Effects of dietary omega-3 polyunsaturated fatty acids on growth and immune response of weanling pigs

MISSING IMAGE

Material Information

Title:
Effects of dietary omega-3 polyunsaturated fatty acids on growth and immune response of weanling pigs
Physical Description:
Mixed Material
Language:
English
Creator:
Li, Qizhang
Brendemuhl, Joel H.
Jeong, Kwang C.
Badinga, Lokenga
Publisher:
Bio Med Central (JAST, Journal of Animal Science and Technology)
Publication Date:

Notes

Abstract:
The recognition that omega-3 polyunsaturated fatty acids (n-3 PUFA) possess potent anti-inflammatory properties in human models has prompted studies investigating their efficacy for animal growth and immunity. This study examined the effect of feeding an n-3 PUFA-enriched diet on growth and immune response of weanling piglets. Newly weaned pigs (averaging 27 ± 2 days of age and 8.1 ± 0.7 kg of body weight) were assigned randomly to receive a control (3% vegetable oil, n = 20) or n-3 PUFA-supplemented (3% marine n-3 PUFA, n = 20) diet for 28 day after weaning. Female pigs consuming the n-3 PUFA-enriched diet were lighter at week 4 post-weaning than those fed the vegetable oil supplement. Weanling pigs gained more weight, consumed more feed and had better growth to feed ratios between days 14 and 28 than between days 0 and 14 post-weaning. Plasma insulin-like growth factor I (IGF-I) decreased between days 0 (87.2 ± 17.0 ng/mL) and 14 (68.3 ± 21.1 ng/mL) after weaning and then increased again by day 28 (155.2 ± 20.9 ng/mL). In piglets consuming the vegetable oil-enriched diet, plasma tumor necrosis factor alpha (TNF-α) increased from 37.6 ± 14.5 to 102.9 ± 16.6 pg/mL between days 0 and 14 post-weaning and remained high through day 28 (99.0 ± 17.2 pg/mL). The TNF-α increase detected in the piglets fed vegetable oil was not observed in the piglets fed n-3 PUFA. Results indicate that weaning induces considerable immune stress in piglets and that this stress can be mitigated by dietary supplementation of n-3 PUFA. Keywords: n-3 PUFA, Growth, Immunity, Pig
General Note:
Li et al. Journal of Animal Science and Technology 2014, 56:7 http://www.janimscitechnol.com/content/56/1/7; Pages 1-7
General Note:
doi:10.1186/2055-0391-56-7 Cite this article as: Li et al.: Effects of dietary omega-3 polyunsaturated fatty acids on growth and immune response of weanling pigs. Journal of Animal Science and Technology 2014 56:7.

Record Information

Source Institution:
University of Florida
Holding Location:
University of Florida
Rights Management:
© 2014 Li et al.; 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/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
System ID:
AA00026996:00001


This item is only available as the following downloads:


