The effect of maternal nutritional status during mid-gestation on placental characteristics in ewes

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Animal

Reproduction

Science

j o ur na l ho me p ag e :w w w. e l s e v i e r . c o m / l o c a t e / a n i r e p r o s c i

The

effect

of

maternal

nutritional

status

during

mid-gestation

on

placental

characteristics

in

ewes

U.

Sen

_,

_E.

_Sirin

_,

_M.

_Kuran

a_{OndokuzMayisUniversity,AgriculturalFaculty,Kurupelit,TR55139Samsun,Turkey}

b_{AhiEvranUniversity,AgriculturalFaculty,Asikpasa,TR40100Kirsehir,Turkey}

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received15February2012

Receivedinrevisedform

22November2012

Accepted29November2012

Available online 7 December 2012 Keywords:

Maternalnutrition

Mid-gestation Placenta Cotyledon

Lambbirthweight

a

b

s

t

r

a

c

t

Theaimofthisstudywastodeterminetheeffectsofmaternalnutritionalstatus dur-ingmid-gestationonplacentalcharacteristicsinewes.Timeofestrusof3–5yearsold Karayakabreedeweswassynchronizedandmatingwasmonitoredtodeterminetheday0 ofgestation.Theeweshadsimilarbodyweights(47.8±0.7kg)andloineyemusclevalues (thickness;20.9±1.0mmandfatthickness;4.7±0.5mm)atmating.Theeweswere allo-catedintotwotreatmentgroupsatday30ofgestation;under-fed(UF;n=12)andwell-fed (WF;n=13)groups.TheewesinUFgroupwerefedwithadiettoprovide50%oftheirdaily requirementfromday30today80ofgestationand100%oftheirdailyrequirementduring therestofthegestationperiod.TheewesinWFgroupwerefedatleast100%oftheirdaily requirementthroughoutgestation.ThesingletonbearingewesintheUFgrouphadalesser (P<0.05)placentalweight(354.1comparedwith378.3g),averagecotyledonweight(1.50 comparedwith1.82g)andlambbirthweight(3.8comparedwith4.2kg)thansingleton bearingewesintheWFgroup.Therewerepositivecorrelationsbetweenplacentalweight andlambbirthweight(r=.469;P<0.05),placentalweightandaveragecotyledonweight (r=.695;P<0.01),averagecotyledonweightandlambbirthweight(r=.742;P<0.01)and placentalefficiencyandcotyledondensity(r=.853;P<0.01)forewesinWFgroup. Addi-tionally,thepatternofweightgain/losswasdifferent(P<0.05)betweenthetwogroups. EwesinUFgrouplostbodyweightprogressivelyfromday30ofgestationuntilday80. Theresultsofpresentstudyshowthatunder-feedingofewesduringmid-gestationmay causeaninsufficientplacentaldevelopmentandhencealterfetaldevelopmentresultingin areducedbirthweightfromsingletonpregnancies.

© 2012 Elsevier B.V. All rights reserved.

1. Introduction

Maternal nutrient intakeduring gestation in various speciesaffectsthesizeanddevelopmentofboththe pla-centaandthefetus(Redmeretal.,2004).Survivalofthe fetusisaffectedespeciallybysufficiencyoftheplacenta (Mellor and Stafford, 2004). Furthermore, the size and

∗ Correspondingauthorat:OndokuzMayisUniversitesi,Ziraat

Fakul-tesi,Kurupelit,TR55139Samsun,Turkey.Tel.:+903624576086;

fax:+903624576034.

