Group Title: Malaria Journal 2009, 8 (Suppl 2): I1
Title: Introduction: development of the sterile insect technique for African malaria vectors
CITATION PDF VIEWER THUMBNAILS PAGE IMAGE ZOOMABLE
Full Citation
STANDARD VIEW MARC VIEW
Permanent Link: http://ufdc.ufl.edu/UF00100231/00001
 Material Information
Title: Introduction: development of the sterile insect technique for African malaria vectors
Series Title: Malaria Journal 2009, 8 (Suppl 2): I1
Physical Description: Archival
Creator: Klassen W
Publication Date: 11/16/2009
 Record Information
Bibliographic ID: UF00100231
Volume ID: VID00001
Source Institution: University of Florida
Holding Location: University of Florida
Rights Management: Open Access: http://www.biomedcentral.com/info/about/openaccess/

Downloads

This item has the following downloads:

01475-2875-8-S2-I1 ( PDF )


Full Text



Malaria Journal


0
BioMled Central


Introduction

Introduction: development of the sterile insect technique for
African malaria vectors
Waldemar Klassen


Address: Tropical Research and Education Center, University of Florida, Homestead, Florida 33031, USA
Email: Waldemar Klassen klassen@ufl.edu



Published: 16 November 2009
Malaria journal 2009, 8(Suppl 2):11 doi:10.1 186/1475-2875-8-S2-11
This article is available from: http://www.malariajournal.com/content/8/S2/ I
2009 Klassen; licensee BioMed Central Ltd.
This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0),
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.


This supplement to Malaria Journal meets a great need for
a convenient assemblage of existing information on the
suppression and/or eradication of Anopheles populations
using the release of sterilized mosquitoes. Publication of
such a collection of articles is overdue for three compel-
ling reasons. Firstly, because malaria control in sub-Saha-
ran Africa, where 90 percent of the 300 to 500 million
malaria cases and one to three million deaths occur from
malaria each year, still depends on only two technologies
for vector intervention: indoor residual spraying and
insecticide-treated bed nets. Secondly, considerable
research and development on the suppression of mosqui-
toes with the sterile insect technique (SIT) was conducted
from the mid-1950s to the mid-1970s. However, nearly
all of the scientists who pioneered this approach have
retired and several of the greatest have died. While the
benefit of the input, judgement and guidance can be pro-
vided from current experts in this field, a record of the key
contributions of people like Chris Curtis, Ed Knipling and
Don Weidhaas has thus far not been assembled. Thirdly,
there are now new technologies available to support area-
wide integrated pest management (AW-IPM) programmes
and much experience has been gained with the imple-
mentation of these programmes against major insect pests
that could be applied to mosquito control [1,2].

In Europe, north of the Alps and Pyrenees, and in the
United States, malaria began to decline in the mid 1800s
as a result of drainage of swamps, use of screens to exclude
insects on windows and doors, increased availability of
quinine, increased literacy and improved education and
general increase in economic well-being [3]. Endemic


malaria in the USA largely disappeared without the eradi-
cation of the anopheline vectors in the late 1940s, when
malaria cases were aggressively treated and large areas
sprayed with DDT. Eradication of endemic malaria in the
USA probably would have been accomplished even with-
out DDT.

Malaria is transmitted only by mosquitoes in the genus
Anopheles and in sub-Saharan Africa, most transmission
from infected to healthy people is accomplished by three
anopheline species, Anopheles arabiensis, Anopheles funestus
and Anopheles gambiae, with An. gambiae being the most
important. Anopheles gambiae was eradicated in Brazil in
1940 [4] and from Egypt in 1945 [5]. Also, because most
mosquitoes readily enter human dwellings and rest on
walls and ceilings, it was found that they could be killed
through applications of residual insecticides to these sur-
faces. Thus, in the 1930s de Meillon in South Africa had
shown that malaria could be controlled by frequent spray-
ing of the walls and ceilings of dwellings with pyrethrins
[6], and this was substantiated by work in India [7]. The
effectiveness of such residual treatment was found to be
vastly prolonged by the use of DDT [8]. Residual treat-
ment was found to result in the complete interruption of
transmission in Cyprus, Greece, Italy, Sardinia, Taiwan,
Venezuela and the USA. These historic achievements
induced confidence that worldwide eradication of malaria
through vector control was feasible. Thus, in 1955, the
World Health Assembly launched the Global Malaria
Eradication Programme with applications of DDT within
dwellings being the primary stratagem [9].



