Association Between Anaemia And Low Birth Weight Among HIV -Infected Pregnant Women Aged 15 – 49 Years In Zimbabwe : A Cross-Sectional Study

Abstract

Background
In Zimbabwe, almost 25% of infants are born with low birth weight (LBW). LBW accounts for over half of the neonatal deaths in the country. Anaemia during pregnancy has been inconsistently associated with an increased risk of LBW. However, very little data is available from countries where HIV prevalence is high, wherein HIV is also known to be a common risk factor to LBW. This study examined the relationship between maternal anaemia and LBW among HIV-infected pregnant women in Zimbabwe.
Methods
This was a secondary data analysis of the 2015 Zimbabwe Demography and Health Survey. Data for 809 HIV positive women aged 15-49 years and their infants from all live births preceding the survey by 5 years were included in the study. Modified-Poisson regression methods were used to determine the association between anaemia and LBW while adjusting for other risk factors.
Results
The prevalence of maternal anaemia and LBW among the HIV-infected pregnant women was 42.3% (n=342) and 16.3% (n =132) respectively. The prevalence of LBW was14.6% (n=50) and 17.6% (n=82) among anaemic and non-anaemic HIV positive women respectively (p=0.264). HIV infected pregnant women with anaemia had a 25% less chance of giving birth to infants with LBW compared to HIV infected mothers without anaemia, however, the association was not statistically significant (RR 0.75; 95% CI 0.53- 1.05).
Conclusions
The findings demonstrate a high prevalence of anaemia and LBW among HIV infected pregnant women. Nonetheless, maternal anaemia was not associated with LBW. There is a need for adapted monitoring of HIV-positive pregnant women and affordable improved nutrition during antenatal care to reduce the risk of LBW infants and maternal anaemia levels. Further research examining the relationship between maternal anaemia and LBW among HIV positive pregnant women whilst factoring in the role of ART and the severity of anaemia is required.

Full text

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Preprint:Pleasenotethatthisarticlehasnotcompletedpeerreview.
AssociationBetweenAnaemiaAndLowBirthWeight
AmongHIV-InfectedPregnantWomenAged15–49
YearsInZimbabwe:ACross-SectionalStudy
CURRENTSTATUS:POSTED
DorothyTChisare
UniversityoftheWitwatersrandSchoolofPublicHealth
dorothyct9@gmail.comCorrespondingAuthor
ORCiD:https://orcid.org/0000-0001-8194-7674
SimbarasheTakuva
UniversityoftheWitwatersrandFacultyofHealthSciences
TariroJ.Basera
MedecinsSansFrontieres
NatashaKhamisa
IIEMSA
JacquelineWitthuhn
IIEMSA
DOI:
10.21203/rs.2.24714/v1
SUBJECTAREAS
Sexual&ReproductiveMedicine
KEYWORDS
Lowbirthweight,anaemia,HIVinfectedpregnantwomen,Zimbabwe

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Abstract
Background
InZimbabwe,almost25%ofinfantsarebornwithlowbirthweight(LBW).LBWaccountsforoverhalf
oftheneonataldeathsinthecountry.Anaemiaduringpregnancyhasbeeninconsistentlyassociated
withanincreasedriskofLBW.However,verylittledataisavailablefromcountrieswhereHIV
prevalenceishigh,whereinHIVisalsoknowntobeacommonriskfactortoLBW.Thisstudy
examinedtherelationshipbetweenmaternalanaemiaandLBWamongHIV-infectedpregnantwomen
inZimbabwe.
Methods
Thiswasasecondarydataanalysisofthe2015ZimbabweDemographyandHealthSurvey.Datafor
809HIVpositivewomenaged15-49yearsandtheirinfantsfromalllivebirthsprecedingthesurvey
by5yearswereincludedinthestudy.Modified-Poissonregressionmethodswereusedtodetermine
theassociationbetweenanaemiaandLBWwhileadjustingforotherriskfactors.
Results
TheprevalenceofmaternalanaemiaandLBWamongtheHIV-infectedpregnantwomenwas42.3%
(n=342)and16.3%(n=132)respectively.TheprevalenceofLBWwas14.6%(n=50)and17.6%
(n=82)amonganaemicandnon-anaemicHIVpositivewomenrespectively(p=0.264).HIVinfected
pregnantwomenwithanaemiahada25%lesschanceofgivingbirthtoinfantswithLBWcomparedto
HIVinfectedmotherswithoutanaemia,however,theassociationwasnotstatisticallysignificant(RR
0.75;95%CI0.53-1.05).
Conclusions
ThefindingsdemonstrateahighprevalenceofanaemiaandLBWamongHIVinfectedpregnant
women.Nonetheless,maternalanaemiawasnotassociatedwithLBW.Thereisaneedforadapted
monitoringofHIV-positivepregnantwomenandaffordableimprovednutritionduringantenatalcare
toreducetheriskofLBWinfantsandmaternalanaemialevels.Furtherresearchexaminingthe
relationshipbetweenmaternalanaemiaandLBWamongHIVpositivepregnantwomenwhilst
factoringintheroleofARTandtheseverityofanaemiaisrequired.

