity and carry-over effects on
subsequent reproductive performance.
Influence of Nutrition on Post Weaning Sow Performance
Lactation
Early research failed to demonstrate an influence of energy
intake during lactation on weaning to remating interval (O'Grady et
al., 1973, 1975). However, sows in these trials had considerable
backfat reserves and the level of digestible energy (DE) restriction
was not severe [50 to 80 MJ DE/(sow ’ d)]. It is now well
documented that energy and protein intake during lactation affect

93
rebreeding performance (King et al., 1982a; Reese et al., 1982a,b;
Hughes et al., 1984; King and Williams, 1984a,b; King et al., 1984;
Reese et al., 1984). Sows that lose less weight during lactation,
rebreed sooner after weaning and have a lower incidence of anestrus
than those having greater weight loss (Etienne and Duee, 1976;
Lengele, 1978; Miyajima et al., 1979; Van der Heyde et al., 1980; Den
Hartog and Van der Steen, 1981; Cox et al., 1982; Armstrong and
Britt, 1984; Aherne and Kirkwood, 1985).
Aherne and Kirkwood (1985) summarized previous results (Reese et
al., 1982a,b, 1984; King and Williams, 1984a; King et al., 1984)
according to energy intake. When energy intake during lactation was
less than 50 MJ DE/(sow ' d), the percentage of sows returning to
estrus was 55 at d 8 and 64.8 by d 14 after weaning. At d 21, 20.1%
of the energy restricted sows were anestrus. In sows consuming
greater than 50 MJ DE/d, 86.9 and 95 percent were in estrus by d 8
and 14, respectively, and only 1.2% were anestrus at d 21. Weight
change had little influence on the postweaning interval to estrus,
but backfat loss was higher (P = .1), percent body fat was lower (P <
.05) and muscle wastage was evidenced by increased concentrations of
creatinine in serum of anestrous sows (Reese et al., 1984). Others
verified the increase in concentrations of creatinine in serum due to
low dietary energy intake (Dulohery et al., 1986a). There was no
major advantage to feeding more than 50 MJ DE/(sow ‘ d) (Reese et
al., 1982a), but intakes of 50 MJ DE/(sow • d) during lactation
were required for follicular development after weaning (Reese et al.,
1982a; King and Williams, 1984a; Reese et al., 1984). A deficiency
of either energy or protein reduces follicular development after

94
weaning (Svajgr et al., 1972; O'Grady and Hanrahan, 1975; King and
Williams, 1984b). The National Research Council (NRC, 1979)
recommends a minumum ME intake of 12.8 Mcal/d for sows during
lactation. Reese et al. (1982a) found that the percentage of
primiparous sows exhibiting estrus within 7 d after weaning was
greater than 90% when sows were fed > 12 Meal ME/d, but was less than
65% if sows were fed 8 Meal ME/d. Nelssen et al. (1985a) reported no
significant differences in the percentage of primiparous sows in
estrus by d 7, 14, 21 or 70 postweaning when fed 10, 12 or 14 Meal
ME/d during a 28 d lactation period. However, there was a slightly
longer interval from weaning to first estrus when primiparous sows
were fed 10 Meal ME/d.
Since adequate energy and protein are required to avoid
rebreeding problems, Britt (1986) indicated that dietary energy
density and protein should be increased in certain situations. He
stated that voluntary feed intake during lactation is often
overestimated by producers, and that primiparous sows consume less
feed than multiparous sows. The suggestion of reduced consumption
(Britt, 1986) is supported by Johnston et al. (1986) in a study in
which very few sows consumed their total daily allottments of 4.09 to
4.54 kg/(sow ’ d). In addition, hot weather and dietary
composition influence feed intake. Cox et al. (1983a) reported that
breeding performance following weaning was increased in primiparous
sows fed fat during the summer, but not winter since the postweaning
interval to estrus was not increased for control sows during the
cooler months. Cole (1982) indicated that sows weaning their first
litter are more susceptible to reproductive failure and benefit from

95
extra dietary energy intake, while sows weaning their third litter
have reached their peak reproductive state. Inclusion of high levels
of protein in the lactation diet of first litter sows may also have a
positive influence on reproductive performance (Svajgr et al.,
1972). However, Armstrong and Britt (1984) reported that energy
restriction (60% as much energy as ad libitum fed sows) during
lactation did not influence the weaning to estrus interval, frequency
of postweaning anestrus or LH and estradiol levels.
Armstrong and Britt (1984) indicated that sows fed energy
restricted diets lost more backfat and weight during lactation and
had higher postprandial blood levels of urea nitrogen. Nelssen et
al. (1985a) confirmed these results in a study of sows consuming 10
vs 12 or 14 Meal ME/(sow ‘ d). Brendemuhl et al. (1987) detected
no difference in interval from weaning to estrus in primiparous sows
due to variation in level of energy supplied during lactation.
However, as dietary energy or protein consumption increased
concentrations of urea in serum decreased. Nelssen et al. (1985a)
reported that, although not significant, levels of creatine in serum
were lower for sows consuming higher levels of energy indicating less
protein catabolism. Nelssen et al. (1984) also reported that sows
restricted in energy intake during lactation that failed to return to
estrus postweaning were also hypothyroid compared to sows which were
fed adequate energy and did return to estrus. Brendemuhl et al.
(1987) confirmed that anestrous sows tend to be hypothyroid. In
addition, although sow energy intake did not affect the interval from
weaning to first estrus, the percentage of sows in estrus by d 7, 14,
and 35 postweaning were higher (P < .004, P < .030 and P < .060,

96
respectively) for sows fed the higher protein level [760 vs 380 g
crude protein/(sow ' d)].
Armstrong et al. (1986c) indicated that dietary treatment did not
alter reproductive performance in their study; however, sows that
mobilized less body tissue during lactation returned to estrus
sooner. Aberrations in energy metabolism during lactation and after
weaning may have predisposed certain sows to experience postweaning
anestrus. Armstrong et al. (1986c) suggested that anestrous sows may
not have a metabolic state that spares glucose because preprandial
glucose concentrations in plasma were greater and concentrations of
free fatty acids were lower on d 12 and 20 of lactation for anestrous
sows than for sows that exhibited estrus. Preprandial PRL:insulin
ratios on d 22 were greater for anestrous sows (30.5) than for sows
that exhibited estrus (9.1). Higher PRL may affected metabolism of
lactating sows by mediating anabolic actions of insulin. Increased
concentrations of PRL in serum are associated with decreased numbers
of insulin receptors on adipocytes and increased numbers of insulin
receptors on mammary epithelial cells (Flint et al., 1979b; O'Keefe
and Cuatrecasas, 1974). In addition, energy restricted sows
continued to catabolize protein for energy after weaning, as
indicated by higher concentrations of urea nitrogen in plasma
postprandially on d 4 after weaning.
Armstrong et al. (1986c) confirmed reports that postweaning
anestrus is due to aberrations in the pattern of GnRH release (Britt
et al., 1985), since the frequency of LH secretion was greater before
weaning in sows that did exhibit estrus after weaning compared to
sows that remained anestrus. Weight loss is negatively correlated

97
with concentrations if LH in plasma during the postpartum interval to
estrus (Nelssen et al., 1984) and this may be responsible for
anestrus in thin sows or those in a negative energy balance.
Pituitary LH stores are also lower in gilts fed very low levels of
energy (Aherne and Kirkwood, 1985). Kirkwood and Aherne (1985)
suggested that alterations in amount and type of estrogens produced
by adipose tissue metablism of androgens during lactation influence
body fat reserves. Armstrong et al. (1986c) indicated that
physiological mechanisms by which energy metabolism during lactation
affect endocrine status of sows before and after weaning remain to be
determined.
Armstrong and Britt (1987) utilized intact and ovariectomized
gilts to evaluate effects of feed restriction on the ovary, anterior
pituitary and hypothalamus. They tested the hypothesis that
nutritionally-induced anestrus results from decreased action of the
hypothalamic pulse generator (GnRH) controlling LH release. Response
to hourly administration of exogenous LH or GnRH on follicular growth
and ovulation in nutritionally anestrous gilts was assessed since
those gilts have suppressed episodic release of LH. In control,
ovariectomzied gilts, episodic release of LH was circhoral (5.8 to
6.3 peaks/6 h), while in ovariectomized, feed restricted gilts, only
1.8+1 peaks/6 h were detected. Mean concentrations of LH were not
different because amplitude of LH was greater in feed restricted,
ovariectomized gilts. Episodic secretion of FSH was not detected
which is consistent with evidence that LH and FSH secretion are
regulated by separate mechanisms (Stevenson et al., 1981). Chronic
restriction of feed intake did not suppress responsiveness of the

98
anterior pituitary to GnRH. Clark and Cummins (1985) demonstrated
that frequency of GnRH stimulation and quantity of releasable LH are
inversely related. Thus, Armstrong and Britt (1987) concluded that
endogenous GnRH stimulation may be less in feed restricted gilts
which have greater LH release in reponse to exogenous GnRH.
Anestrus induced by feed restriction can be reversed by
increasing feed intake. Resumption of estrous cycles is preceeded by
an increase in body weight as well as an increase in concentrations
of LH and frequency of release of LH pulses. These results are
consistent with the hypothesis that the primary effect of feed
restriction is at the level of the hypothalamus. Originally,
Armstrong and Britt (1987) suggested that feed restriction may be
associated with increased concentrations of opioid peptides in the
hypothalamus. Naloxone infusion as a single dose, however, had no
effect on LH secretion in feed-restricted gilts. But when given over
a 5-h period, naloxone allowed resumption of pulsatile LH secretion
in 2 of 6 nutritionally-anestrous gilts. The exact role of opiod
peptides in mediating effects of feed restriciton on LH secretion
were not determined.
Differences in insulin status may alter GnRH secretion.
Postprandial concentrations of insulin in plasma of ovariectomized
feed restricted gilts are higher than those for ad libitum fed
ovariectomized gilts (Cox et al., 1987). Receptors for insulin are
present in the median eminence (Landau et al., 1983; van Houten et
al., 1983) and glucose uptake by the hypothalamus is insulin
dependent (Debons, 1969). In addition, Cox et al. (1987) determined