Page 1 of 4
(page number not for citation purposes)







http://www.malariajournal.com/content/8/S2/ 1


Eradication of malaria was accomplished in due course in
the temperate areas of Europe and Asia, in some subtropi-
cal areas, the Mediterranean Basin, and the southern USA,
and on a number of the tropical islands of the Caribbean
[8], and malaria was greatly reduced in Brazil and India.
Spectacular progress was made in Sri Lanka, where the
number of cases was reduced from a high of two or more
million cases each year in 1958 to just 17 in 1963. In 1964
spraying was halted and the consolidation phase of the
Programme was implemented. Meanwhile, newly discov-
ered gem fields attracted large numbers of miners into the
previously malaria endemic area who dug large numbers
of pits in search of gem-stones. The soon-abandoned pits
filled with water and became the source of dense popula-
tions of Anopheles culicifacies, the main malaria vector
[10]. In 1967 malaria resurged strongly and spraying was
resumed, but the dense vector population was found to
have become resistant to DDT. Malathion was substi-
tuted, but it was objectionable to some families, required
more frequent applications and was more expensive.
Thus, the battle was lost and the incidence of malaria grew
to more than 500,000 cases each year [3].

As described above, some economic development has
diminished transmission, but certain ecological changes,
which attend economic development, strongly favour the
population growth of Anopheles species. In particular,
water development projects (dam construction, expanded
irrigation, production of wetland rice) tend to create ideal
mosquito breeding conditions, while mining, industriali-
zation, urbanization and deforestation also tend to shift
ecological conditions in favour of growth of vector popu-
lations and malaria transmission [10].

By 1966, progress in the eradication of malaria had
slowed noticeably, and in 1967 the World Health Assem-
bly retreated from the goal of global eradication. Thus, the
people of sub-Saharan Africa failed to benefit from the
Global Malaria Eradication Programme (1957-1967).
Nevertheless, the World Health Organization (WHO)
conducted numerous pilot projects in sub-Saharan Africa
to assess the degree of effectiveness of the residual treat-
ment approach alone and in conjunction with mass
administration of anti-malarial drugs. WHO coordinated
a particularly thorough large-scale pilot project in the
Garki District of northern Nigeria from 1969 to 1976. This
study showed that in certain villages, the intensity of
transmission and the vectorial capacity sometimes
approached up to 200 times the critical value for interrup-
tion of transmission and the number of infectious bites
per person per annum (the so-called Entomological Inoc-
ulation Rate) reached 132 in one village during the 6-
month rainy season. Even though residual insecticide
treatment reduced vectorial capacity by 90%, the inci-
dence of malaria was reduced only by 25%. Immigration


of vectors and humans from untreated sites was not con-
sidered to have been a significant factor in causing such
unsatisfactory suppression of malaria. The primary reason
for the lack of high efficacy of the residual treatment
approach was found to be the tendency of the vectors to
rest outdoors after blood feeding (exophily). Even the
addition of mass drug administration at frequent intervals
with strong community participation failed to halt trans-
mission, although it did reduce the incidence of malaria
to very low levels. Thus in such areas where ecological
conditions support extremely high vector populations,
the combination of residual treatment and drug adminis-
tration cannot halt transmission.

The inadequacy of area-wide residual treatment can be
overcome to a significant degree by the area-wide use of
insecticide-impregnated bed nets. While impregnated bed
nets cannot protect against outdoor feeding of a signifi-
cant fraction of the vector population [2], they do prevent
a significant fraction of the vector population from attain-
ing the age of about 12 days the age at which the females
can become infective [11].

Since malaria transmission can be interrupted only if the
density of the vector population is reduced below a critical
level, determined efforts were made from the mid-1950s
to the mid-1970s to develop the SIT for mosquito sup-
pression. Edward F Knipling, the inventor of the tech-
nique, advanced the hypothesis that if sterile males are
released initially at a rate (number per km2) high enough
to cause a decline in the wild population, then the sus-
tained release of this constant number of sterile males into
the wild population each generation will achieve a pro-
gressively greater degree of suppression of the wild popu-
lation in each successive generation [12]. In contrast, an
insecticide at a constant dosage rate tends to kill the same
fraction of an insect population at all population densi-
ties. Further, Knipling posited that the SIT could be inte-
grated with the use of cultural, biological and chemical
measures to achieve robust and powerful systems of pop-
ulation control. The initial reduction of the vector popu-
lation by, say, 90-98 percent, would greatly reduce the
number of sterile males needed to achieve a continuing
downward trend in the population. The SIT, other genetic
methods and sex-pheromone traps are the only methods known
to science, which become progressively more powerful with
decreasing population density of the target pest.