Full Text

PAGE 1

RESEARCHOpenAccessEffectsofdietary omega -3polyunsaturatedfatty acidsongrowthandimmuneresponseof weanlingpigsQizhangLi,JoelHBrendemuhl,KwangCJeongandLokengaBadinga*AbstractTherecognitionthat omega -3polyunsaturatedfattyacids( n -3PUFA)possesspotentanti-inflammatoryproperties inhumanmodelshaspromptedstudiesinvestigatingtheirefficacyforanimalgrowthandimmunity.Thisstudy examinedtheeffectoffeedingan n -3PUFA-enricheddietongrowthandimmuneresponseofweanlingpiglets. Newlyweanedpigs(averaging272daysofageand8.10.7kgofbodyweight)wereassignedrandomlyto receiveacontrol(3%vegetableoil,n=20)or n -3PUFA-supplemented(3%marine n -3PUFA,n=20)dietfor28day afterweaning.Femalepigsconsumingthe n -3PUFA-enricheddietwerelighteratweek4post-weaningthanthose fedthevegetableoilsupplement.Weanlingpigsgainedmoreweight,consumedmorefeedandhadbettergrowth tofeedratiosbetweendays14and28thanbetweendays0and14post-weaning.Plasmainsulin-likegrowthfactor I(IGF-I)decreasedbetweendays0(87.217.0ng/mL)and14(68.321.1ng/mL)afterweaningandthenincreased againbyday28(155.220.9ng/mL).Inpigletsconsumingthevegetableoil-enricheddiet,plasmatumornecrosis factoralpha(TNF)increasedfrom37.614.5to102.916.6pg/mLbetweendays0and14post-weaningand remainedhighthroughday28(99.017.2pg/mL).TheTNFincreasedetectedinthepigletsfedvegetableoil wasnotobservedinthepigletsfed n -3PUFA.Resultsindicatethatweaninginducesconsiderableimmunestressin pigletsandthatthisstresscanbemitigatedbydietarysupplementationof n -3PUFA. Keywords: n-3PUFA,Growth,Immunity,PigBackgroundNutritional,environmentalandimmunechallengesassociatedwithweaningmayleadtoconsiderableeconomic lossestoporkproducers.Thisperiodisgenerallycharacterizedbydecreasedvoluntaryfeedintake,alteredgut integrityandincreasedconcentrationsofinflammatory cytokinesinblood[1-3].Thesenutritionalandphysiologicalabnormalitiesoftenresultindiarrheaanddepressionofgrowthinnewlyweanedpiglets.Restrictionsof antibioticusageinswinehavecompelledtheindustryto findalternativesthatofferbothperformanceenhancementandprotectionfromdisease[4,5].Inthisregard, Liuetal.[6]reportedthatdietaryfishoilreducedthereleaseofpro-inflammatorycytokinesinweanedpigschallengedwith Escherichiacoli lipopolysaccharide.Amore recentstudyindicatedthatprenatalexposuretolongchain n -3PUFAincreasedpostnatalglucoseabsorption inpiglets[7].Althoughexactmechanismsbywhichdietary n -3PUFAmodulateimmuneandmetabolicfunctionsinpigsareyettobefullyelucidated,theabove studywouldindicatethatdietary n -3PUFAmayhelp thepigletsadaptquicklytotherapidlychangingdietat weaning[7]. Currently,thereisverylittleinformationregardingthe useof n -3PUFAinthedietsofpigsraisedunderminimaldiseaseandstressconditions.Totestthehypothesis thatnutritionalmanagementstrategiesthatattenuateintestinalinflammationmaypartitionnutrientstoskeletal muscleforoptimalgrowth,thisstudywasdesignedto examinetheeffectsofdietary n -3PUFAongrowthand immuneresponseofweanlingpigsraisedwithoutan addedbacterialorenvironmentalchallenge. *Correspondence: lbadinga@ufl.edu DepartmentofAnimalSciences,InstituteofFoodandAgriculturalSciences, UniversityofFlorida,Gainesville32611,USA 2014Lietal.;licenseeBioMedCentralLtd.ThisisanOpenAccessarticledistributedunderthetermsoftheCreative CommonsAttributionLicense(http://creativecommons.org/licenses/by/4.0),whichpermitsunrestricteduse,distribution,and reproductioninanymedium,providedtheoriginalworkisproperlycredited.TheCreativeCommonsPublicDomain Dedicationwaiver(http://creativecommons.org/publicdomain/zero/1.0/)appliestothedatamadeavailableinthisarticle, unlessotherwisestated.Li etal.JournalofAnimalScienceandTechnology 2014, 56 :7 http://www.janimscitechnol.com/content/56/1/7