E-mailaddress:[email protected](M.Kuran).

nutrienttransfer capacityof theplacentaplay a central roleindeterminingtheprenatalgrowthtrajectoryofthe fetusandresultinginlong-termprogrammingeffectson birthweight,postnatalgrowth,viability,productivityand long-termhealthoftheoffspring(McMullenetal.,2005). Maternal nutrient restrictionduring gestationhas been reportedtocauseareduction inproliferationof placen-tal mass, as well as impaired umbilical blood flows. A poorlydevelopedplacentarestrictsnutrientand respira-torygasessupply,leadingtofetalhypoxia,hypoglycemia or low nutrientuptakes, asymmetricorgan growthand reducedfetal growthrates(Wuetal.,2006;Ocaket al., 2009).Indeedtheimportanceoftheplacentalcirculationis

0378-4320/$–seefrontmatter © 2012 Elsevier B.V. All rights reserved.

exemplifiedbythecloserelationshipsamongfetalweights, placentalweightsandutero-placentalbloodflowsin nor-malandgrowthrestrictedpregnancies(Greenwoodetal., 2000; Redmer et al., 2004). Severe restrictions of sub-stratesupplymayresultinmaternal,placentalandfetal adaptationstothealteredpre-natalenvironment,which allowssurvival oftheoffspring, oftenattheexpenseof thenormalfetaldevelopment(Quigleyetal.,2008).There isincreasingevidencefromepidemiological and experi-mentalstudiesthattheprogrammingoffetaldevelopment maybeparticularlysensitivetomaternalnutrientstatus duringtheperi-conceptionperiod(Robinsonetal.,1997; Quigleyetal., 2005;Hernandezetal.,2009; Igwebuike, 2010).Thus,itisobviousthatamountofmaternal nutri-tionaffectingplacentalvasculardevelopmentwillhavea dramaticimpactonfetalgrowthanddevelopment.

Attachmentoffetalcotyledonstothematernal carun-clesoccursbetweendays25and30ofgestationinsheep, and growthrestriction duringthis period can limit the eventualnumberofplacentomesthatformtheplacenta (Igwebuike, 2010). The majority of placental growth in termsofmassandnetcellularproliferationoccursduring thefirsttwo-thirdsofgestationinsheep(Redmeretal., 2004; Igwebuike,2010). Also, the placentaachieves its maximumweightbyday90ofgestationandnochangein tissuedrymattercontentoccursthereafter(Samminetal., 2009;Igwebuike,2010).Duringthisperiod,thefetushas only10%ofitseventualbirthweightbythetimethe pla-centahasreacheditsmaximumsize(Redmeretal.,2004; Samminetal.,2009).Inthiscontext,approximately90% offetal growthoccursduringthelast thirdof gestation whenafterthecompletedevelopmentoftheplacentain sheep(Redmeretal.,2004).Theindicationisthatplacental sizeandevenfunctionlateringestationmaybe substan-tiallyinfluencedatthisearlystageinsheep(Igwebuike, 2010).

Theconsequencesofnutritionstatusinthefirsthalfof pregnancyforruminantplacentalgrowthhavebeenrarely studied.However,availableevidencesupporttheideathat placentalgrowth,andbyimplication,fetalgrowthismost vulnerabletomaternalnutritionalstatusduringthe peri-implantation period and thefirst trimester of gestation whenrapidplacentaldevelopmentoccurs(Wuetal.,2004). Theusualmatingperiodofewesinmostpartsoftheworld coincideswiththeautumnandearlywintermonthsduring whichnutrientintakeofpregnantewesmaybelessthanat othertimesoftheyearduetopoorrangelandquality.Thus itcanbepostulatedthatmostofsheepinmostpartsofthe worldexperiencemalnutritionduringthegestationperiod which maycausealtered placental development result-inginlesserbirthweightsandpooreradultperformance postweaningduetonutritionalprogrammingeffects dur-inggestation.Theaimofthepresentstudy,therefore,was todeterminetheeffectsofmaternalnutritionalstatus dur-ingmid-gestationonplacentalcharacteristicsinsingleton bearingewes.Itiswellknownthatlittersizehasa signif-icantroleintheplacentalsize(Konyalietal.,2007;Ocak etal.,2009).TheKarayakabreedsheepusedinthisstudy isagoodmodelforassessingnutritionalinfluenceson pla-centalcharacteristicsbecausethisbreedisknownforlow prolificacy(approximately1.1)thustheinfluenceoflitter

sizeonplacentalcharacteristicswasminimizedbyusing thisbreed.