99
that exogenous insulin increased the frequency of LH release during
the follicular phase.
In conclusion, Armstrong and Britt (1987) indicate that feed
restriction causes cessation of estrous cycles by decreasing the
pulse frequency of the LH pulse generator. Exogenous GnRH or LH
induce ovarian follicular growth, estradiol secretion increases and
basal concentrations of LH are elevated within 3 to 5 d after
treatment with GnRH or LH. Estrus can be induced in primiparous
anestrous sows at d 35 after weaning following deprivation of protein
(2% crude protein in gestation; 5% crude protein during lactation) by
administration of eCG (1500 IU) followed by hCG (750 IU) 90 h later.
The sows exhibited estrus 12 to 36 h after hCG and ovulated normally
(Svagr et al., 1972). Although, Armstrong and Britt (1987) utilized
ovariectomized and intact gilts as their model, results of their
study help to explain mechanisms associated with anestrus in sows
which have lost body weight and body fat during lactation.
In addition, to influencing the postweaning interval to estrus,
weight change during lactation may influence ovulation rate during
that estrus (Hardy and Lodge, 1969). Brooks (1982) suggested that
gilts in a catabolic condition following lactation had decreased
ovulation rates while other investigators have not detected effects
of lactation weight loss on ovulation rate (Pike and Boaz, 1972; King
et al., 1982a; Hughes et al., 1984; King and Williams, 1984a,b).
Hardy and Lodge (1969) reported adverse effects of sow weight
loss during lactation on subsequent conception rates which have not
been confirmed by others (Reese et al., 1982b; King et al., 1984;
King and Williams, 1984a). That these contrasting results could be

100
due to poor estrus detection was suggested by Aherne and Kirkwood
(1985). King and Williams (1984a,b) did not observe an influence of
low energy and protein during lactation on embryonic survival in
subsequent pregnancies. However, adverse effects of low levels of
feed intake were detected in other studies (King et al., 1984; Hughes
et al., 1984). Embryonic survival of sows fed 3 kg/d was 63.4%
compare to 75.3% for sows consuming 7 kg/d. Armstrong and Britt
(1986c) reported that size of subsequent litters was related to
energy metabolism 2 to 4 d prior to the first postweaning estrus.
Sows with lower preprandial concentrations of glucose at 2 to 4 d
prior to estrus farrowed larger litters (P < .05) and concentrations
of glucose and insulin 2 to 4 d prior to estrus accounted for 61% of
the variation in subsequent litter size. In some respects, this is
in contrast to results of Jones et al. (1983) who indicated that
administration of insulin prior to estrus resulted in increased
ovulation rates in gilts. Aherne and Kirkwood (1985) questioned
whether lactation losses affect only those sows that are already
thin. Thus, it may not be backfat loss during lactation but a
minumum level of backfat which is associated with increased embryonic
losses. If lactation losses influence embryonic survival, the
mechanism responsbile has not been established. Aherne and Kirkwood
(1985) suggested that the problem may be similar to that of early
weaning. For example, Kirkwood et al. (1984a,b) reported that
secretion of LH in the preovulatory period following short lactations
was decreased which may influence luteinization of CL and their
subsequent secretion of progesterone. In addition, Hughes et al.
(1984) reported lower concentrations of progesterone in plasma during

101
early pregnancy (P. E. Hughes, personal communication cited by Aherne
and Kirkwood, 1985) and greater clearance rates for progesterone in
sows receiving low levels of feed during the previous lactation
leading to increased embryonic mortality. Bensadoun and Reid (1962)
reported that plane of nutrition influences hepatic blood flow in
sheep. Aherne and Kirkwood (1985) suggested that excessive body
weight and body fat losses during lactation may result in increased
hepatic blood flow and, therefore, increased metabolic clearance
rates for progesterone.
Post Weaning
After weaning the piglets, sow management goals include
shortening the interval from weaning to estrus, synchronizing estrus
and maximizing ovulation and conception rates. Initially, a "drying
off period" in which sows received no food or water was recommended
to synchronize estrus and shorten the postweaning interval to estrus
(MacLean, 1969). However, no benefit (Allrich et al., 1979; Tribble
and Orr, 1982) or even detrimental effects in some cases (Allrich et
al., 1979) are associated with food deprivation after weaning.
Increasing feed intake after weaning (Brooks and Cole, 1972) or
supplementing rations with 10% fat during the summer (Cox et al.,
1983a) increased the number of primiparous sows returning to estrus
within 10 d after weaning and increased synchrony of estrus if
control sows had prolonged remating intervals from weaning to
estrus. King and Williams (1984a) did not detect differences in
postweaning sow performance due to increased energy consumption by
weaned primiparous sows. In addition, Cox et al. (1983a) detected no
beneficial effect of dietary fat supplementation for sows weaned in

102
the winter. Multiparous sows do not have short postweaning intervals
to estrus in response to increased feed intake after weaning (Dyck,
1972, 1974; Brooks et al., 1975; Fahmy and Dufour, 1976; Tribble and
Orr, 1982). Aherne and Kirkwood (1985) indicated that response to
diet during the postweaning periods depends on parity and body weight
change and(or) feed intake of sows during lactation. Generally, high
energy intake after weaning is unlikely to improve reproductive
performance of sows unless there was poor nutritional management
during lactation (Pike and Boaz, 1972; Aherne and Kirkwood, 1985) or
other factors, e.g., season, which impair reproductive performance of
sows. However, Dulhorey et al. (1986a,b) fed the same lactation
treatments [8 or 16 Meal ME/(sow ' d)] and postweaning treatments
[5.75 and 11.5 Meal ME/(sow â–  d)] throughout two parities and,
although no major effects on sow reproduction were detected, second
parity litter size was influenced favorably by greater energy
intake. In contrast, Johnston et al. (1986) indicated that increased
energy intake during lactation and the postpartum period lengthened
the postweaning interval to estrus in primiparous sows. Postweaning
feeding levels [5.54 vs 9.61 Meal ME/(sow ' d)] or lactation
treatments [12.5 vs 16 Meal ME/(sow - d)] did not influence
postweaning interval to estrus. However, a lactation dietary
treatment x postweaning dietary treatment interaction (P < .01) was
detected since the interval from weaning to estrus was reduced as
lactation energy increased for sows previously fed a low energy
diet. When sows received high energy diets postweaning, the
postweaning interval to estrus was lengthened as energy intake
increased. The authors concluded that feeding 12.5 Meal ME per sow

103
per day during lactation, as recommended by the NRC (1979), supports
acceptable postpartum reproductive performance. Feeding higher
energy levels continously may have detrimental effects on postweaning
reproductive performance of sows.
Factors Influencing Piglet Survival
Preweaning mortality rates have been estimated to be as high as
10 to 20% (Spicer et al., 1986). Newborn pigs are susceptible to
hypothermia due to limited insulation because of sparse hair coats,
thin hides and small amounts of body fat (Moser, 1985). Estimated
percentages of body fat range from 1 to 2% (Manners and McCrea, 1973;
Seerley and Poole, 1974; Lodge et al., 1978; Boyd et al., 1978b).
Because piglets are born with little body fat that can be mobilized
and have limited gluconeogenic capacity when fasted (Pegorier et al.,
1982), they are dependent upon glycogen stores in liver, heart and
muscle and ample colostrum and milk intake to avoid hypoglycaemia.
Energy reserves are rapidly depleted after birth due to homeothermic
mechanisms and energy expended in competing for nursing position
(Morrill, 1952; Seerley and Poole, 1974; Boyd et al., 1978b; Okai et
al., 1978; Seerley et al., 1978a,b). Boyd et al. (1978b) reported
that liver glycogen concentrations (mg/g) declined from 177.9 to 25.4
during the first 24 h after birth. Similarly, Okai et al. (1978)
indicated that, even for nursing pigs, concentrations of liver
glycogen decline by as much as 70% during the first day after birth.
Therefore, as glycogen is depleted, piglets must receive an external
source of energy or hypoglycemia develops and piglets become weak.