PAGE 2

ResultsanddiscussionWeaningimposestremendousstressonpigletsandis accompaniedbymarkedchangesingastrointestinalphysiology,microbiologyandimmunology[8].Thebiochemical andhistologicalchangesthatoccurinthesmallintestinecauseexcessivesecretionofpro-inflammatorycytokinesandinducesevereintestinalinflammation. Omega -3 PUFAareknowntopossessanti-inflammatoryproperties inhumans[9,10],swine[6,11]andchickens[12].Totest thehypothesisthatnutritionalmanagementstrategiesthat attenuateintestinalinflammationmayrepartitionnutrientstotissueaccretion,weexaminedtheeffectsofdietary n -3PUFAongrowthandimmuneresponseofweanling pigs(Figure1)raisedwithoutanaddedbacterialorenvironmentalchallenge. Inclusionof3% n -3PUFAintheweanlingpiglet ’ sdiet didnotresultinsignificantlyimprovementofaverage dailygain(ADG),averagedailyfeedintake(ADFI)or growthtofeedratio(G:F)inweanlingpigs.Thesefindingsareconsistentwithanearlierstudy[13]whichdetectednoeffectsofdietaryflaxseedmeal(richinalpha linolenicacid)onbasalbodyweightgain,feedintakeor feedefficiencyinweanlingpigs.Additionalstudiesusing controldietswithless18:3 n -3areneededtoexaminetrue effectsoflong-chain n -3PUFAongrowthandfeedintakeresponses.Femalepigletsconsumingthe n -3PUFAsupplementeddietwerelighteratweek4post-weaning thanthoseconsumingthevegetableoil-enricheddiet. Whetherornotthisphenomenonwasduetoalteration inbodycompositionasaresultoffeeding n -3PUFAto nurserypigswasnotdocumented.Inrodents[14-16] andhumans[17,18],dietsrichin n -3PUFAlowerfat storesandincreaseleantissuemass.Itis,therefore, possiblethatthesmallerbodyweightoffemalepiglets Figure1 Bodyweightsofmale(A)andfemale(B)pigsduringfourweeksafterweaning. Adietxgenderxweekinteractionwasdetected ( P <0.04)forbodyweight.Asteriskindicatessignificantdifference( P <0.01)atthespecifiedweek. Li etal.JournalofAnimalScienceandTechnology 2014, 56 :7Page2of7 http://www.janimscitechnol.com/content/56/1/7

PAGE 3

consuming n -3PUFAdetectedatweek4post-weaning wasduetoadecreaseinfataccretionattheexpenseof leantissue.Theimprovementofbodyweightgaindetectedinexperimentalanimalsbetweendays14and28 post-weaninglikelyresultedfromanincreaseinfeedintakeandadecreaseinbasalinflammatorychallenges duringthesecondphaseofgrowth(Figure2). ConcentrationsofIGF-Iinplasmadecreasedimmediatelyfollowingweaningandincreasedagainbyday28 post-weaning(Figure3).Thesefindingsindicatethat weaningmaycauseasignificantmetabolicstressin weanlingpigsandthatthisstressdecreaseswithincreasingweeksafterweaning.Thereislittleinformationon theeffectofdietary n -3PUFAonperipheralconcentrationsofgrowthfactorsinthepig.Inthepresentstudy, inclusionof3% n -3PUFAintothepiglet ’ sdiethadno detectableeffectsonplasmaIGF-Iconcentrationduring thefirstfourweeksafterweaning.Theseobservations areconsistentwithpreviousstudies[6,13]whichshowed nobeneficialeffectsofdietaryfishoilonbasalIGF-I concentrationinweanedpigs.ThissenandVerniers[19] reportedthatIL-6andTNFdecreasedbothgrowth hormone(GH)andIGF-ImRNAinrathepatocyte primarycultures.WedidnotexamineGHorIGF-Itranscriptmodulationbyinflammatorycytokines,andtherefore,whetherornotthelackof n -3PUFAeffectson plasmaIGF-Iconcentrationdetectedinthepresentstudy wasindicativeofcytokine-mediateduncouplingofGH andIGF-Igeneexpressioninweanlingpigswarrantsfurtherinvestigation. Tumornecrosisfactor,acytokineproducedprimarilybymonocytesandmacrophages,isthoughttobe oneoftheprincipalmediatorsofinflammation[20].In thepresentstudy,plasmaTNFconcentrationswere lowerinweanlingpigletssupplementedwith n -3PUFA thanthosefedthevegetableoilsupplement(Figure3). Thesefindingsareconsistentwithpreviousinvitro [21-23]andinvivo[11,24,25]studiesandsuggestthat n -3PUFAinclusioninthedietcouldmitigatetheimmunestressinweanlingpigs.Whereasexactmechanismsof n -3PUFAsuppressionofTNFareyettobe fullyelucidated,wespeculatethatsuppressionofTNFproductionby n -3PUFAmaybeattributed,inpart,to theirinhibitoryeffectsonNFBactivationandortranslocationtothenucleus[9,22,23].NuclearfactorBare normallyconfinedinthecytoplasmthroughtheirassociationwithI .Whencellsareactivatedbyinflammatory stimuli,theI arerapidlyphosphorylatedanddegraded tofreetheNF.ThefreeNFthenmigratetothenucleuswheretheybindtocognateDNAbindingsitesand activateinflammatorygenetranscription[9].Anyfactor thatpreventsI phosphorylationand,thus,NFactivation,willdecreasepro-inflammatorygeneexpressioninthenucleus.Additionally,long-chainPUFAserve asligandsforperoxisomeproliferator-activatedreceptors (PPAR),whichareknowntoinhibitnucleartranslocation ofNF[9].Thus,activationofPPARmaybeanother intracellularmechanismbywhichmarine n -3PUFA regulateNFactivationandTNFproductionin animalmodels[9]. Hematologicaltraitsofswineareinfluencedbyavarietyofenvironmentalandphysiologicalfactorsincluding diet,age,genderandhousing[26,27].Inthepresentstudy,mostofthebloodcharacteristicsexamineddidnot differamongpigsfedthetwodiets(Table1).Bloodsamplesforcompletebloodcellcountswerecollectedat Figure2 Averagedailyfeedintake(A),gain(B)andG:F(C)of weanlingpigletsfeddietswithvegetableoil(Control,n=20)or n -3PUFA(Omega,n=20). Foreachresponse,pairsofhistograms withdifferentsuperscriptsaredifferentat P <0.01.Therewereno differencesamongresponses(P>0.05)duetothedietarytreatment. Li etal.JournalofAnimalScienceandTechnology 2014, 56 :7Page3of7 http://www.janimscitechnol.com/content/56/1/7