2. Materialsandmethods

The experimental procedures were approved by the Local AnimalCareand EthicsCommitteeof Gaziosman-pasaUniversity,Tokat,Turkeyensuringcompliancewith ECDirective86/609/EECforanimalexperiments.Thestudy wasconductedwithinthenormalseasonalbreedingcycle of ewes in Turkey (Septemberto March). Experimental animals were of the Karayaka breed,3–5 years of age, andmaintainedattheSheepFarmofGaziosmanpasa Uni-versity,Tokat,Turkey(40◦31N,36◦53Eand650mabove thesealevel).Timeofestruswassynchronizedbyuseof intravaginalspongescontaining30mgflugestoneacetate (Chronogest;Intervet,Turkey)for12daysfollowedbyan intramuscularinjectionof1mlofPGF2␣(Dinolytic;5mg

PF2␣/ml,Pharmacia,Belgium).Forty-eighthourslater,the eweswereintroducedtoKarayakarams(approximately oneramtoevery10ewes),andthematingwasmonitored todetermineday0ofgestation.Theeweshadsimilarbody weightsandeyemusclevalues,measuredbyanultrasonic linearprobeatmating.

Eweswerehousedinindividualpensatday55of gesta-tion.Themeanbodyweightsofewesweredeterminedat days30,45,60and80ofgestationandatbirth. Addition-ally,lointhicknessandfatthicknessvaluesofeyemuscle weredeterminedat days30 and80 ofgestationand at birth.Theeweswereallocatedintotwotreatmentgroups; under-fed(UF;n=12)andwell-fed(WF;n=13)groups.The ewesinWFgroupwerecomposedoftwosub-groups;ewes offeredwithadiettobefedeitheradlibitum(sub-group1; n=4;consumed175%ofthedailyrequirements)or100% oftheirdailyrequirements(sub-group2;n=9)fromday 30today80ofgestation.Thesetwosub-groupswere com-bined, becausethere werenodifferencesbetweenewes whenallvariablesweremeasured.TheewesinUFgroup were fedwith a diet tomeet 50%of thedaily require-mentsfromday30today80ofgestation.Duringtherest ofthegestationperiod,theewesinbothgroupswerefed withadiettomeet100%ofthedailyrequirements.The dailyDMrequirementsofewesthroughoutthisstudywere calculatedonanindividualewebodyweightbasis.Diets were composedof concentrate (89.5%DM, 23.4% crude proteinand 10.9MJME/kgDM),and goodqualityalfalfa hay(88.4%DM,16.8%crudeproteinand8.2MJME/kgDM). Theamountsof concentrateandhayconsumptionwere 991.3±77.1and975.9±29.1g/day/eweinWFgroup,and 200.0±0.2and468.4±8.9g/day/eweinUFgroup, respec-tively.Dietsweregivendailyintwoequalmealsat08:30 and16:30.Eweswereweighedatintervalsofaboutevery 2weeksandthequantityofdietadjustedforweightgain andforweightloss.Waterandmineralswerefreely avail-ablethroughoutthestudy.Allewesgavebirthtosingletons exceptfourewesinWFgroup.Theseeweswereexcluded fromthestudytoavoidlittersizeeffectsonplacental char-acteristics.

Birthweightandthesexoflambswererecordedwithin 12hafterlambing.Eachewewaslefttodelivertheplacenta naturally and placentas were collected from singleton

pregnanciesimmediatelyafterdelivery(approximately2h afterthebirthofthelamb);carewastakentoensurethat anyplacentalweightstakenwereofthetotalplacentawith anyfluidbeingremovedbeforeweighting.Thenumbers andweightsofcotyledonswerealsocounted,determined andrecorded.Placentalefficiency(definedasgramoflamb produced pergramofplacenta)wascalculatedforeach ewe.Thecotyledondensitywascalculatedasthenumber ofcotyledonsingramplacentalweight.

Theeffectofmaternalnutritionduringmid-gestation onlambbirthweight,placentalcharacteristicsandother variables wereinvestigated usingacompletely random-izeddesignbyusingGLMprocedureofMinitab(Minitab, 1998).Thesexoflambswasusedasacofactorinthemodel toadjustthebirthweightandtheplacental characteris-tics. Relationshipsbetween theplacental characteristics weredeterminedwithaPearsoncorrelationanalysisatthe 95%confidenceinterval.TheFisherztransformationtest wasappliedtoassess thesignificance ofthedifferences between correlation coefficients of two groups. Signifi-cantdifferencesbetweenmeansweretestedusingTukey’s multiplecomparisontestsandresultswerecomputedas mean±SEM.