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Background
Birthweightisasignificantindicatoroftheimmediateandfuturehealthstatusofanewbornand
predictsthechild’schancesofsurvival[1].AsdefinedbytheWorldHealthOrganization(WHO),
infantswithabirthweightlessthan2500grams(2.5kilograms)areknownaslowbirthweight(LBW)
infantsregardlessofgestationalage[2].Globally,morethan20millioninfants,accountingfor15.5%
ofallbirthsarebornwithaLBW[3],themostprevalentregionsbeingSouthAsia(30%),followedby
Sub-SaharanAfrica(SSA)(18%)andSouthAmerica(17.9%)[4,5].LBWisaleadingunderlyingfactor
ofneonatalmortality,accountingfor38%ofallinfantdeathsin2000,45%in2015and60–80%
(30milliondeaths)in2017[4,6].Withaprevalenceof10–24%varyingbyregionandaccountingfor
overhalfofneonataldeathsinZimbabwein2015,LBWisaprudentmaternalandchildhealthissue
inthecountry[7,3].HeandcolleaguesindicatethatLBWinfantsare40timesmorelikelytodie
withinthefirst30daysoflifecomparedtonormalbirthweightbabies(NBW)[6].
Maternalanaemiaisasignificantglobalhealthissuethataffectsabout500millionwomenof
reproductiveage[8].AnaemiaduringpregnancyincreasestheriskofLBWandthisriskis
exacerbatedbyinadequateaccesstoprenatalcare,socio-economicstatusofthepregnantwoman,
andexposuretoinfectiousdiseasessuchassexuallytransmitteddiseases,malariaorHIVinfection
[5].StudieshaveshownthatinfantsborntoHIVpositivemothershavea9.87timeshigherriskof
LBWcomparedtoHIVunexposedinfants[6],andthosethatsurvivebecomeillwithinthefirstsix
daysoflife[9].Moreover,highratesofanaemia,ariskfactortoLBWhavebeenreportedamongHIV
positivepregnantwomenrangingfrom73%inSouthAfrica,40%inKenya,56.4%inTanzaniaand
37.7%inZimbabwefrom2011to2013[10].LBWinfantsborntoanaemicmothershaveatwo-fold
likelihoodofneonatalmortalitythanthoseborntonon-anaemicwomen[11].Theconsequencesof
LBWonthehealthofinfantsincludecognitiveandneurologicalimpairment,cholesterol,obstructive
lungdisease,renaldamage,impairedimmunefunctionandchronicconditionssuchashighblood
pressureanddiabetesintheiradulthoodyears[12].Athresholdof> 5.0%prevalenceofanaemiais
deemedapublichealthconcernwhilst > 40%prevalenceaseverehealthissueandcouldbefatalto
bothwomanandchildorcausecomplicationssuchasLBW[2].Studieshavereportedhighprevalence

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ofLBWamonganaemicpregnantwomenrangingfrom30%inTanzania[11]to53.6%inZimbabwe
[3].
ThereisadearthinliteraturetohighlighttheassociationbetweenanaemiaandLBWinthecontextof
HIVorthemechanismsthroughwhichbothdiseasessimultaneouslycontributetoLBWinZimbabwe.
SuchadearthinknowledgeaffectsthemethodsoftheZimbabweanhealthcaredeliverysystemon
optimallyrespondingtotheneedsofHIVexposedinfants[9].Giventhehighprevalenceandpublic
healthimportanceofHIVinfection,anaemiainpregnancyandLBWasamajorriskfactorforinfant
mortalityinZimbabwe,thisstudyassessedwhethermaternalanaemiawasassociatedwithLBWin
thecontextofHIVinfection.IdentifyingtheassociationofbothconditionsonLBWiscrucialin
improvingthedevelopmentaloutcomesofHIVexposedinfantswhoareatincreasedriskofLBW
comparedtonon-exposedinfants[13]andsupportthedevelopmentofeffectivestrategiestargeting
LBWwithinneonatalhealthprogramsinZimbabwe.Theobjectiveofthisstudywastodeterminethe
prevalenceofLBWanditsassociationwithmaternalanaemiaamongHIVinfectedpregnantwomen
aged15to49yearsinZimbabwe.
MaterialsAndMethods
StudyDesign
Theprimarystudy,the2015ZimbabweDemographicandHealthSurvey2015(ZDHS)wasacross
sectionalsurveywheredataontheoutcome(LBW)andotherexplanatoryvariablessuchasanaemia
wascollectedatasinglepointintimehencethisstudyusedacross-sectionaldesigntoanalysethe
secondarydata.
StudySetting,Population,AndSampling
ZimbabweisinthesouthernregionofAfricaandisborderedbyfourcountriesnamelyBotswana,
Zambia,SouthAfrica,Mozambiquetothenortheast[14].BasedonZimstat(2016)estimates,
Zimbabwehasapopulationofapproximately14.5millionpeople,andtheaveragelifeexpectancyis
58years.Between1990and2015,theinfantmortalityrateaveraged50deathsper1000livebirths
[14];andtheunder-fivemortalitywas76deathsper1000livebirths[14].
TheZDHSisanational-levelhousehold-basedsurveyundertakeninallofZimbabwe’stenprovinces,