A number of successful small-scale field trials were con-
ducted with one or more species each ofAedes, Culex and
Anopheles [13]. The largest-scale trials were conducted in
El Salvador and India. Unfortunately, both of these trials
were interrupted in the mid-1970s, before they could be
completed. In El Salvador, the work was terminated by the
eruption of civil war and in India by hysteria induced by


Page 2 of 4
(page number not for citation purposes)


Malaria Journal 2009, 8(Suppl 2):11







http://www.malariajournal.com/content/8/S2/ 1


false accusations that the project was intended to collect
data on biological warfare.

In India, the work led by the late Chris Curtis showed that
two important culicine vector species could be mass-
reared, and the sexes separated (according to pupal size)
to ensure that 99.8% of the released insects were males.
Males were either chemosterilized in the pupal stage, or
their sterility was produced by male-linked chromosome
translocations combined either with cytoplasmic incom-
patibility or sex-ratio distortion due to meiotic drive. Field
tests showed that the mating competitiveness of the males
of both species was acceptable. However, the mass release
of Culex quinquefasciatus males in villages achieved only
limited levels of sterility in eggs laid by wild females
because of the influx of already-mated females from out-
side the target release area. A planned mass release of ster-
ile male Aedes aegypti, aimed at the eradication of this
urban mosquito from a whole town, was prevented by the
political problem mentioned above.

In El Salvador, the target was the malaria vector Anopheles
albimanus, and the work was conducted by a team from
the US Department of Agriculture Laboratory, Gainesville,
Florida The wild population was multi-resistant to insec-
ticides (partly due to the agricultural use of insecticides)
and, therefore, difficult to control by conventional means.
In the initial study, releases during five months around
Lake Apastapeque were successful in inducing 100% ste-
rility in eggs laid by wild females. Later, sex separation was
greatly improved by a genetic sexing strain in which a
chromosome translocation was induced to link a pro-
poxur-resistance gene to the Y chromosome, and this was
combined within a crossover-suppressing chromosome
inversion. Propoxur treatment at the egg stage selectively
eliminated all but 0.2% of females, thereby allowing a
doubling of the male production for release. By eliminat-
ing the handling losses in the adult stage, the net release
was increased from 200,000 males per day to over one
million, and these males, when released as sterile pupae,
were almost fully competitive in the field. Compared with
the seasonal upward trend of the untreated population,
the releases reduced the target field population by more
than 97%.

The immigration of females already inseminated by fertile
males outside the release area is a major obstacle to
progress for AW-IPM programmes using sterile insects. In
the case of the New World screwworm, Cochliomyia hom-
inivorax, eradication in North America, this problem was
overcome by large-scale rolling programmes of release of
sterile insects. Ten years ago, Curtis and Andreasen [11]
sadly asserted that "finding the capital for this seems unlikely
for a programme directed against An. gambiae, which extends
over huge areas of rural Africa and threatens the lives of the


children of the poor, but not cash crops which accountants see
as a worthwhile investment."

However, better times are dawning for Africa. The African
Union, formed in 2002 is gradually resolving conflicts
and improving social and economic conditions including
commerce and international trade. African leaders in
2000 had strongly committed their governments to
malaria eradication in the Abuja Declaration and in their
support of the Roll Back Malaria Initiative of the World
Health Organization. Africa has become a priority for
bilateral and multilateral development and public health
assistance. At the 1998 G8 Summit, the leaders of the
world's wealthiest countries pledged to increase donor
funding to combat malaria, and some of this is being pro-
vided by the European Alliance Against Malaria, the Glo-
bal Fund to FightAIDS, Tuberculosis and Malaria, the U.S.
President's Malaria Initiative [14].

There is renewed interest in the scientific community to
improve or even replace the SIT through the techniques of
molecular biology to make Anopheles incapable of trans-
mitting the Plasmodium protozoan parasite. Thus, IAEA
seems to have been especially prescient in initiating rele-
vant planning in 2001 and in launching a project in 2004
to assess the feasibility of the use of the SIT against
selected populations of An. arabiensis in sub-Saharan
Africa. All Africans and all who wish Africa well have a tre-
mendous stake in the outcome. Likewise, this supple-
ment, "Development of the Sterile Insect Technique for
African malaria vectors", will become available early in
this new era when the potential for beneficial impact is
the greatest. The authors of the various chapters deserve
our respect and high praise for assembling a supplement,
which will have to be on the desk of every investigator
interested in combating the vectors of malaria in Africa.