3. Results

The changes in maternal body weights (BW) from mating to birth in experimental ewes in WF and UF groupsarepresented inFig.1.Alleweshad similarBW (47.8±0.7kg) at mating and there were no significant differences between ewes in WF (48.5±0.9kg) and UF (48.2±0.7kg)groupsatday30ofgestation.Thepatternof weightgain/losswas,however,different(P<0.05)between thetwogroups.EwesinUFgrouplostweightprogressively fromday30untilday80(P<0.05)ofgestation.Fromday 80ofgestation,followinginitiationoffeedingof100%of thedailyrequirements,ewesgainedweightsuchthatat theendofgestationtheBWwasnotdifferentfromthatof ewesinWFgroup(WF;49.4±0.9kg,UF;48.9±0.7kg).

Thechangesinlointhicknessandfatthicknessvalues oftheloineyemusclefrommatingtobirthinWFandUF

Changes in body weight (kg)

-6 -4 -2 0 2 4 6 8 10 WF UF

*

*

*

Fig.1.Thechangesinmaternalbodyweightsfrommatingtoday30,

45,60,80ofgestationandbirthinewesinWFandUFgroups.Asterisks

indicatedifferencesbetweentreatmentgroups(P<0.05).UF=under-fed

group,WF=well-fedgroup.

Changes in loin thickness (mm)

-3 -2 -1 0 1 _WF UF

*

Fig.2.Thechangesinloineyethicknessvaluesfrommatingtoday30,80

ofgestationandbirthinewesinWFandUFgroups.Asteriskindicates

differencesbetweentreatmentgroups(P<0.05).UF=under-fedgroup,

WF=well-fedgroup.

ewesarepresentedinFigs.2and3,respectively.Allewes hadsimilarloineye(20.9±1.0mm)andfat(4.7±0.5mm) thicknessvalues atmating. Also, there wereno signifi-cantdifferences in loin eye and fat thickness values of eye muscle between WF (loin thickness; 21.0_±1.1mm and fatthickness; 4.7±0.5mm)and UF(lointhickness; 20.9±1.0mmandfatthickness;4.5±0.7mm)ewesatday 30ofgestation.Therewasadecrease(P<0.05)inloineye andfatthicknessvaluesinUFewesatday80ofgestation, afterwhichtherewasnofurtherchangeuntilbirth.Loineye andfatthicknessvaluesweresimilarthroughoutgestation intheWFgroup.

Unadjustedand adjusted meansfor length of gesta-tion,lambbirthweightsand placentalcharacteristicsof ewesinWFandUFgroupsarepresentedinTable1.The sexoflambshadnoeffectonanyvariablesstudied.The lengthofgestationwasnotsignificantlydifferentbetween UFandWFewes.Therewas,however,adecreaseinthe birthweightofthelambsbornfromewesinUFgroup com-paredwiththelambsfromewesinWF(P<0.05).Number ofcotyledons,cotyledondensityandplacentalefficiency werenotsignificantlydifferentbetweenUFandWFewes. However,thereweredecreasesintheplacentaland aver-agecotyledonweightsinUFewescomparedtoWFewes (P<0.05).

Changes in fat thickness (mm)

-0,6 -0,3 0 0,3 WF UF

*

Fig.3.Thechangesinfatthicknessvaluesfrommatingtoday30,80

ofgestationandbirthinewesinWFandUFgroups.Asteriskindicates

differencesbetweentreatmentgroups(P<0.05).UF=under-fedgroup,

Table1

Unadjustedandadjustedmeans,accordingtolambsex,forlengthofgestation,lambbirthweightsandsomeplacentalcharacteristics(means±SEM)of

ewesinWFandUFgroups.