104
During the first postnatal days, competition for nursing position
(Hartsock et al., 1977) leads to considerable energy dissipation
and(or) inadequate milk intake by smaller piglets. By 3 or 4 d
postpartum, each piglet has selected a nipple that it nurses
exclusively (McBride, 1963; Hartsock et al., 1977). Piglets having
low blood glucose (from depleted glycogen reserves or inability to
obtain access to milk), injuries, disease or genetic defects are
predisposed to being overlain by sows (Moser, 1985). Spicer et al.
(1986) reviewed factors such as these which predispose piglets to
preweaning mortality. Frequent nursing after birth normally prevents
hypoglycaemia. However, piglets born with low birth weights or
litters in which piglet number exceeds sow nursing capacity have high
postnatal death losses.
That piglets with low birth weights also have low survival rates
is well documented (Vestal, 1938; England and Day, 1970; Fahmy and
Bernard, 1971). When piglets are exposed to chilling, low birth
weight adversely affects their ability to return to normal body
temperature after cessation of chilling (Newland et al., 1952). In
addition, low birth weight piglets have greater elevations of blood
sugar levels in response to chilling, due to greater necessity for
utilization of stored glycogen for heat production. Newland et al.
(1952) indicated that smaller piglets have larger body surface area
per unit of body mass resulting in greater heat loss for small
compated to larger pigs at low ambient temperatures. Hall et al.
(1984) demonstrated that as pig birth weight increased, survival rate
increased through 21 d of lactation. Piglets weighing less than 1 kg

105
(.45, .68 or .91 kg) had less than a 60 % (16, 39, or 59%,
respectively) survival rate.
Heritability of birth weight is near zero (England, 1986), thus
selection for increased birth weight is not practical. However,
nutrition of dams during gestation can increase birth weights of pigs
(Clawson et al., 1963; Lodge et al., 1966; Vermedahl et al., 1969;
Baker et al., 1969). Pettigrew (1981) indicated that supplemental
fat in sow diets during late gestation does not alter piglets' body
stores of carbohydrates at birth, but body fat stores are increased
slightly. In addition, supplemental dietary fat during late
gestation and(or) lactation increased milk production and fat content
of colostrum and milk. Therefore, survival rates for piglets in
herds with average survival rates of less than 80% were impaired.
Solutions to the problem of low birth weights of piglets include
nutritional considerations and protocols to favorably alter
metabolism of sows and piglets (Stahly et al., 1980; Steele et al.,
1980; Spence et al., 1985).
In addition to increasing piglet energy reserves and milk
production by sows, alternate energy sources may be required in some
situations. Conditions may require cross - fostering of piglets when:
(1) litter size is too great for the number of functional mammary
glands; (2) partial or total agalactia; (3) aggressive or
cannabalistic behavior of sows; (4) death of the dam and (5) nipples
too large or sows too large to allow nursing by small pigs (English,
1985) . As reviewed by England (1986) , sows are generally receptive
to piglets other than their own and cross - fostering can be used to
adjust for inequities in number of piglets and number of functional

106
teats. In situations in which sows die before newborn piglets have
nursed, fresh or frozen colostrum should be available.
In addition, to relying on cross - fostering of piglets, there is
also the possibility of artificially rearing piglets (Lecce, 1975).
Artificial rearing systems can accomodate extra piglets in litters
and allow for earlier rebreeding of sows. Diarrhea is frequently
encountered in early weaned piglets since antibodies in colostrum or
milk normally prevent Escherichia coli. transmissible gastroenteritis
or rotavirus from producing diarrhea by adversely affecting
enterocytes (Lecce, 1986). Specific antibodies bathing the gut also
afford passive protection when added to the diet or as part of normal
mammary secretions. Jones (1986) summarized research involving
artificial feeding of piglets through automatic feeders after they
were removed from sows at 2 to 21 d of age. Under certain conditions
this system increased sow productivity by two pigs per sow per year.
The dietary formula consisted of 18% protein, 15% fat, 56.1%
carbohydrate and 1.5% minerals and vitamins.
England and Keeler (1965) found no differences in growth rate or
feed efficiency between pigs of various birth weights when tested
from equal beginning weights instead of equal ages. Furthermore,
England (1963) concluded that prenatal and postnatal growth rates did
not affect carcass traits. George and England (1973) indicated that
gilts of different birth weights did not have different reproductive
or litter trait performances. Therefore, it is beneficial to provide
an opportunity for low birth weight piglets to survive (England,
1986). Dietary and metabolic alterations during gestation and
lactation are important to allow maximum piglet growth and milk

107
production. However, as reviewed, alternative measures are being
tested which will improve both availability of nutrients for piglets
and postnatal survival.
Factors Associated with Anestrous
During and After Lactation in Sows
Follicular development during lactation and after weaning can be
influenced by parity, season, nutrition, suckling intensity of
litters, exposure to mature boars and exogenous hormone treatment
(for review, see Britt et al. , 1985; Britt, 1986). During lactation
sows are typically anestrus for the first 4 to 6 weeks (wk). Weaning
increases size of antral follicles and leads to estrus and ovulation
within 3 to 10 d. Prior to weaning, most follicles are less than 5
mm in diameter. After weaning, follicles grow rapidly to greater
than 8 mm in diameter (Warnick et al., 1950; Lauderdale et al., 1965;
Crighton and Lamming, 1969). Palmer et al. (1965a) reported that
average diameter of follicles is greatest 1 d after parturition and
then during the fifth to ninth wk of lactation. Rate of follicular
atresia was higher during the first week than wk 2 through 9 of
lactation (Palmer et al., 1965b). Kunavongkrit et al. (1982)
compared atretic versus healthy follicles and found that the percent
of atretic follicles declined from d 4 to 56 of lactation and
verified that small diameter follicles predominate during lactation.
If piglets are weaned after parturition (d 0), often abnormal or
cystic follicles develop (Peters et al., 1969b; Kunavongkrit et al.,
1983a,b) and the farrowing-to-mating interval is extended more than
if piglets are weaned after a lactation of typical length, i.e., 30 d
(Elliot et al., 1980). Numerous experiments have indicated that
weaning after lactation (length of lactation varied from 35 to 62 d)

108
results in increased average diameter of follicles, increased numbers
of follicles greater than 5 mm in diameter and decreased numbers of
follicles less than 5 mm in diameter (Palmer et al., 1965a; Cox and
Britt, 1982a, Dyck, 1983). Britt et al. (1985) concluded that
although the number of antral follicles doesn't change during
lactation, size of follicles gradually increases with the greatest
increase occuring after the fifth wk of lactation. The percentage of
atretic follicles declines during lactation and is related inversely
to the percentage of larger-sized follicles. Weaning at birth
results in development of cystic follicles in 30 to 50% of sows,
possibly due to failure of the positive - feedback mechanism to induce
LH release. Weaning after lactation is followed by a rapid increase
in the numbers of medium- and large-sized (> 10 mm) follicles and
decreased numbers of small follicles.
Britt et al. (1985) indicated that FSH stimulates follicular
development up to 5 to 6 mm and then LH is necessary for the final
stages of follicular maturation and ovulation. Secretion of LH
occurs in discrete episodic pulses every 2 to 5 h (Shaw and Foxcroft,
1985) during lactation (Edwards and Foxcroft, 1983). Inhibin may
control FSH secretion (Stevenson et al., 1981) and LH is suppressed
in some way by the suckling stimulus during lactation, perhaps by
lowering gonadotropin-releasing hormone (GnRH) secretion or
production (Cox and Britt, 1982a). That inhibin or some factor other
than estradiol controls FSH secretion was supported by work of Cox
and Britt (1983) in which they cauterized follicles greater than 3 mm
in diameter before weaning and reported that FSH, but not LH
secretion increased. In addition, Martin et al. (1984) indicated

109
that charcoal- treated porcine follicular fluid contains a factor
other than steroids that does not affect changes in plasma LH
concentrations after ovariectomy, but inhibits the post-ovariectomy
increase in a FSH concentrations in ovariectomized gilts. When
treatment with charcoal-treated porcine follicular fluid was stopped,
plasma concentrations of FSH increased. Concentrations of LH and FSH
in serum gradually increase after the third wk of lactation. Britt
et al. (1985) indicated that this may be related to a natural
reduction in suckling frequency of the litter. In sows nursing small
(2 to 4 pigs) litters, LH is higher during lactation than in sows
nursing average size (7 to 12 pigs) litters. However, Bevers et al.
(1981) reported that the LH response to exogenous GnRH (25 ug)
increased from 1 through 3 wk of lactation and was not affected by
litter separation.
Sensitivity to positive feedback to estradiol may change during
lactation and influence LH release. Exogenous estradiol (60 ug/kg)
did not influence a LH surge on d 5 of lactation, although an
increase in LH was detected 48 to 72 h after treatment on d 35 in 4
of 9 sows (Elsaesser and Parvizi, 1980). Administration of estradiol
benzoate (800 ug) at 2 or 3 wk of lactation did not elicit an LH
surge although an LH surge was induced in 1 sow at 3 wk of lactation
and resulted in estrus in 8 of 9 sows challenged during the third or
fourth wk of lactation (Ramirez et al., 1985a).
Concentrations of LH in serum increase within 8 to 12 h after
weaning (Cox and Britt, 1982a; Edwards and Foxcroft, 1983; Shaw and
Foxcroft, 1985) and frequency of LH pulses increases over the next 2
to 3 d (Cox and Britt, 1982c; Shaw and Foxcroft, 1985). Although

110
there is no clear episodic pattern of FSH secretion, rate of FSH
secretion increases after weaning (Cox and Britt, 1982a; Edwards and
Foxcroft, 1983; Shaw and Foxcroft, 1985), but to a lesser extent than
for LH. Lactation periods of shorter duration (3 vs 5 wk) are
associated with less FSH 2 to 3 d after weaning (Edwards and
Foxcroft, 1983) and early weaning (10 or 21 d vs 35 d) results in
lower preovulatory LH surges (Edwards and Foxcroft, 1983; Kirkwood et
al., 1984a; Kirkwood et al., 1984b).
Concentrations of GnRH in medial basal hypothalamus and stalk
median eminance increase by 60 h after weaning at 5 wk of lactation
and are associated with increased LH secretion (Cox and Britt,
1982a). By 96 h after weaning, GnRH increases in the hypophysial
portal area as well and this coincides with increased concentrations
of LH and FSH in serum.
Although prolactin (PRL) concentrations are sevenfold higher when
piglets are present than when piglets are removed from sows (Bevers
et al., 1981), it does not appear that PRL plays a role in
suckling-induced suppression of LH secretion. Armstrong et al.
(1986a,b) confirmed that litter separation decreased PRL and
increased LH secretion. When sows were treated with bromocryptine to
suppress serum PRL concentrations, there was no effect on LH response
to exogenous GnRH (Bevers et al., 1981). Armstrong et al. (1986a)
indicated that suckling may suppress pulsatile release of LH and
increase PRL during lactation by increasing endogenous opioid
"tone". In one trial, they examined effects of infusing naloxone or
saline or separating litters. Naloxone infusion increased the
frequency of LH release and decreased PRL. In a second trial,