PAGE 4

4weeksafterweaning,anditispossiblethatbythis samplingtime,theweanlingpigletshadalreadyrecoveredfrommostphysiologicalanddietarychallengesnormallyassociatedwithweaninginpigs.Alternatively,the pigletsusedinthisstudywereraisedinacleanenvironmentand,thus,maynothaveacquiredthe “ normal ” gastrointestinalmicroflorathatwouldcauseclinicaldiseases.Thishypothesiswasfurthersupportedbyourinabilitytodetectsalmonellaandenterotoxigenic E.coli in fecalsamplescollectedatweek4post-weaning(datanot shown).ConclusionsInthepig,theperiodfollowingweaningisgenerally characterizedbysub-optimalgrowth,deterioratedfeed efficiency,andahighincidenceofdiarrhea.Resultsof thisstudyprovidednoevidencefor n -3PUFAmodulationofgrowthofmaleweanlingpigsraisedintheabsenceofsignificantimmunologicalandenvironmental challenges.Theobservationthatfemalepigletsconsumingthe n -3PUFA-supplementeddietwerelighterat week4post-weaningthanthoseconsumingthevegetableoil-enricheddiet(Figure2)maybeindicativeofa decreaseinfataccretionattheexpenseofleantissue. Additionally,dietary n -3PUFAmayimprovetheimmunestatusofweanlingpigs,asreflectedbyconsiderablylowerplasmaTNFinpigsconsuming n -3PUFA thanthosefedvegetableoil.Thegradualincreaseinbody weight,feedintakeandfeedefficiencyfollowingweaning likelyreflectsaprogressiveadaptationtopost-weaning dietsandagradualimprovementofthegastrointestinal microbiota.MethodsAnimals,dietsandexperimentaldesignTheanimalprotocolforthisresearchwasapproved bytheinstitutionalAnimalResearchCommitteeofthe UniversityofFlorida.Toavoidpotentialdifferencesdue tofarrowingseason,thestudywasconductedusing40 pigletsbornwithinoneweekattheSwineResearch UnitoftheUniversityofFlorida(Gainesville,FL)during themonthofMarch2013.Fortycrossbredpigs(averaging 272daysofageand8.10.7kgofbodyweight)were balancedforinitialbodyweightandgenderacrosstwo treatmentgroupsinacompleterandomizedblockdesign.Experimentalanimalswerefedeitheracontrol(3% vegetableoil,n=20)or n -3PUFA(3%marine n -3PUFA; Gromega345 ,JBSUnited,Inc,SheridanIN,n=20)supplementeddietforfourweeksafterweaning.The vegetableoilwaspurchasedfromSyscoCorporations (Houston,TX)andcontainedapproximately22%total fat.Omega-3fattypolyunsaturatedfattyacidsusedinthis studywereprovidedbyJBSUnited(Sheridan,Indiana) Figure3 ConcentrationsofIGF-I(A)andTNF(B)inplasmaof weanlingpigletsfeddietswithvegetableoil(Control,n=20) or n -3PUFA( Omega ,n=20). PlasmaIGF-Iconcentrationswere affectedbythegrowthphase( P <0.01),butnotthedietarytreatment ( P >0.44).PlasmaTNFconcentrationswereaffectedbythedietary treatment( P <0.01),butnotthegrowthphase( P >0.28). Table1Hematologicaltraitsofweanlingpigsfeddiets withvegetableoilorlong-chain omega -3fattyacidsaTraitExperimentaldietsbSEMPcControlOmega WBCd103/mm314.215.71.20.44 Lymphocytes,%42.341.54.00.90 Neutrophils,%52.851.03.80.75 Eosinophils,%1.52.80.40.07 Monocytes,%2.54.30.70.13 RBCe103/mm37.06.60.30.45 Hemoglobin10.49.20.70.28 Hematocrit,%34.131.42.10.41 Platelets103/mm3378.5674.080.40.04aMeansrepresent4pigsperdietarytreatment.bDietswere:Control(3%vegetableoil)and omega (3%GromegaUltra345, providedbyJBSUnited,Inc.,Sheridan,IN).cP -valuesforcontrolcomparedtoOmegadiet.dWhitebloodcells.eRedbloodcells.Li etal.JournalofAnimalScienceandTechnology 2014, 56 :7Page4of7 http://www.janimscitechnol.com/content/56/1/7