Traits Sub-group1 Sub-group2 Treatmentgroupsc

WF UF

Unadjusted mean

Adjustedmean Unadjusted

mean Adjusted mean F/M(n) 2/2 4/5 6/7 6/6 LG(day) 146.7±0.83 147.9±0.58 147.1±0.68 146.6±0.83 148.9±0.58 147.8±0.7 BW(kg) 4.28±0.039 4.21±0.013 4.24±0.027a _4.22±0.033a _3.74±0.119b _3.73±0.141b PW(g) 404.3±15.4 379.8±9.3 387.3±10.28a _387.8±11.94a _352.8±13.33b _348.7±15.54b TCN(n) 71.28±0.980 69.03±0.670 69.69±0.850 70.16±0.982 71.75±3.925 70.22±4.620 ACW(g) 1.92±0.497 1.90±0.312 1.91±0.381a _1.90±0.051a _1.57±0.136b _1.62±0.176b PE 11.13±0.947 11.51±0.803 11.35±0.859 11.27±0.295 10.75±1.481 10.84±0.455 CD 0.188±0.042 0.187±0.035 0.187±0.038 0.188±0.005 0.202±0.045 0.199±0.015

Meansinrowswithdifferentletters(a,b)aredifferentatP<0.05.

SEM=standarderrorofmean,F=female,M=maleLG=lengthofgestation,BW=lambbirthweight,PW=placentalweight,TCN=totalcotyledonnumber

perplacenta,ACW=averagecotyledonweight,PE=placentalefficiency,CD=cotyledondensity.

c _{TheewesinWF(well-fed)groupwerecomposedoftwosub-groups;ewesofferedwithadiettobefedeitheradlibitum(sub-group1;n=4;consumed}

175%oftheirdailyrequirement)or100%oftheirdailyrequirements(sub-group2;n=9)fromday30today80ofgestation.TheewesinUFgroup(under-fed;

n=12)werefedwithadiettomeet50%oftheirdailyrequirementsfromday30today80ofgestation.

Table2

Pearsoncorrelationcoefficients(95%confidenceintervals)ofplacentalcharacteristicsandlambbirthweightofewesinWFgroups.

Traits PW PE CD ACW BW CN 0.053(−0.609,0.715) −0.053(−0.715,0.609) 0.286(−0.349,0.921) −0.323(−0.951,0.305) −0.059(−0.721,0.603) PW −0.868**_{(−1.197,0.538) −0.889}**_{(−1.192,−0.585) 0.695}**_{(0.217,1.172) 0.469}*_{(−0.117,1.055)} PE 0.853**_{(0.506,1.199) −0.459(−1.048,0.130) −0.077(−0.738,0.584)} CD −0.799**_{(−1.198,−0.399) −0.470(−1.055,0.115)} ACW 0.742**_{(0.297,1.186)}

BW=lambbirthweight;PW=placentalweight;PE=placentalefficiency;CN=cotyledonnumber;CD=cotyledondensity;ACW=averagecotyledonweight.

* _P<0.05.

** _P<0.01.

Table3

Pearsoncorrelationcoefficients(95%confidenceintervals)ofplacentalcharacteristicsandlambbirthweightofewesinUFgroups.

Traits PW PE CD ACW BW CN 0.032(−0.672,0.736) −0.076(−0.778,0.626) 0.759**_{(0.300,1.217) −0.539}*_{(−1.132,0.054) 0.019(−0.685,0.723)} PW −0.797**_{(−1.222,−0.371) −0.619}*_{(−1.172,−0.065) 0.287(−0.387,0.961) 0.021(−0.683,0.725)} PE 0.445(−0.185,1.075) 0.004(−0.700,0.708) 0.565*_{(−0.016,1.146)} CD −0.645*_{(−1.183,−0.106) −0.034(−0.738,0.670)} ACW 0.435(−0.199,1.069)

BW=lambbirthweight;PW=placentalweight;PE=placentalefficiency;CN=cotyledonnumber;CD=cotyledondensity;ACW=averagecotyledonweight.

* _P<0.05.