Ill
Armstrong et al. (1986a), infused morphine with or without litter
separation. Litter removal alone increased concentrations and
frequency of release of LH. Morphine infusion suppressed pulsatile
LH in only 2 of 4 sows. Morphine infusion, alone or combined with
litter separation, depressed both the frequency of episodes of LH and
mean level of LH. In sows induced to exhibit behavioral estrus with
estradiol benzoate during lactation, naloxone administration did not
affect LH concentrations when given over the time of an expected
endogenous LH surge in nonlactating pigs (Schneller et al., 1987).
There was not a clear involvement of endogenous opiod peptides in
ovulatory failures associated with inducing estrus during lactation.
Secretion of cortisol and ACTH may affect follicular development
during and after lactation in sows (Kunavongkrit, 1984; Liptrap,
1970, 1973; Barb et al., 1982), but their influence is not well
defined. As reviewed by Britt et al. (1985), other hormones may also
affect development of follicles pre- and post-weaning, i.e., oxytocin
may decrease follicular development during lactation through adverse
effects on FSH secretion (Peters et al., 1969a).
To decrease the interval from farrowing to estrus and mating,
exogenous hormones have been administered to induce estrus and
ovulation during lactation, and success of treatments has depended
upon the duration of lactation. Response of lactating sows to such
treatments improved as the length of lactation increased. Britt et
al. (1985) summarized effects of numerous studies in which follicular
development was induced in lactating sows with varying doses (450 to
3400 i.u.) of equine chorionic gonadotrophin (eCG). In general,
estrus and conception cannot be induced during the first 5 days of

112
lactation (Cole and Hughes, 1946; Hausler et al., 1980), but after
the third wk of lactation, induction of estrus and percentage of sows
farrowing after eCG treatment increased (Cole and Hughes, 1946;
Heitman and Cole, 1956; Guthrie et al., 1978; Hausler et al., 1980;
Hodson et al., 1981). Treatment with eCG during the first 2 wk after
farrowing resulted in conception in approximately 50% of treated
sows, but this percentage increased substantially ween sows were
treated during later stages of lactation (Britt, 1986). Hodson et
al. (1981) suggested that eCG treatments not be given before the 3rd
wk after farrowing and concluded that 1500 IU eCG and either 500 or
1000 IU hCG were satisfactory when given 72 to 96 h after eCG.
Johnston (1985) reported that 20 of 24 sows treated with 2000 IU eCG
on d 10 of lactation and 1000 IU hCG 4 d later conceived following
artificial insemination at 24 and 39 h after hCG without regard to
estrus. Pigs were weaned 8 d later and farrowing interval was
reduced to 129 d compared to 144 d for sows bred after weaning at d
23 of lactation without treatment. Induction of fertility in
post-partum sows by injection of a crude FSH preparation showed
limited success (Peters et al., 1968; 1969b). Esbenshade and
Armstrong (1987) administered porcine pituitary extracts hourly for 6
d during the third week of lactation and induced estrus in all four
treated sows 114 + 8 h after initiation of treatment. Hourly
administration of purified LH over a 150 h period induced estrus
during lactation when given at a dose of 1.54 ug/kg BW per h, but had
limited or no effect at doses of .58 or 2.89 ug/kg BW per h.
Pulsatile intravenous administration of GnRH induced fertile estrus
in multiparous lactating sows when given beginning on d 25 (2.5 ug/2

113
h) or on d 31 (1.5 ug/h) of lactation if treatment was continued for
24 h after onset of estrus (Cox and Britt, 1982b). Ramirez et al.
(1985b) infused GnRH (1.5 ug/h) beginning on d 24 of lactation and
detected no differences in ovulation rate or subsequent litter size
between sows which received GnRH after estrus for either 0 or 24 h.
Protocols are also being developed to induce estrus in anestrous
sows following weaning to reduce the interval from farrowing to
estrus and mating. Primiparous sows and sows weaned during the
summer or early autumn have a greater likelihood of being anestrus
after weaning (Love, 1978; Stork, 1979; Hurtgen et al., 1980; Cox et
al., 1983a; Britt et al., 1983). As reviewed by Britt et al. (1985),
various treatments can stimulate estrus and ovulation in weaned
anestrous sows, but normal fertility has only been reported for sows
treated with eCG alone or eCG in combination with hCG (Schilling and
Cerne, 1972; Dyck et al., 1979; King et al., 1982b; Dial et al.,
1984) or pulses of GnRH (Armstrong and Britt, 1985). Other
treatments, e.g., estradiol benzoate administration, will not promote
additional follicular development after the LH surge, so exogenous
estradiol apparently causes ovulation of only mature follicles
present at treatment (Cox et al., 1983b; Dial et al., 1984). Ovaries
of anestrous sows have few medium and large follicles (Cox et al.,
1983b). Administration of eCG 1 d postweaning reduced postweaning
anestrus in primiparous sows from which piglets were weaned after a
lactation of 3 to 4 wk (Hurtgen and Leman, 1979; Britt et al.,
1984). It appears that eCG stimulates sufficient follicular
development so that endogenous secretion of estrogen leads to
positive feedback and an LH surge. Furthermore, eCG alone or in

114
combination with hCG, is more practical to use than GnRH because
fewer injections are required (Britt et al., 1985).
The effect of suckling intensity on lactational anestrous is
mediated through mechanisms associated with release of GnRH from the
hypothalamus (Cox and Britt, 1982a). Number of piglets nursed is
negatively related to the interval from weaning to estrus (Fahmy et
al., 1979). Since older piglets suckle less frequently, the interval
from weaning to estrus declines following longer lactations (Self and
Grummer, 1958; Moody and Speer, 1971; Cole et al., 1975). Partial
weaning, i.e., separating piglets from sows for 6 to 12 h daily
beginning on the second or third wk of lactation, results in a high
percentage of sows in estrus during lactation (Smith, 1961; Walker
and England, 1978; Thompson et al., 1981; Stevenson and Davis,
1984). However, this protocol was not effective in other studies
(Kirkwood et al., 1983; Henderson and Hughes, 1984). Britt and Levis
(1982) reported that partial weaning for 2 d prior to weaning
improved percentage of sows exhibiting estrus if that interval was
protracted for control sows. Split-weaning and weaning larger
piglets 2 to 5 d prior to weaning small piglets increased the
percentage of sows exhibiting estrus within 5 to 10 d after weaning
(Stevenson and Britt, 1981; Cox et al., 1983a; Stevenson and Davis,
1984). In general, the interval from weaning to estrus is extended
in primiparous sows, sows with larger litter and sows having short
periods of lactation (Kunavongkrit, 1984).
Exposure of lactating sows to either a synthetic boar pheromone
(5 alpha-androst-16-en-3-one) or to mature boars can reduce the
weaning to estrus interval (Hillyer, 1976; Petchey and English, 1980;

115
Rowlinson et al., 1975; Petchey and Jolly, 1979; Rowlinson and
Bryant, 1981, 1982; Bryant et al., 1983; Bryant and Rowlinson, 1984);
however, this was not confirmed in other studies (Guthrie et al.,
1978; Petchey et al., 1978). Booman et al. (1983) reported increased
LH release in sows following exposure to boars. Others have
indicated that grouping of sows and litters without the presence of a
boar induced lactational estrus (Petherick et al., 1977). Newton et
al. (1986) suggested that litter separation combined with boar
exposure during the last 8 d of laction increased basal and pulsatile
LH secretion in both multi- and primiparous sows. However, lack of
follicular development and estradiol secretion may have predisposed
primiparous sows to anestrus during lactation despite increased LH
secretion. In addition, Newton et al. (1986) suggested that higher
concentrations of cortisol and progesterone in plasma following
litter separation and boar exposure may have adversely affected onset
of estrus in primiparous sows during lactation, but higher cortisol
and progesterone secretion in multiparous sows following treatment
did not block estrous behavior. Newton et al. (1987) further
addressed the influence of altered suckling intensity with and
without boar exposure, duration of altered suckling intensity and
season and parity on interval to estrus in a study involving 140
sows. As long as sows were exposed to boars for at least 1 h each
day, the incidence of estrus during lactation was about equal to that
for litter separation of 3 h (65%) vs 6 h (79%). However, litter
separation of 6 h slightly (P = .08) decreased the interval to estrus
in sows that returned to estrus during lactation. Newton et al.
(1987) also indicated that boar exposure alone did not initiate

116
estrus during lactation and concluded that litter separation was more
beneficial. As reported by others, parity had an effect on response
to treatment, with the percentage of lactating primiparous sows
exhibiting estrus being less than that for lactating multiparous
sows. An exception was noted in this trend when sows were mated with
Chester White boars suggesting that breed of boar may influence
lactational anestrus.
Seasonal influences on postweaning interval to estrus were not
detected in the study of Newton et al. (1987). However, Armstrong et
al. (1984) suggested that sows weaned in the fall, consumed less
energy, mobilized more body fat and, as a result of a decreased
activity and(or) feedback sensitivity of the hypothalamic-hypophyseal
axis, had prolonged intervals from weaning to estrus. Greater
average concentrations of LH in serum were detected in sows weaned in
the spring, while the number of LH surges was greater at 71 vs 0 h
after weaning during the fall.
In summary, follicular development and estrous behavior expressed
after and during lactation can be influenced by parity, season,
suckling intensity (litter size and duration of lactation), boar
exposure, exogenous hormonal treatments and nutrition. Effects of
nutrition and body condition on reproductive performance after
weaning have been discussed in a previous section.
Metabolism of Glutathione
Glutathione (GSH) is a tripeptide composed of L-glutamic acid,
L-cysteine, and glycine with a molecular formula of
^10^17^6^3^ anc* contains a reactive thiol group (Meister and
Anderson, 1983). According to Brittain and Tottle (1986), discovery