PAGE 5

andcontainedaminimumof39%crudefat.CompleteingredientcompositionsandFAprofilesofexperimentaldietsaresummarizedinTables2and3,respectively.Pigs werehousedinpens(groupsof5animalsperpen;pen size=2.4m1.8m)andkeptonthesamedietforthe entireexperimentalperiod.Bodyweightandfeedconsumptionwererecordedweeklythroughoutthe4-week experiment.Theseobservationswereusedtocalculate ADG,ADFI,andG:F.BloodcollectionandanalysisOndays0,14and28oftheexperiment,jugularvenous bloodsamples(8mlfromeachexperimentalpig)were collectedintoevacuatedheparinizedtubes(BDFranklin Lakes,NJ)andcentrifuged(3,000 g for15min)toseparateplasma.Theplasmasampleswerestoredat 80C untilanalysis.ConcentrationsofIGF-IandTNFin plasmawereanalyzedusingcommerciallyavailableELISA kits(R&DSystems,Inc.,Minneapolis,MN).Hormone andcytokineanalyseswereperformedinsingleassaysand intra-assayCVwere4.0and4.7%forIGF-IandTNF, respectively.Theleastdetectableconcentrationswere 0.06ng/mLand5.50pg/ml.Onday27oftheexperiment, additionalbloodsampleswerecollectedforcomplete bloodcellcounts,andhematologicaltraitsweredeterminedasdescribedbyQuiroz-Rochaetal.[28].FecalevaluationTwofecalconsistencyscoreswereassignedtoeachpen onweeks1,2,3,and4post-weaning.Thescaleusedto assessfecalconsistencywasbasedonanumericalscale Table2Ingredientandcalculatedcompositionsof experimentaldietsCompositionExperimentaldietsaOmega Control Ingredient: Corn,%61.9061.90 Soybeanmeal,%25.0025.00 Vegetableoil,%3.00GromegaUltra345,%-3.00 Min-VitPremix,%10.0010.00 L-Lysine.HCL,%0.100.10 Calculatedcomposition: ME,kcal/kg3282.383282.38 CP,%19.5319.53 CF,%3.393.39 Lysine,%1.401.40 Calcium,%0.780.97 Phosphorus,%0.630.63aDietswere:Control(3%vegetableoil)andomega(3%GromegaUltra345, providedbyJBSUnited,Inc.,Sheridan,IN). Table3Fattyacidprofile(g/100goftotalfat)of experimentaldietsaFattyacidExperimentaldietsbOmega Control C14:00.212.61 C15:00.002.61 C16:014.6819.76 C16:1,9c0.322.98 C17:00.130.42 C17:10.000.39 C18:04.264.71 C18:1,9c24.7223.89 C18:2 n -649.7937.04 C18:3 n -34.532.15 C18:4 n -30.000.47 C20:00.380.40 C20:1 n -90.000.71 C20:5 n 30.001.30 C22:00.410.26 C22:5 n -30.000.26 C22:6 n -30.000.96 C24:00.260.34 n -649.7937.04 n -34.535.54 n6/ n -310.996.69 SFA20.3328.79 UFA79.3670.15aFattyacidanalysiswasperformedbytheUniversityofMissouriAnalytical Laboratory.bDietswere:Control(3%vegetableoil)and omega (3%GromegaUltra345, providedbyJBSUnited,Inc.,Sheridan,IN). Table4Fecalconsistencyscoresaofweanlingpigsfed dietswithvegetableoilorlong-chain omega -3fatty acidsbWeek post-weaning DietscOmega SEMPdControl 12.62.50.20.67 21.91.90.21.00 32.01.90.20.68 41.31.10.20.68aThescaleusedforassessingfecalconsistencywasbasedonanumericalscale of1to3,where1representedanormal(hard)feces,2representedasoft moistfeces,and3representeddiarrhea(wateryliquid).bMeansrepresentaveragefecalscoresfor4pensperdietarytreatment.cDietswere:Control(3%vegetableoil)and omega (3%GromegaUltra345, providedbyJBSUnited,Inc.,Sheridan,IN).dP -valuesforcontrolcomparedto Omega diet.Li etal.JournalofAnimalScienceandTechnology 2014, 56 :7Page5of7 http://www.janimscitechnol.com/content/56/1/7