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withthelastsurveyconductedin2015.Nosamplingwasdoneinthisstudyasitinvolvedasecondary
analysisofsurveydata,thereforeallHIVpositivewomenwhoreportedonthebirthweightoftheir
infant,withananaemiatestresultmeetingtheinclusioncriteria,constitutedtheanalysissample.In
total,809HIVpositivewomenaged15–49yearsmettheinclusioncriteria.Nonetheless,atestwas
performedtoassesstheadequacyofthesampleforthisstudyusingthefollowingpowertest
calculation:
whereNistheestimatedminimumsamplesize,PistheexpectedproportionofLBW(15%),zαisthe
confidencelevelof95%(standardvalueis1.96)andEisthemarginoferror(+-5%)therefore;
Therefore,thesamplesizeof809isadequatetodetectanydifferenceswith5%marginoferror.
TheZDHSusedastratified,two-stageclustersamplingapproachfromJulytoDecember2015.The
firststageinvolvedselectingsamplesfromamastersamplingframeconstructedfromenumeration
(400enumerationareas(EAs)thatcomprised166EAsinurbanareasand234inruralareas)andthe
secondstageinvolvedsystematicsamplingofthehouseholdslistedfromeachclusterensuring
adequatenumbersofcompletedinterviews.Thosewholivedininstitutionalgroupssuchasarmy
barracks,clinicsorhospitals,policestations,andboardingschoolswereexcludedfromtheZDHS.
TrainedpersonnelwithintheZDHSinterviewedafinalsampleof9955womenaged15–49yearswho
wereeitherpermanentresidentsorovernightvisitorsoftheincludedhouseholdsfollowingtheir
consentusingcomputerassistedpersonalinterviewing(CAPI)inthethreelocallanguages.Ofthe

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9955women,therewere20791livebirthsrecordedandeachrespondent(mother)wasaskedto
provideadetailedbirthhistoryforbirthsintheprecedingfiveyearsbeforesurvey.The
questionnaireswereadaptedfrommodelsurveyinstrumentsdevelopedfortheDHSProgram.Birth
weightwasrecordedusingthemetricscale(ingrams)[14].HIVandanaemiatestingwasperformed
onthoseparticipantswhoconsentedtotesting[14].
VariableDefinitions
ThestudyoutcomeLBWwasadichotomousvariable,lowbirthweight=“Yes”if < 2500gor“No”if >
2500g.Anaemiawascategorizedasanaemia(≤ 12.0Hbg/dl)andnoanaemia(> 12.0Hbg/dl).
DataAnalysis
TheZDHSdatawasprovidedinSTATAfileformatanditwasimportedtoSTATAversion13(Stata
Corp,CollegeStation,Texas,USA).Datacleaningprocesses,codingandanalysiswasdoneinSTATA
version13(StataCorp,CollegeStation,Texas,USA).Missingvaluesandduplicatesweredropped.
Thedistributionthesocio-demographic,socio-economicandobstetriccharacteristicsofthestudy
participantsaswellastheprevalenceofLBWareexpressedasfrequencieswiththeircorresponding
percentages.Inaddition,themeanandstandarddeviationofLowbirthweightispresentedasitwas
normallydistributed.ThePearsonChi-squaretestwasusedtotestdifferencesbetweenexplanatory
variablesandLBW.
MultivariablePoissonregressionmodelswithrobusterrorvariancewereusedadjustingforclustering
toexaminetheassociationbetweenanaemiaandlowbirthweightadjustingforotherconfounding
variables.LBWhadacommonprevalence(≥ 10%)[15]hencethemodifiedPoissonregression
approachwasusedtoexplorepredictorsoflowbirthweightwith;maternalanaemia,maternalage,
maternaleducationstatus,maternalemployment,wealthquintile,residencetypeLBW,maternalBMI,
ironandfolatesupplementintakeandnumberofANCvisitsinourstudyparticipants.Poisson
regressionavoidsthebiasofoverestimatingtheprevalenceoftheoutcomeinquestion,hence
presentingmorerobustfindingscomparedtousinglogisticregression[15].Crudeandadjusted
relativerisks(RR)withcorresponding95%confidenceintervals(CI)arereported.Variablesthatwere
apriori,hadap-value < 0.20onbivariateanalysiswereconsideredaspotentialcandidatesfor