117
of GSH is credited to de Rey-Pailhode in 1888, and GSH was first
crystallized in 1921 (Hopkins, 1921). In mammalian cells, the
concentration of GSH is often very high (1 to 10 mM range) and most
of the intracellular GSH exists in the thiol (GSH) form (Meister,
1975). Glutathione in the reduced form is referred to as GSH, while
glutathione in the oxidized or glutathione disulfide form is
abbreviated as GSSG (e.g., Meister, 1983). Glutathione metabolism
and function of GSH have been extensively reviewed (Arias and Jakoby,
1976; Meister and Tate, 1976; Sies and Wendel, 1978; Meister, 1983;
Meister and Anderson, 1983; Meister, 1985a; Meister, 1985d).
The overall metabolism of GSH involves several key reactions: (1)
those of the "gamma-glutamyl cycle", which accounts for synthesis and
degradation of GSH and involves transport of GSH out of cells and
gamma-glutamyl amino acids into cells; (2) those involved in
reversible conversion of GSH to GSSG and (3) those involved in
formation and metabolic transformations of S-substituted GSH
conjugates (Meister and Anderson, 1983). Glutathione is synthesized
intracellularly by consecutive actions of gamma-glutamylcysteine
synthetase and GSH synthetase (Meister and Anderson, 1983; Seelig and
2+
Meister, 1985). These enzymes, in the presence of Mg , catalyze
the following respective, reversible reactions:
(1) L-glutamate + L-cysteine + ATP <-->
L-gamma-glutamyl-L-cysteine + ADP + Pi
(2) L-gamma-glutamyl-L-cysteine + glycine + ATP <-->
glutathione + ADP + Pi
Gamma-glutamylcysteine synthetase is competitively,
nonallosterically inhibited by glutathione and, therefore, reaction 1

118
can be inhibited by a physiologically significant feedback mechanism
(Richman and Meister, 1975). This feedback inhibition involves
binding of GSH to the glutamate site of the enzyme as well as to
another enzyme site; this second site may require a sulfyhdryl group
since gamma-glutamyl-alpha-aminobutyryl-glycine is a weak inhibitor
(Seelig and Meister, 1985). The synthetase enzyme first reacts with
MgATP followed by reaction with glutamate, and it appears that an
enzyme-ADP-gamma-glutamyl phosphate complex is formed (Yip and
Rudolph, 1976). Rate of GSH synthesis is determined by levels of
sulfur-containing amino acids available and, in part, by the supply
of ATP (Tateishi et al., 1974).
In the reaction catalyzed by GSH synthetase, an intermediate
enzyme-bound acyl phosphate complex is formed through a mechanism
similar to those catalyzed by glutamylcysteine and glutamine
synthetases (Meister, 1985b). Substrate specificity of glutathione
synthetase in rat kidney has been examined (Oppenheimer et al.,
1979) , and results indicate a high degree of specificity toward
gamma-glutamyl amino acids in which the amino acid moiety is
sterically similar to cysteine, e.g., alpha-aminobutyrate, serine,
and alanine.
Degradation of GSH is initiated by gamma-glutamyl transpeptidase,
a membrane bound enzyme localized on the external surface of cells
(Tate and Meister, 1981) which is associated with its transport, in
the form of GSH, out of cells. Gamma-glutamyl transpeptidase
transfers the gamma-glutamyl moiety of GSH (and GSSG) to: (1) amino
acid acceptors, e.g., L-cystine, L-glutamine, and L-methionine and
certain dipeptides, to form gamma-glutamyl amino acids and cysteinyl

119
glycine by transpeptidation; (2) to GSH to form gamma-glutamyl-GSH by
autotranspeptidation and (3) to water by hydrolysis (Meister and
Anderson, 1983). Transport of GSH into cells allows release of the
cysteine moiety intracellularly (Tate and Meister, 1981).
Gamma-glutamyl transpeptidase plays a role not only in the transport
of amino acids, but in metabolism of prostaglandins (Cagen and
Pisano, 1979), estrogens, (Kuss, 1969) and leukotrienes (Hammarstrom
et al., 1980; Anderson et al., 1982b) and in processing of
mercapturic acids (Boyland and Cresseaud, 1969) . High
gamma-glutamyl transpeptidase activity is found in numerous cells
which exhibit secretory or absorptive functions (Meister and
Anderson, 1983). In most mammals, the kidney exhibits the highest
activity (Tate and Meister, 1985) and specificity studies indicate
that three separate subsites are in the active center of the
transpeptidase: (1) the gamma-glutamyl donor site which exhibits
broad optical and steric specificity; (2) the cysteinyl acceptor
subsite which prefers neutral amino acids and (3) the glycine
acceptor subsite which prefers glycine. Kinetic mechanism studies
(see Allison, 1985) indicate that the first substrate to bind
transpeptidase is the gamma-glutamyl donor. A gamma-glutamyl enzyme
intermediate is formed and the first product, cysteinylglycine, is
released if the donor was GSH. The acceptor substrate then binds to
the gamma-glutamyl enzyme, transferring the gamma-glutamyl moiety to
the alpha-amino group of the amino acid or peptide to another
molecule of donor substrate by autotranspeptidation or to water by
hydrolysis. Griffith and Tate (1980) indicated that GSH oxidase
activity associated with gamma-glutamyl transpeptidase is due to

120
oxidation of cysteinylglycine with GSH to form the mixed disulfide or
with another product to form cystinylbisglycine. Either product can
then undergo transhydrogenation with free GSH to form either GSSG or
a mixed disulfide (cysteinylglycine + GSH).
Gamma-glutamyl cyclotransferase catalyzes the conversion of
gamma-glutamyl amino acids to 5-oxoproline and corresponding free
amino acids (Meister and Anderson, 1983). The enzyme is widely
distributed in mammalian tissues and is highly active toward the
L-gamma-glutamyl derivatives of glutamine, methionine, alanine,
cysteine, cystine and several other amino acids (Meister and
Anderson, 1983) . It is much more active towards certain
di-gamma-glutamyl amino acids (Meister, 1985c). Beta-aminoglutaryl-
L-alpha-amino-butyrate is a selective inhibitor of gamma-
glutamylcyclotransferase (Meister, 1985c). Meister and Anderson
(1983) indicated that multiple forms of the enzyme exist which may be
involved in enzyme regulation.
5-Oxoprolinase catalyzes ATP-dependent cleavage of 5-oxoproline
to glutamate; cleavage of ATP is required to cleave the peptide bond
because of the unusual stability of the 5-oxoproline amide bond
(Meister and Anderson, 1983; Meister et al., 1985). 5-oxoproline is
formed by: (1) action of gamma-glutamylcyclotransferase on
gamma-glutamyl amino acids; (2) enzymatic cleavage of amino terminal
5-oxoprolyl residues of peptides and proteins; or (3) the action of
gamma-glutamylaminocyclotransferase on epsilon-(L-alpha-glutamyl)-
L-lysine derived from degradation of proteins containing
transglutaminase-generated cross-links (see Meister et al., 1985).
Diet and nonenzymatic cyclization of gamma-glutamyl compounds such as

121
glutamine are additional sources of 5-oxoproline (Meister and
Anderson, 1983). 5-oxoprolinase is found in most mammalian tissues,
but apparently not in erythrocytes or the lens of the eye (Meister
and Anderson, 1983). The reaction catalyzed by 5-oxoprolinase may be
facilitated by binding of ATP and 5-oxoproline which induces a
conformational change that brings the substrates into juxtaposition
(Meister et al., 1985). Conversion of 5-oxoproline to L-glutamate is
essentially reversible, but slow reversal has been demonstrated
(Griffith and Meister, 1981). Meister et al. (1985) suggested the
mechanism for the reaction involves phosphorylation of 5-oxoproline
by ATP, perhaps on the amide carbonyl oxygen atom, followed by
hydrolysis of the resulting intermediate to yield gamma-glutamyl
phosphate, which would then be hydrolyzed to glutamate and inorganic
phosphate.
Cysteinylglycine and its S-derivatives produced from GSH
catabolism are hydrolyzed to their component amino acids possibly by
aminopeptidase M, an enzyme in the kidney and jejunal microvillus
membranes which has broad substrate specificity, or by a membrane
bound dipeptidase which has also been located in microvillus
membranes of rat kidney, jejunum and epididymis (Tate, 1985).
Although dipeptidase may play a greater role in hydrolysis of
cysteinylglycine and its derivatives, neither enzyme effectively
hydrolyzes L-cysteinylglycine (Anderson and Meister, 1983). There is
evidence that intracellular hydrolysis or extracellular oxidation of
L-cysteinylglycine may occur (Meister and Anderson, 1983) , but
neither aminopeptidase M or dipeptidase utilize GSH as a substrate
(Tate, 1985).