** _P<0.01.

Pearsoncorrelationcoefficientsofplacental traitsfor ewesinWFandUFgroupsarepresentedinTables2and3, respectively.Inbothgroupstherewerenegative correla-tionsbetweenplacentalweight and placentalefficiency (r=−.868; and r=−.797; P<0.01), placental weight and cotyledon density (r=−.889; P<0.01 and r=−.619; P<0.05), and cotyledon density and average cotyle-don weight (r=−.799; P<0.01 and r=−.645; P<0.05) for ewes WF and UF groups, respectively. There were positive correlations between placental weight and lamb birth weight (r=.469; P<0.05), placental weight and average cotyledon weight (r=.695; P<0.01), aver-age cotyledon weight and lamb birth weight (r=.742; P<0.01) and placental efficiency and cotyledon den-sity (r=.853; P<0.01) for ewes in WF group. As can be expected there were positive correlations between cotyledon number and cotyledon density (r=.759;

P<0.01) and negative correlations between average cotyledon weight and cotyledon number (r=−.539; P<0.05) for ewes in UF group. There were positive correlationsbetweenplacentalefficiencyandlambbirth weight(r=.565;P<0.05)intheUFgroup.Therewereno significantcorrelationcoefficientsforvariablesintheUF andWFgroups.

4. Discussion

Thepresentstudydemonstratesthatamountof nutri-tionduringmid-gestation(from30to80days)influences placental weight, average cotyledon weight and birth weightinsingletonbearingewes.Additionally undernour-ishedeweshada lesserbody weight,loineyethickness andfatthicknessvaluethanwell-fedewesbyday80of gestation,reflectingthenutritionaltreatments.

The placentais theorganthrough whichrespiratory gases,nutrients,andwastes areexchangedbetweenthe maternal and fetal systems (Wu et al., 2006).The pla-centaalsoistheprimarycontributortotheintrauterine environment for growthand developmentof the fetus. Although the fetal genome plays an important role in growthpotentialinutero,thereisevidencesuggestingthat theintrauterineenvironmentisanimportantdeterminant offetalgrowth(Wuetal.,2006;Igwebuike,2010).Placental andtheumbilicalcordsizearecloselyrelatedtofetal devel-opmentandgrowthrate(GodfreyandBarker,2000;Wu etal.,2006;Ocaketal.,2009).Maternalnutrition,however, mayimpactplacentaldevelopment,growthandvascular beddevelopment(angiogenesis),therebyaffecting utero-placentalbloodflowandnutrientuptakebythefetus,all ofwhichmayplayanimportantroleinfetalgrowthand metabolism,aswellasbirthweight(Redmeretal.,2004). Experiments in sheepshowedthat amountof maternal nutritioninearlyandmidgestationcanexertmajoreffects onthegrowth,developmentandweightoftheplacenta andtherebyalterfetaldevelopment(Clarkeetal.,1998; Osgerbyetal.,2002;Faheyetal.,2005;McMullenetal., 2005)assupportedbytheresultsofthepresentstudy.

Although there are differences between treatment groups in terms of birth weight, placental weight and averagecotyledonweight,itisinterestingthatplacental efficiency andcotyledon densitydidnot differbetween ewes inUF andWF groups.Thismay beduetosimilar directionalchangesinbirthandplacentalweightsinboth groups.Infact,therewereapproximately9%decreasesin placental and 12%in birth weight.Theresultsobtained from the present study show that amount of maternal nutritionbetweenday30 andday80 ofgestation influ-encedplacental andaveragecotyledonweights,but not totalcotyledonnumberperplacenta.Theseobservations arein agreementwiththeviewthatmaternal nutrition during gestation can affect placental development and thusreduceplacentalweightanddecreaseplacentalsize (Clarkeetal., 1998;Osgerbyetal.,2002; Redmeretal., 2004; Wu et al.,2006).Additionally, suchan alteration in placentaldevelopmentmayhavedramatic functional consequences in fetal development.The reason for the reducedlambbirthweightinundernourishedewesmight beinadequateplacentalgrowthanddevelopment.Lambs fromundernourishedewesduringmid-gestationmayhave pooreradultperformance duetothegenomic program-mingeffectsofnutritionduringgestation(Redmeretal., 2004;Wuetal.,2006).Indeedit hasbeenreportedthat thelambsfromtheUFgrouphadalesserweaningweight, alteredcarcasscompositionandmusclefibertypes follow-ingfattening(Kuranetal.,2007,2008).