PAGE 6

of1to3,where1representedanormal(hard)feces,2 representedasoft(moist)feces,and3representeddiarrhea(wateryliquid).Theweeklyscoreforeachpenwas calculatedbyaveragingthetwofecalconsistencyscores (Table4).StatisticalanalysisEffectsofdietsongrowth,IGF-I,TNFandfecalcharacteristicswereanalyzedusingtheMIXEDprocedure ofStatisticalAnalysisSystem(version9.3)withrepeatedmeasures[29].Forindividualmeasurements(body weights),fixedeffectsincludeddiet,gender,dietgender interaction,weekafterweaning,dietweekinteraction, genderweekinteractionanddietgenderweekinteraction.Thepig,nestedwithingenderanddiet,wasconsideredarandomvariable,andthereforethepigvariance wasusedtotesttheeffectsofdiet,gender,anddietxgenderinteraction.Initialweightswereusedascovariatesin theseanalyses.Asimilarmodelwasusedtotesttheeffect ofdietonplasmaIGF-IandTNFconcentrations,except thatweekafterweaningwasreplacedbydayofblood samplecollection.Forcollectivemeasurements(feedintake,averagedailygain,feedefficiency,andfecalconsistencyscore),thestatisticalmodelincludedtheeffectof diets,pen(diet),weekrelativetoweaning,dietweek interaction.Inthesemodels,penwasusedasexperimentalunittotestthemaineffectofdiet.Singlebloodsampleswerecollectedforcompletebloodcellcounts,and, therefore,thestatisticalmodelsforhematologicaltraits containedonlythemaineffectofdiet.Forallresponses,significantdifferencesbetweenmeansweredeclared at P <0.05.Abbreviations ADFI: Averagedailyfeedintake;ADG:Averagedailygain;G:F:Gaintofeed ratio;GH:Growthhormone;IGF-I:Insulin-likegrowthfactorI;PPAR: Peroxisomeproliferator-activatedreceptors;RBC:Redbloodcells; TNF:Tumornecrosisfactoralpha;WBC:Whitebloodcells. Competinginterests Theauthorsdeclarethattheyhavenocompetinginterests. Authors ’ contributions QLcarriedouttheexperimentandwasresponsibleforfielddataprocessing andlaboratoryanalysis.JHBwasinvolvedinthedesignandorganizationof theexperimentattheUniversityofFloridaSwineUnit.KCJperformed bacterialanalysisoffecesandcontributedsubstantiallytothewritingofthe manuscript.LBwasinvolvedinthedesign,analysisandexecutionofthe experimentandhadprimaryresponsibilityfordataprocessingandwritingof themanuscript.Allauthorsreadandapprovedthefinalmanuscript. Acknowledgements TheauthorsthankJBSUnited,Inc(Sheridan,IN,USA)forkindlyproviding GromegaUltra345 forthisresearchandtheUniversityofFloridaSwineUnit crewfortheirhelpwiththefieldwork.Thepresentstudywassupported partiallybytheDepartmentofAnimalSciencesoftheUniversityofFlorida. Received:31May2014Accepted:17July2014 Published:24July2014 References1.LeDividichJ,SveB: Effectsofunderfeedingduringtheweaningperiod ongrowth,metabolism,andhormonaladjustmentsinthepiglet. Domest AnimEndocrinol 2000, 19: 63 – 74. 2.MontagneL,BoudryG,FavierC,LeHurou-LuronI,LallsJP,SveB: Main intestinalmarkersassociatedwiththechangesingutarchitectureand functioninpigletsafterweaning. BrJNutr 2007, 97: 45 – 57. 3.PiS,LallsJP,BlazyF,LaffitteJ,SveB,OswaldIP: Weaningisassociated withanup-regulationofexpressionofinflammatorycytokinesinthe intestineofpiglets. JNutr 2004, 134: 641 – 647. 4.CromwellGL: Whyandhowantibioticsareusedinswineproduction. AnimBiotechnol 2002, 13: 7 – 27. 5.VondruskovaH,SlamovaR,TrckovaM,ZralyZ,PavlikI: Alternativesto antibioticgrowthpromotersinpreventionofdiarrhoeainweaned piglets:areview. VetMedic 2010, 5: 199 – 224. 