122
In addition to reactions of the gamma-glutamyl cycle, GSH
metabolism includes reactions involved in conversions of GSH to GSSG
(GSH disulfide) or vice versa. GSH reductase, a flavoprotein
isolated from numerous organisms, catalyzes the NADPH-dependent
reduction of GSSG to GSH (Carlberg and Mannervik, 1985) . This
reaction is irreversible, takes place exclusively within cells and is
essential for maintenance of GSH levels which accounts for high
GSH:GSSG ratios in cells (Carlberg and Mannervik, 1985). As
mentioned previously, activity of transpeptidase is also indirectly
involved in GSH oxidation (Griffith and Tate, 1980).
Glutathione peroxidase activity has been demonstrated in all
mammalian tissues examined (Flohe et al., 1979) and catalyzes
GSH-dependent reduction of hydroperoxides:
ROOH +2GSH --> ROH + H20 + GSSG
In this reaction, R may be either an aliphatic or aromatic
organic group, or hydrogen (Mannervik, 1985). Products of the
reaction are water, an alcohol (ROH), a second H2O when hydrogen
peroxide serves as a substrate and GSSG (Mannervik, 1985). In
erythrocytes, reduction of H2O2 is coupled with oxidation of
glucose - 6-phosphate and of 6-phosphogluconate, which provides NADPH
for reduction of GSSG by GSSG reductase. In red blood cells, GSH
peroxidase protects against the formation of methemoglobin by
consuming H2O2 (see Lehninger, 1982). It also is involved in
H2O2 metabolism in many other cells and catalyzes reduction of
other peroxides (see Meister and Anderson, 1983), which protect
membrane lipids against oxidation. Glutathione peroxidase also plays
a role in biosynthesis of prostaglandins and in regulation of

123
prostacyclin formation (Flohe, 1979). In most animals, the active
site of GSH peroxidase contains a residue of selenocysteine, in which
the sulfur atom of cysteine is replaced by a selenium atom
(Lehninger, 1982). However, in guinea pig liver, the selenoprotein
is absent and GSH peroxidase activity is not selenium dependent
(Lawrence and Burk, 1978). In hepatocytes, selenium-dependent GSH
peroxidase has been localized primarily in the cytosol and in the
matix of mitochondria (Flohe and Schlegel, 1971).
Many metabolic functions involve thiol-disulfide exchange, e.g.,
protein synthesis and degradation, activation and inactivation of
enzymes, synthesis of deoxyribose intermediates required for DNA
synthesis and reduction of cystine (Meister and Anderson, 1983) .
Thiol transferase catalyzes the reversible thiol-disulfide
interchange reactions in which R is a thiol and R'SSR' is a disulfide
(Larson et al., 1985): RSH + R'SSR' <--> RSSR' + R'SH. The enzyme
has a major role in maintaining intracellular thiols in a reduced
state by coupling to GSH and GSH reductase (Mannervik, 1980), and may
play a role in cellular regulation by modifying proteins by
thiol-disulfide interchange (Mannervik and Axelsson, 1980).
Reduction of ribonucleotides to deoxyribonucleotides for DNA
synthesis is catalyzed by ribonucleoside diphosphate reductase
(Holmgren, 1981). As reviewed by Holmgren (1985), two different
hydrogen donor systems for this enzyme have been identified: (1) the
NADPH-dependent thioredoxin system and (2) a GSH-dependent system
where glutaredoxin couples the oxidation of GSH to the reduction of
ribonucleotides. Then GSSG is reduced by GSH reductase and NADPH.
Other transhydrogenase functions associated with GSH include those of

124
GSH-insulin transhydrogenase, protein-disulphide-isomerase or
thiol:protein disulfide oxidoreductase, all which may be the same
enzyme (see Meister and Anderson, 1983; Morin and Dixon, 1985). The
GSH:insulin transhydrogenase may function in insulin degradation
(Meister and Anderson, 1983). Transhydrogenases (see Meister and
Anderson, 1983) have varied substrates and participate in a number of
reactions involved in assembly of proteins, regulation of enzymes and
reductive degradation of proteins.
Glutathione-S-transferases catalyze reactions between GSH and a
variety of electrophilic compounds of endogenous or exogenous origin
to form GSH conjugates (Meister, 1983). Because of the large number
of GSH-transferase isoenzymes found in each species, a consistent
system of nomenclature has been devised for the rat (Jakoby et al.,
1984) which may eventually be utilized for other species (Jakoby,
1985). Glutathione-S-transferases exist in substantial quantities in
liver and other tissues, e.g., erthrocytes, intestine, placenta and
lung (Meister and Anderson, 1983; Warholm et al., 1985). Because of
its thiol anion, compounds with an electrophilic center readily
conjugate with GSH either spontaneously or as catalyzed by
GSH-S-transferases (Meister, 1983; Meister and Anderson, 1983). As
reviewed by Meister and Anderson (1983), conjugates of GSH are
transported across cell membranes as substrates of gamma-glutamyl
transpeptidase, and the gamma-glutamyl moiety of the conjugate is
transferred to an acceptor. The resulting cysteinylglycine conjugate
is converted by dipeptidase to a cysteinyl conjugate which is then
N-acetylated to form an N-acetylcysteine conjugate (a mercapturic
acid). Cysteine-S-conjugate N-acetyl transferase catalyzes the

125
acetylation step in mercapturic biosynthesis (Duffel and Jakoby,
1985) , and the mercapturic acid form is then excreted in urine or
feces (Meister, 1983; Meister and Anderson, 1983). As reviewed by
Meister and Anderson (1983), GSH-S-transferases may function in
metabolism of ethanol, heavy metals and drugs, and thus detoxify for¬
eign compounds. However, they also function in conjugating endoge¬
nous compounds, i.e., leukotrienes (Meister and Anderson, 1983).
Activities of many enzymes are influenced by GSH and other thiols
and GSH participates as a coenzyme in several enzymatic reactions
(Meister and Anderson, 1983). The glyoxylase reactions result in a
hemimercaptal formed by nonenzymatic interaction of methylglyoxal and
GSH which is converted into S-lactyl GSH by glyoxlase I and then
hydrolyzed to D-lactate and GSH. This sequence of reactions requires
GSH as a coenzyme. Other reactions or enzymes requiring GSH include:
(1) cis-trans isomerization of maleylacetoactetate to
fumarylacetoacetate; (2) isomer malelylpyruvate to fumarylpyruvate;
(3) dehydrochlorination of 1,1,1-trichloro-2,2-bis(para-chlorophenyl)
ethane; (4) those catalyzed by prostaglandin endoperoxide D-isomerase
and E-isomerase and (5) formaldehyde dehydrogenase (Meister and
Anderson, 1983).
Meister (1985d) indicated that studies of GSH transport have
shown that the intact peptide is not taken up by cells. Also, the
apparent uptake of GSH by some cells is due to extracellular
breakdown of GSH, uptake of products formed and intracellular
resynthesis of GSH (Jensen and Meister, 1983; Meister and Anderson,
1983). However, Meister (1985d) did not exclude the possibility that
intact GSH is transported into some cells. Meister (1983; 1985d)

126
reviewed methods for selectively modifying GSH metabolism and
studying GSH transport. Of particular relevance is his discussion of
methods to increase cellular GSH levels. Meister (1985d) indicated
that administered GSH does not seem to enter most cells although
there is considerable evidence that many cells export GSH.
Derivatives of GSH, e.g., monoethyl and monomethyl esters of GSH,
appear to be effectively transported into cells and then hydrolyzed
intracellularly. Administration of monoethyl (or methyl) ester of
GSH to mice leads to a substantial increases in GSH levels within the
liver and kidney. Esters also increase intracellular GSH levels
after pretreatment with buthionine sulfoximine, an irreversible
inhibitor of gamma-glutamylcysteine synthetase, excluding the chance
that increased intracellular GSH was due to synthesis of GSH from
amino acids. Use of esters is attractive because feedback inhibition
on GSH synthesis is eliminated and intracellular energy for GSH
synthesis is not required. Furthermore, many cells have high levels
of esterase that hydrolyze GSH esters after their transport into
cells.
Directly or indirectly, GSH metabolism involves other reactions
not covered in this review. Because of the varied metabolic pathways
and ubiquitous nature of GSH, it can potentially participate in
numerous functions and biological systems, some of which will be
reviewed in the subsequent section.
Functions of Glutathione
Larsson et al. (1983) stated that glutathione (GSH) is the most
important nonprotein thiol present in animal cells as well as in most
plants and bacteria. Douglas (1987) stated "research in the vast

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field of GSH biochemistry and physiology has been spurred
consistently in the past by the search for 'the role of GSH'. The
crusade for this Holy Grail led to the recognition of a myriad of
functions for this relatively simple tripeptide. It is the variety
of modes in which this ubiquitous biochemical can assist in natural
processes that is most impressive and few current workers, if any,
would still advocate a single, central purpose for its widespread
presence in living cells." Some of the roles of GSH include
detoxifying drugs and endogenous metabolites, acting as an
intracellular reducing agent, storing and transporting cysteine,
transporting amino acids through the gamma-glutamyl cycle, serving as
a coenzyme and synthesizing deoxyribonucleotide precursors of DNA
(Meister, 1983). Glutathione is also involved in other important
cell functions including maintenance of membrane integrity and
cytoskeletal organization and modulation of protein conformation and
enzyme activity (Kosower and Kosower, 1978). Involvements of GSH in
immune response (Droge et al., 1986), aging (Al-Turk et al., 1987;
Furukawa et al., 1987; Perry et al., 1987), inhibition of tumor
growth (Novi, 1981), protection against teratogens (Harris et al.,
1987; Slott and Hales, 1987) and detoxification of xenobiotics (Sipes
et al., 1987; Reitjens et al., 1987; Moldeus and Quanguan, 1987) are
currently being investigated. Discussing GSH function(s) in detail
is impossible. Therefore, this review will describe some of the more
recent areas of research involving GSH.
Glutathione participates in detoxification of xenobiotic
compounds by virtue of its thiolate anion nucleophilicity and(or)
free radical stability in at least two detoxifying pathways (Arrick