Ocak et al. (2009) reported that placental weight waspositivelycorrelatedwithaveragecotyledonweight, cotyledonnumberandcotyledondensityinsheep.Konyali etal.(2007)reportedsimilarfindingsforgoats.The cor-relationsobservedinthepresentstudybetweenplacental characteristicsinthewell-fedgroupsupportstheviewthat theinfluenceof maternalnutritiononplacental charac-teristics resultsinaltered birthweight.It wasobserved thatincreasedplacentalweightasa resultofamountof nutritioncausesanincreaseinaveragecotyledonandlamb

birthweight.Therewasalsoapositivecorrelationbetween averagecotyledonandlambbirthweightinwell-fedewes. The negative correlationbetween placental weight and efficiencyobservedinthepresentstudysupportsthe find-ingsofOcakandOnder(2011)forgoats.

ItisinterestingthattheewesintheUFgroupshowed compensatorygrowthfromday80tobirth,andthe nutri-tionalinfluenceonliveweight,loineyethicknessandfat thicknesswasnotevidentbetweencontrolandtreatment groupsbythetimeofbirth.Howeverdifferencesin placen-talweightsbetweenewesinUFandWFgroupsremained atbirthrepresentinglongtermeffectswhendietsdonot meet nutritionalrecommendations onplacental growth anddevelopment.Feedingdietsthatdo notmeet nutri-tional recommendations during mid-gestation caused a decreaseinbodyweight,loineyethicknessandfat thick-nessinthepresentstudy.Thisresultindicatesthatbody reservesinpregnantewesdependonamountofnutritional intake.Osgerbyetal.(2002)reportedthatundernourished ewes(onthe70%diet)duringdifferentperiodsofgestation (45,90,135dayofgestation)hadlesserbodyweightsand bodyconditionscorescomparedtothewell-fedewes(on the100%diet).

5. Conclusions

Theresultsof present studyshowedthat amountof maternalnutritionduringmid-gestationimpacts placen-talgrowthanddevelopmentofsingletonbearingewesas indicatedbyplacentalandaveragecotyledonweight caus-ingalteredfetaldevelopmentandhenceresultinginlesser lambbirthweightswhichmayaffectadultperformanceof lambs.Thesefindingsmaybeimportanttodevelopnovel nutritionalstrategies duringcriticalperiodsof gestation whichmayyieldpreferableadultperformanceandmeat quality.

Acknowledgement

The authors acknowledge the financial support by TUBITAK(TBAG-U/148)tocarryoutthisstudy.

References

Clarke,L.,Heasman,L.,Juniper,D.T.,Symonds,M.E.,1998.Maternal

nutri-tioninearly-midgestationandplacentalsizeinsheep.Br.J.Nutr.79,

359–364.

Fahey,A.J.,Brameld,J.M.,Parr,T.,Buttery,P.J.,2005.Theeffectof

mater-nalundernutritionbeforemuscledifferentiationonthemusclefiber

developmentofthenewbornlamb.J.Anim.Sci.83,2564–2571.

Godfrey,K.M.,Barker,D.J.P.,2000.Fetalnutritionandadultdisease.Am.

J.Clin.Nutr.71,1344–1352.

Greenwood,P.L.,Slepetis,R.M.,Bell,A.V.,2000.Influencesonfetaland

placentalweightsduringmidtolategestationinprolificeweswell

nourishedthroughoutpregnancy.Reprod.Fertil.Dev.12,149–156.

Hernandez,C.E.,Harding,J.E.,Oliver,M.H.,Bloomfield,F.H.,Held,S.D.E.,

Matthews,L.R.,2009.Effectsoflittersize,sexandpericonceptional

ewenutritiononsidepreferenceandcognitiveflexibilityinthe

off-spring.Behav.BrainRes.204,82–87.

Igwebuike,U.M.,2010.Impactofmaternalnutritiononovine

foetoplacen-taldevelopment:areviewoftheroleofinsulin-likegrowthfactors.