6.LiuYL,LiDF,GongLM,YiGF,GainesAM,CarrollJA: Effectsoffishoil supplementationontheperformanceandimmunological,adrenal,and somatotropicresponsesofweanedpigsafteranEscherichiacoli lipopolysaccharidechallenge. JAnimSci 2003, 81: 2758 – 2765. 7.GablerNK,RadcliffeJS,SpencerJD,WebelDM,SpurlockME: Feeding long-chain n -3polyunsaturatedfattyacidsduringgestationincreases intestinalglucoseabsorptionpotentiallyviatheacuteactivationof AMPK. JNutrBiochem 2009, 20: 17 – 25. 8.HeoJM,OpapejuFO,PluskeJR,KimJC,HampsonDJ,NyachotiCM: Gastrointestinalhealthandfunctioninweanedpigs:areviewoffeeding strategiestocontrolpost-weaningdiarrhoeawithoutusingin-feed antimicrobialcompounds. JAnimPhysiolAnimNutr 2012, 97: 207 – 237. 9.CalderPC: Omega-3fattyacidsandinflammatoryprocesses. Nutrients 2010, 2: 355 – 374. 10.CalderPC: Omega-3polyunsaturatedfattyacidsandinflammatory processes:nutritionorpharmacology? BrJClinPharmacol 2012, 75: 645 – 662. 11.CarrollJA,GainesAM,SpencerJD,AlleeGL,KatteshHG,RobertsMP, ZannelliME: Effectofmenhadenfishoilsupplementationand lipopolysaccharideexposureonnurserypigs.I.Effectsontheimmune axiswhenfeddietscontainingspray-driedplasma. DomestAnimEndocrinol 2003, 24: 341 – 351. 12.KorverDR,KlasingKC: Dietaryfishoilaltersspecificinflammatory immuneresponsesinchicks. JNutr 1997, 127: 2039 – 2046. 13.EastwoodL,KishPR,BeaulieuAD,LetermeP: Nutritionalvalueofflaxseed mealforswineanditseffectsonthefattyacidprofileofthecarcass. JAnimSci 2009, 87: 3607 – 3619. 14.BaillieRA,TakadaR,NakamuraM,ClarkeSD: Coordinateinductionof peroxisomalacyl-CoAoxidaseandUCP-3bydietaryfishoil:amechanism fordecreasedbodyfatdeposition. ProstaglandinsLeukotEssentFattyAcids 1999, 60: 351 – 356. 15.BelzungF,RaclotT,GroscolasR: Fishoiln-3fattyacidsselectivelylimit thehypertrophyofabdominalfatdepotsingrowingratsfedhigh-fat diets. AmJPhysiol 1993, 264: R1111 – R1118. 16.HillJO,PetersJC,LinD,YakubuF,GreeneH,SwiftL: Lipidaccumulation andbodyfatdistributionisinfluencedbytypeofdietaryfatfedtorats. IntJObesRelatMetabDisord 1993, 17: 223 – 236. 17.JumpDB,ClarkSD,ThelenA,LiimattaM: Coordinateregulationof glycolyticandlipogenicgeneexpressionbypolyunsaturatedfattyacids. JLipidRes 1994, 35: 1076 – 1084. 18.NoreenEE,SassMJ,CroweML,PabonVA,BrandauerJ,AverillLK: Effectsof supplementalfishoilonrestingmetabolicrate,bodycomposition,and salivarycortisolinhealthyadults. JIntSocSportsNutr 2010, 7: 31 – 37. 19.ThissenJP,VerniersJ: Inhibitionbyinterleukin-1 andtumornecrosis factoroftheinsulin-likegrowthfactorImessengerribonucleicacid responsetogrowthhormoneinrathepatocyteprimaryculture. Endocrinology 1997, 138: 1078 – 1084. 20.BemelmansMH,vanTitsLJ,BuurmanWA: Tumornecrosisfactor:Function, releaseandclearance. CritRevImmunol 1996, 16: 1 – 11. 21.LoCJ,ChiuKC,FuM,LoR,HeltonS: Fishoildecreasestumornecrosisfactor genetranscriptionbyalteringtheNFactivity. JSurgRes 1999, 82: 216 –221. 22.NovakTE,BabcockTA,JhoDH,HeltonWS,EspatNJ: NFBinhibition by -3fattyacidsmodulatesLPS-stimulatedmacrophageTNFtranscription. AmJPhysiolLungCellMolPhysiol 2003, 284: L84 – L89. 23.ZhaoY,Joshi-BarveS,BarveS,ChenLH: Eicosapentaenoicacidprevents LPS-inducedTNFexpressionbypreventingNF-kBactivation. JAmColl Nutr 2004, 23: 71 – 78.Li etal.JournalofAnimalScienceandTechnology 2014, 56 :7Page6of7 http://www.janimscitechnol.com/content/56/1/7