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and Nathan, 1984; Jakoby, 1978). Thiolate anions are excellent
nucleophiles and can easily undergo substitution reactions either
directly or catalyzed by enzymes such as glutathione-S-transferases
(Russo et al., 1986). The role of glutathione in detoxification of
alkylating agents, both in terms of initial tumor response, and
drug-induced resistance to these aklylating agents was examined by
Russo et al. (1986). Modulation of intracellular glutathione levels
was shown to change the cytotoxicity of drugs via redox cycling of
gluathione disulfide to gluathione and vice versa. Russo et al.
(1986) suggested the possibility of beneficially manipulating
intracellular glutathione levels to enhance antineoplastic
chemotherapy.
Novi (1981) reported that reduced GSH produced regression of
aflatoxin B-^-induced liver tumors when administered in the later
stages of tumor progression. Following induction of tumor growth,
rats received GSH (100 mg per rat per day) by stomach intubation.
All rats treated only with aflatoxin died of liver tumors within 20
months after discontinuing carcinogen treatment, whereas 81% of the
aflatoxin-treated rats that received GSH were still alive and
apparently healthy 4 months later. Novi (1981) indicated that
macroscopic changes detected at autopsy indicated that GSH-treated
rats experienced remodeling of the liver. Thus, Novi (1981)
suggested that fully transformed malignant cells had been reversed by
administration of GSH. The author questioned whether GSH induced
regression of tumor growth by modifying properties of malignant
cells, i.e., by inducing differentiation, or by selectively killing
neoplastic cells and allowing normal cells to reconstitute the liver

129
parenchyma. Some evidence such as increased smooth endoplasmic
reticulum following GSH administration indicated that the mechanism
involved reversion of malignancy.
Slott and Hales (1987) evaluated the protective effects of GSH
against in vitro embryotoxicity of acrolein. Acrolein is a component
of cigarette smoke, automobile exhaust and by-products of and
reactants in many industrial processes (Johnstone and Plimmer, 1959;
Tanimoto and Uehara, 1975; Izard and Libermann, 1978) and is
embryolethal and teratogenic in vivo in several species after
intraamniotic injection (Claussen et al., 1980; Hales, 1982; Korhonen
et al., 1983; Slott and Hales, 1985) and in vitro in rat whole embryo
culture (Slott and Hales, 1986). Acrolein is reactive towards
thiols, forming conjugates with GSH in vivo and in vitro either
nonezymatically or enzymatically with GSH-S-transferases (Kaye, 1973;
Giles, 1979; Patel et al., 1980). In addition, acrolein depletes
hepatic GSH levels in intact rats and cultured hepatocytes (Gurtoo et
al., 1981; Zitting and Heinonen, 1980). Slott and Hales (1987)
suggest that thiols such as GSH protect against toxic effects of
acrolein either directly by reacting with acrolein or indirectly by
enhancing tissue levels of sulfhydryls. Kitchin et al. (1984)
demonstrated that GSH supplementation to culture medium can prevent
embryolethality and growth retardation, but not teratogenesis induced
from mercuric chloride addition to cultured rat embryos. However,
Kitchin et al. (1984) also reported that lOOuM GSH causes
telencephalic abnormalities in all exposed embryos. Since it is
known that thiols can protect against the teratogenicity of certain
drugs, Slott and Hales (1987) tested the specific role of GSH on

130
protection against embryotoxicity. Embryonic deaths, malformations,
growth retardation and content of GSH and protein were evaluated
following concurrent or sequential additions of acrolein and GSH to
culture of d 10 rat embryos. Acrolein was lethal to 64 and 100% of
embryos at 120 and 160 uM, respectively, when added at the initiation
of the culture period. At 80 and 120 uM acrolein concentrations, 50
and 100%, respectively, of surviving embryos were malformed and
growth retardation was manifested by decreases in yolk sac diameter,
crown-rump and head lengths, number of somites and morphological
score. Concurrent exposure to 100 or 500 uM GSH protected embryos
against all of these effects. When rat embryos were cultured in the
presence of acrolein for 2 h prior to GSH addition, no protection was
afforded against lethal, teratogenic or growth retardation effects
induced by acrolein. However, a 6 h preincubation period with 500 uM
GSH prior to exposure to acrolein decreased the incidence of
embryonic deaths induced from acrolein (160 uM) exposure and tended
to decreased the number of deaths and malformations among embryos
exposed to a lower dose of acrolein (120 uM) to a level that was not
different from controls. However, sequential treatment with GSH and
acrolein did not inhibit growth retardation effects. None of the
treatments affected GSH concentration per mg protein. Slott and
Hales (1987) concluded that exogenous GSH protected against in vitro
embryotoxicity of acrolein. They proposed that the protective effect
was due to a direct interaction between GSH and acrolein when added
concurrently or to an indirect effect on embryos when GSH was added
prior to acrolein. Although the ability of the yolk sac and embryo
to take up exogenous GSH was not investigated, since GSH content or

131
concentration per mg protein did not change following GSH treatment,
it may be that cysteine formed from GSH degradation was responsible
for the observed effects. Cysteine is protective against toxic
effects of irradiation and chemicals (Connors, 1966; Thor et al.,
1979) and against teratogenesis (Ashby et al., 1976; Hales, 1981).
The authors alternatively suggest that the ratio of reduced to
oxidized GSH or reduction of protein sulfhydryls may be important in
protecting the embryo from acrolein toxicity. In contrast to Kitchin
et al. (1984), Slott and Hales (1987) did not detect telencephalon
abnormalities following GSH administration. Slott and Hales (1987)
suggested that administration of a GSH precursor or GSH monoester
(which is more easily taken up by cells) (Puri and Meister, 1983) may
be a useful treatment for protection against maternal drug exposure.
Harris et al. (1987) determined the extent to which modulation of
GSH levels can influence the incidence and(or) severity of
malformations caused by 2-Nitrosofluorene (NF), an agent known to
elicit dysmorphogenesis in vitro. Buthionine-sulfoximine (BSO), an
inhibitor of GSH synthesis, produced malformations (50%) in embryos
exposed to 14 uM NF, but produced no additional effects on embryos
exposed to higher NF concentrations. Treatment with BSO alone
resulted in greater than a 50% decrease in GSH content in visceral
yolk sacs and decreased (15%) GSH content of embryos. Embryonic
protein levels were increased 20% and yolk sac protein levels were
unchanged. Addition of BSO in combination with NF at the onset of
the culture period decreased embryonic GSH in a dose-dependent
manner, suggesting GSH turnover could be increased by addition of an
exogenous substrate capable of forming conjugates with and removing

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GSH from cells. Oxothiazolidine-carboxylate, which provides an
additional source of intracellular cysteine and increases GSH
synthesis, produced no significant changes in embryonic or yolk sac
GSH when added alone to the culture medium, but when added in
combination with NF, eliminated NF-elicited malformations.
Ketterer (1986) discussed the structure and function of a family
of GSH-dependent enzymes, GSH transferases, to which major functions
have been attributed: (1) detoxication of by-products of oxygen
utilization and (2) detoxication of electrophiles arising from
mixed-function oxygenation of xenobiotics. The first function
involves substrate limited to free fatty acid hydroperoxides and
hydroxyalkenals which have similar long-chain hydrocarbon moieties in
common. In contrast, electrophiles derived from xenobiotics have an
enormous potential range of structures. Ketterer (1986) suggested
that multiplicity of the GSH transferase isoenzymes is an adaptation
to the range of structures of xenobiotic origin which need to be
utilized as substrates. They further indicate that clues for
functions of GSH transferases which have not yet been defined may lie
in variations in distribution of isoenzymes between tissues of
different functions or cells of the same origin in different
differentiation states.
One important function of GSH-S-transferases is conjugation of
GSH with certain xenobiotic compounds, thus enhancing excretion of
xenobiotics. Activated metabolites produced from xenobiotic
compounds by the action of mixed function oxygenase may also be
conjugated with GSH. Sipes et al. (1987) indicated that in certain
cases, the GSH conjugate may result in reactive intermediates which

133
lead to tissue injury. Other GSH conjugates may undergo
intramolecular rearrangement to unstable intermediates that also
result in toxic reactions. Thus, although GSH conjugation is
important for "detoxifying" reactions, for certain xenobiotic
compounds formation of an unstable GSH conjugate may be the first
step toward production of a toxic metabolite (Sipes et al. , 1987).
Rietjens et al. (1987) reported that GSH-S-tranferase catalyzed
detoxification of potential intermediates in ozone - induced cell
damage. Ozone cell damage has been suggested to arise from oxidation
of the unsatruated fatty acid moieties in membrane phospholipids
(Pryor et al. , 1976; Mustafa and Tierney, 1978; Menzel, 1984).
Oxidation of these unsaturated fatty acids may be preceeded by
formation of fatty acid ozonides (Menzel, 1984). Although the exact
mechanism of this detoxification process has not been elucidated,
Rietjens et al. (1987) suggest that detoxification of the fatty acid
ozonide by GSH and GSH-transferases may proceed by a nucleophilic
attack of GSH on the ozonide ring structure, analogous to the
reaction between GSH and epoxides or hydroperoxides.
Moldeus and Quanguan (1987) reviewed the importance of the
glutathione cycle in detoxification of reactive intermediates formed
intracellularly either spontaneously or enzymatically. In these
reactions GSH may serve as a nucleophile forming conjugate or as a
reductant. Moldeus and Quanguan (1987) indicated that GSH can
conjugate, enzymatically though GSH-S-transferase or
nonezymatically, with different types of electrophiles such as arene
oxides, quiñones and electrophilic cations. Conjugation of
electrophilic metabolites formed intracellularly are most likely