Anim.Reprod.Sci.121,189–196.

Konyali,A.,Tolu,C.,Das,G.,Savas,T.,2007.Factorsaffectingplacental

traitsandrelationshipsofplacentaltraitswithneonatalbehaviourin

Kuran,M.,Sen,U.,Sirin,E.,Aksoy,Y.,2008.Levelofmaternalnutrition

betweenday30andday80ofpregnancyaffectspostnatalmuscular

developmentofoffspringonday150.In:BookofAbstractsof59th

AnnualMeetingofEAAP14,p.155.

Kuran,M.,Sen,U.,Sirin,E.,Aksoy,Y.,Kilinc,K.,Ulutas,Z.,2007.Maternal

nutritionfromday30today80ofpregnancyinsingletonbearing

ewesincreasesthelambbirthweight.In:BookofAbstractsof58th

AnnualMeetingofEAAP13,p.210.

McMullen,S.,Osgerby,J.C.,Milne,J.S.,Wallace,J.M.,Wathes,D.C.,2005.

Theeffectsofacutenutrientrestrictioninthemid-gestationaleweon

maternalandfetalnutrientstatus,theexpressionofplacentalgrowth

factorsandfetalgrowth.Placenta26,25–33.

Mellor, D.J., Stafford, K.J., 2004. Animal welfare implications of

neonatal mortality and morbidity in farm animals. Vet. J. 168,

118–133.

MinitabforWindows(version12.11)[ComputerProgram],1998.

Avail-ableDistributor:MinitabInc.3081EnterpriseDriveStateCollege,PA

16801-3008,U.S.A.

Ocak,S.,Emsen,E.,Koycegiz,F.,Kutluca,M.,Onder,H.,2009.Comparison

ofplacentaltraitsandtheirrelationtolittersizeandparityweightin

sheep.J.Anim.Sci.87,3196–3201.

Ocak,S.,Onder,H.,2011.Placentaltraitsandmaternalintrinsic

fac-torsaffectedbyparityandbreedingoats.Anim.Reprod.Sci.128,

45–51.

Osgerby,J.C.,Wathes,D.C.,Howard,D.,Gadd,T.S.,2002.Theeffectof

maternalundernutritiononovinefetalgrowth.J.Endocrinol.173,

131–141.

Quigley, S.P., Kleeman,D.O., Kakar, M.A.,Owens,J.A., Nattrass, G.S.,

Maddocks,S.,Walker,S.K.,2005.Myogenesisinsheepis altered

bymaternalfeedintakeduringtheperi-conceptionperiod.Anim.

Reprod.Sci.87,241–251.

Quigley,S.P.,Kleemann,D.O.,Walker,S.K.,Speck,P.A.,Rudiger,S.R.,

Nat-trass,G.S.,DeBlasio,M.J.,Owens,J.A.,2008.Effectofvariablelong-term

maternalfeedallowanceonthedevelopmentoftheovineplacenta

andfetus.Placenta29,539–548.

Redmer,D.A.,Wallace,D.,Reynolds,L.P.,2004.Effectofnutrientintake

duringgestationonfetalandplacentalgrowthandvascular

develop-ment.Domest.Anim.Endocrinol.27,199–217.

Robinson,J.S.,Hartwich,K.M.,Walker,S.K.,Erwich,J.J.H.M.,Owens,J.A.,

1997.Earlyinfluencesonembryonicandplacentalgrowth.Acta

Pae-diatr.423,159–163.

Sammin,D.,Markey,B.,Bassett,H.,Buxton,D.,2009.Theovineplacenta

andplacentitis.Vet.Microbiol.135,90–97.

Wu,G.,Bazer,F.W.,Cudd,T.A.,Meininger,C.J.,Spencer,T.E.,2004.Maternal

nutritionandfetaldevelopment.J.Nutr.134,2169–2172.

Wu,G.,Bazer,F.W.,Wallace,J.M.,Spencer,T.E.,2006.Intrauterinegrowth

retardation:implicationsfortheanimalsciences.J.Anim.Sci.84,