PAGE 7

24.GainesAM,CarrollJA,YiGF,AlleeGL,ZannelliME: Effectofmenhadenfish oilsupplementationandlipopolysaccharideexposureonnurserypigs.II. Effectsontheimmuneaxiswhenfedsimpleorcomplexdiets containingnospray-driedplasma. DomestAnimEndocrinol 2003, 24: 353 – 365. 25.MalekshahiMoghadamA,SaedisomeoliaA,DjalaliM,DjazayeryA,PooyaS, SojoudiF: Efficacyofomega-3fattyacidsupplementationonserum levelsoftumournecrosisfactor-alpha,C-reactiveproteinand interleukin-2intype2diabetesmellituspatients. SingaporeMedJ 2012, 53: 615 – 619. 26.FriendshipRM,LumsdenJH,McMillanI,WilsonMR: Hematologyand biochemistryreferencevaluesforOntarioswine. CanJCompMed 1984, 48: 390 – 393. 27.WilsonGD,HarveyDG,SnookCR: Areviewoffactorsaffectingblood biochemistryinthepig. BrVetJ 1972, 128: 596 – 610. 28.Quiroz-RochaGF,LeBlancSJ,DuffieldTF,WoodD,LeslieKE,JacobsRM: Referencelimitsforbiologicalandhematologicalanalytesofdairy cowsoneweekbeforeandoneweekafterparturition. CanVetJ 2009, 50: 383 – 388. 29.LittellRC,HenryPR,AmmermanCB: Statisticalanalysisofrepeated measuresdatausingSASprocedures. JAnimSci 1998, 76: 1216 – 1231.doi:10.1186/2055-0391-56-7 Citethisarticleas: Li etal. : Effectsofdietary omega -3polyunsaturated fattyacidsongrowthandimmuneresponseofweanlingpigs. Journalof AnimalScienceandTechnology 2014 56 :7. Submit your next manuscript to BioMed Central and take full advantage of: € Convenient online submission € Thorough peer review € No space constraints or color “gure charges € Immediate publication on acceptance € Inclusion in PubMed, CAS, Scopus and Google Scholar € Research which is freely available for redistribution Submit your manuscript at www.biomedcentral.com/submit Li etal.JournalofAnimalScienceandTechnology 2014, 56 :7Page7of7 http://www.janimscitechnol.com/content/56/1/7