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catalyzed enzymatically by glutathione transferases. At least seven
soluble GSH-S-transferase enzymes exist in rat liver. Although there
are examples of endogenous compounds that are metabolized by GSH
conjugation, e.g., leukotrienes, most electrophilic metabolites that
react with GSH are of exogenous origin and formed in reactions
catalyzed by the cytochrome P-450 linked monooxygenase system present
in the endoplasmic reticulum of mammalian cells (Moldeus and
Quanguan, 1987). Reduction of peroxides is catalyzed by GSH
peroxidase which exists in a least two forms: (1) one which is
dependent on selenium for activity and (2) one related to gluathione
transferases (Jakoby, 1978). The selenoprotein glutathione
peroxidase is active in the metabolism of both hydorgen peroxide and
organic hydroperoxides. Moldeus and Quanguan (1987) indicate the
following:
"Organic hydroperoxides are formed continuously as a
consequence of the aerobic environment. The major group of
hydroperoxides comprise those derived from polyunsaturated fatty
acids as a result of lipoxygenase and other enzyme activities.
Since they may cause toxicity if allowed to accumulate, their
reduction is an important detoxication reaction. Hydrogen
peroxide is also a normal cellular metabolite that is formed in
all subcellular compartments. Although hydrogen peroxide can be
metabolized by catalase located in the peroxisomes, GSH
peroxidase seems to be responsible for the reduction of hydrogen
peroxide formed in other cellular compartments. The metabolism
of organic hydroperoxides and hydrogen peroxide by GSH peroxidase
is associated with GSH oxidation. Most of the GSSG formed is
subsequently reduced by GSH reductase, and GSH is regenerated at
the expense of NADPH. An efflux of GSSG, however, which may lead
to depletion of cellular GSH under extreme conditions, is
sometimes observed as a consequence of stimulated GSH peroxidase
activity."
Sandy et al. (1986) utilized isolated hepatocytes as a model
system and diquat, a bipyridylium compound, as a substrate to
demonstrate the importance of the GSH peroxidase/GSH reductase system

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in protecting against the toxicity of hydrogen peroxide. If
hepatocytes are compromised, by pretreament with l,3,-bis(2-
choloroethyl)-1-nitrosourea, which inhibits the GSH reductase
activity, diquat redox cycling results in rapid depletion of cellular
GSH with a concomitant GSSG formation and cell death within one hour.
A fluorescent labelling reagent, mono-bromo-bimane which labels
thiols (Fahey et al., 1981; Kosower et al., 1983) utilized in
conjunction with HPLC (Newton et al. , 1981) were applied to identify
and quantitate cellular glutathione levels in mice during gestation
(Brittain and Tottle, 1986). Brittain and Tottle (1986) reported
that GSH is the major small molecular weight thiol present in
embryonic red blood cells, GSH:hemoglobin ratio is maintained at 0.6
from 13 d of gestation to adulthood in mice and decay of GSH in
samples can be avoided by addition of glucose containing buffers.
They concluded that although GSH is required for maintenance of
normal hemoglobin function, GSH concentration has no role in
modulating hemoglobin oxygen binding characteristics which vary in
embryonic mice (Purdie et al., 1983). Brittain and Tottle (1986)
also demonstrated that in order to obtain true values of GSH
concentrations within red blood cells, loss of labelled GSH must be
corrected for and the time taken to complete the analytical procedure
must be minimized and taken into consideration. Co-precipitation of
GSH with hemoglobin and decreases in concentrations of GSH after 1 h
were considerable.
Bannai and Tateishi (1986) described the role of membrane
transport in metabolism and function of GSH in mammals, specifically
transport of precursor amino acids of GSH. The reaction catalyzed by

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gamma-glutamylcysteine synthetase is thought to be rate limiting in
GSH synthesis. Rate of GSH synthesis and GSH level is significantly
influenced by the availability of intracellular cysteine (Tateishi et
al., 1974). Membrane transport is one of the major factors
regulating intracellular level of cysteine (Bannai and Tateishi,
1986). Cysteine is transported by a Na+-dependent system which
mediates both inward and outward flows of neutral amino acids with
small side chains, especially those having a -SH or -OH groups.
Extracellular cysteine raises intracellular levels of cysteine
(Bannai and Ishii, 1982), while extracellular alanine, serine and
glutamine lower the intracellular level of cysteine. Another
important factor that regulates intracellular level of cysteine is
transport of cystine. Cystine is transported by a Na+-independent
system which transports anionic amino acids and possibily is involved
in exchange of cystine and glutamate. Apparently intracellular
glutamate functions to draw in extracellular cystine and maintain an
adequate balance between cysteine and glutamate in cells. When cells
are exposed to electrophilic attack, influx of cystine is enhanced
resulting in stimulation of GSH synthesis and GSH may accumulate to
serve for detoxication of the electrophilic agent. Impaired
transport of amino acids across erythrocyte membranes may lead to
deficiencies of GSH. Bannai and Tateishi (1986) also discussed the
transport of GSH. Since enzymes that catabolize GSH are localized on
external surfaces of cells, efflux of GSH is the initial step in GSH
degradation. The liver is the major source of plasma GSH (Lauterburg
et al., 1984). The primary organ for clearance of circulating GSH is
the kidney (McIntyre and Curthoys, 1980; Orrenius et al., 1983).

137
Glutathione filtered by glomeruli is degraded to its constituent
amino acids by actions of gamma-glutamyltransferase and peptidases
localized on the luminal surface of the brush border membrane of
proximal tubules. The kidney also synthesizes and secretes GSH
actively. In the kidney GSH is secreted into tubular lumen and
degraded there, and the amino acids formed are reabsorbed and used
for GSH synthesis. A similar circulation is observed in the liver;
GSH secreted into the bile is partially degraded and the constituent
amino acids may be transported back into the liver (Inoue et al.,
1984). Functions of extracellular metabolism of GSH may include
supplying cysteine steadily to other tissues (Tateishi et al., 1977)
or acting as a reductant that protects membranes from oxidative
stress. The sulfhydryl group of GSH is more stable than that of
cysteine and GSH at high concentrations in cells is far less toxic
than cysteine making GSH a useful storage and transport form of
cysteine.
Tateishi et al. (1982) studied the availability of the cysteine
moiety released from dietary GSH for protein synthesis in rats to
determine the L-methionine-sparing effect of GSH. Rats were fed
diets containing 18% of an amino acid mixture having a composition
similar to that of whole egg, with or without GSH, with varying
proportions of labelled L-methionine, L-cysteine and GSH in the
diet. Incorporation of label into proteins and GSH in liver and into
proteins in the plasma was determined to assess utilization of sulfur
atoms from these compounds. Dietary GSH was found to be incorporated
efficiently into proteins and GSH in the liver. Tateishi et al.
(1982) concluded that dietary GSH exerted an L-methionine-sparing

138
effect as demonstrated by its incorporation of labelled sulfur into
proteins and GSH. In addition, GSH spared L-methione almost as
efficiently as L-cysteine in plasma protein synthesis, but was
slightly less efficient in liver protein synthesis. As dietary
concentrations of GSH increased, the methionine-sparing effect
increased.
Tateishi et al. (1982) further indicated that there are few
studies in which GSH was given to animals orally. Dyer and du
Vigneaud (1936) reported that oral or subcutaneous administration of
GSH stimulated growth of young rats fed a diet containing 6% casein
as efficiently as if given equivalent amounts of cystine. However,
control rats in their experiments, consumed less food than treated
rats. Harter and Baker (1977) demonstrated that chicks given GSH
orally grew as rapidly in 8 d as those given an equal amount of
sulfur in the form of cystine. Utilization of dietary GSH by chicks
was attributed to its breakdown into constituent amino acids by
intestinal enzymes, and then absorption of the liberated cysteine.
In rats, gamma-glutamyltransferase was detected in villus cells of
the jejunal mucosa (Curthoys and Shapiro, 1975; Garvey et al., 1976)
and may degrade extracellular GSH. Tateishi et al. (1982) imply that
since peptide transport in intestinal mucosa cells is in some cases
more efficient than that for constituent amino acids (Matthews, 1977)
transport of dietary GSH may occur in an intact form. They indicated
that whether GSH or GSSG were absorbed from the gut without
degradation to constituent amino acids remains to be examined.
Tateishi et al. (1982) stated that because methionine is an essential
amino acid for growth of mammals, its requirement would increase in

139
periods of active protein synthesis such as the perinatal period.
They refer to unpublished data (Tateishi et al.) in which
radiolabelled-GSH given in food or injected into pregnant mice during
the perinatal period was incorporated rapidly into the liver of
fetuses. In addition, they reported that the incorporation of GSH
into high molecular weight compounds was greater in fetuses than in
adult mice.
Al-Turk et al. (1987) indicated that changes in GSH levels
and(or) its metabolizing enzymes with age may be related to impaired
immunological responsiveness, increased susceptibility to drugs and
free radicals and enhanced susceptibility to some disease. Since GSH
plays a role in cells as an antioxidant and since free radicals may
be responsible for cellular aging (Al-Turk and Stohs, 1981; Vanella
et al., 1982), several studies have been conducted to correlate GSH
and its metabolizing enzymes with the aging process (Stohs et al.,
1980; 1982; Al-Turk et al., 1987). Harman (1980) proposed that the
aging process involves an increased susceptibility to free radicals.
Levels of GSH and activities of GSH-S-transferases and GSH reductase
were determined in human erythrocytes and lymphocy