I feel deeply honoured by having been given the privilege
of providing this Foreword of a series of articles that seems
certain to usher in a new successful era in the epic struggle
against malaria, the most deadly and persistent malady of
mankind.

Competing interests
The author declares that they have no competing interests.

Acknowledgements
This article has been published as part of Malaria journal Volume 8 Supple-
ment 2, 2009: Development of the sterile insect technique for African
malaria vectors. The full contents of the supplement are available online at
http://www.malariaiournal.com/supplements/8/S2.

References
I. Koul O, Cuperus GW, Elliot N: Areawide Pest Management Theory and
Implementation Wallingford: CAB International; 2008.



Page 3 of 4
(page number not for citation purposes)


Malaria Journal 2009, 8(Suppl 2): 11








http://www.malariajournal.com/content/8/S2/ 1


2. Vreysen MJB, Robinson AS, Hendrichs J: Area-wide Control of Insect
Pests. From Research to Field Implementation Dordrecht, The Netherlands:
Springer; 2007.
3. Collins FH, Paskewitz SM: Malaria: current and future prospects
for control. Annu Rev Entomol 1995, 40:195-219.
4. Coggeshall LT: Anopheles gambiae in Brazil, 1930 to I940. Geo-
graphical Review 1944, 34:308-310.
5. Shousha AT: Species-eradication. The eradication of Anophe-
les gambiae from Upper Egypt, 1942-1945. Bull World Health
Organ 1948, 1:309-353.
6. de Meillon B: The control of malaria in South Africa by meas-
ures directed against the adult mosquito in habitations.
League of Nations Health Organisation Quarterly Bulletin 1936,
5:134-137.
7. Russell PF, Knipe FW: Malaria control by spray-killing adult
mosquitoes: Third season's results. journal of the Malaria Institute
of India 1941,4:181-197.
8. Gahan JB, Travis BV, Morton FA, Lindquist AW: DDT as a residual
type treatment to control Anopheles quadrimaculatus: practi-
cal tests. j Econ Entomol 1945, 38:23 1-235.
9. Wright JW, Fritz RF, Haworth J: Changing concepts of vector
control in malaria eradication. Annu Rev Entomol 1972,
17:75-102.
10. Gratz NG: Emerging and resurging vector-borne diseases.
Annu Rev Entomol 1999, 44:51-75.
I I. Curtis CF, Andreasen MH: Large-scale control of mosquito vec-
tors of disease. In Areo-wide Control of Fruit Flies and Other Insect Pests
Edited by: Ton K-H. Pulau Pinang: Penerbit Universiti Sains Malaysia;
1998:135-142.
12. Knipling EF: Possibilities of insect control or eradication
through the use of sexually sterile males. J Econ Entomol 1955,
8:459-469.
13. Klassen W, Curtis CF: History of the sterile insect technique. In
Sterile Insect Technique. Principles and Practice in Area-Wide Integrated
Pest Management Edited by: Dyck VA, Hendrichs j, Robinson AS. Dor-
drecht, The Netherlands: Springer; 2005:3-38.
14. Feachem RGA, Sabot OJ: Global malaria control in the 21st cen-
tury. j Am Med Assoc 2007, 297:2281-2284.


Page 4 of 4
(page number not for citation purposes)


Publish with BioMed Central and every
scientist can read your work free of charge
"BioMed Central will be the most significant development for
disseminating the results of biomedical research in our lifetime."
Sir Paul Nurse, Cancer Research UK
Your research papers will be:
available free of charge to the entire biomedical community
peer reviewed and published immediately upon acceptance
cited in PubMed and archived on PubMed Central
yours you keep the copyright

Submit your manuscript here: BioMedcentral
http://www.biomedcentral.com/info/publishingadv.asp


Malaria Joumnal 2009, 8(Suppl 2): 11




University of Florida Home Page
© 2004 - 2010 University of Florida George A. Smathers Libraries.
All rights reserved.

Acceptable Use, Copyright, and Disclaimer Statement
Last updated October 10, 2010 - - mvs