7
inclusionintothemultivariablemodels.Allp-values < 0.05wereconsideredstatisticallysignificant.
Results
Figure1illustratesselectionprocessofparticipantsalsohighlightingreasonsfortheexcludedparticipants.
Thesocio-demographic,socio-economicandobstetricfactorsareillustratedinTable1.Overall,809HIV-positive
womenwereincludedinthestudy.AsillustratedinTable1,mostoftheHIV-positivewomenwerebetweenthe
agesof25–34years(53.8%,n = 435)followedbythe35yearandaboveagegroup(25.3%,n = 205)andlastly
20.9%were15–24years(n = 169).Amongwomenwithanaemia,mostofthemwere25–34yearsofage(54.1%,
n = 185)while26.6%(n = 91)wereaged35yearsandabove.Mostofthemarriedwomendidnothaveanaemia
(77.3%,n = 361).About53.8%offemalechildren(n = 435)and46.2%malechildren(n = 374)werebornto
anaemicwomen.Themean(standarddeviation[SD])birthweightoflivebirthswas3124.8grams(± 622.9).
Infantsborntoanaemicmotherswereonaverage73.8gramsheavierthanthoseborntonon-anaemicmothers.
Whenthebirthweightwasdichotomized,theprevalenceofLBWamonginfantsborntoanaemicwomenwas
lower(14.6%,n = 50)thantheircounterparts(17.6%,n = 82),nonethelessthedifferenceswerenotstatistically
significant(p = 0.264).
Approximatelyhalfoftheinfantsweresecondorthirdbornchildrenwithnomajordifferencesbetweenanaemic
women(50.3%,n = 172)andnon-anaemicwomen(49.5%,n = 231).Overall,99.3%(806)ofmothersreceivedat
leastprimaryeducation,ofwhichmostofthemotherswithanaemia(67%,n = 229,67%)andwithoutanaemia
(68.3%,n = 319),hadtertiaryeducation.Sixtypercentofwomeninthestudywereemployed(n = 485),witha
lowerpercentageofemployedmothersamongstthosewithanaemia(56.4%).Mostwomenresidedinrural
communities(60%,n = 485)withmarginaldifferencesbetweenwomenwhohadanaemiaandthosewithout
anaemia(60.5%and59.5%respectively).Approximately,athirdoftheparticipantswerefromahouseholdinthe
fourthwealthquintile(31.8%,n = 257).Approximately,88.3%(n = 576)ofthestudyparticipantstookiron
supplementsduringtheirlastpregnancyandahigherpercentageofthesewomenwereanaemic(90.8%,n =
247).Fewerwomentookfolatesupplementsduringtheirlastpregnancy(50.6%,n = 330)andthiswassimilar
amonganaemicwomenandnon-anaemicwomen(50.4%and50.8%respectively).MostwomenhadnormalBMI
(63.1%,n = 510),mostofwhomwerenon-anaemic(64.2%,n = 299).Approximatelyhalf(51.4%,n = 335)ofthe

8
studyparticipantshadtherecommended5ormoreANCvisitsduringpregnancyandtherewerenodifferencesin
ANCattendancebetweennon-anaemic(50.5%,n = 192)andanaemicwomen(52.6%,n = 143)(Table1).
Table1
Socio-demographic,socio-economicandobstetriccharacteristicsofthestudyparticipants
Variables Total Anaemia Noanaemia
N(%) Mean(STD) Mean(STD)
LowBirthWeight(g) 3124.8(622.9) 3166.3(648.3) 3049.5(602.6)
Total
N(%)
Anaemia
n(%)
Noanaemia
n(%)
LowBirthWeight(g)
Yes(≤ 2500g)
No(above2500g)
132(16.3)
677(83.7) 50(14.6)
292(85.4) 82(17.6)
385(82.4)
MaternalAge
15–24
25–34
≥ 35
169(20.9)
435(53.8)
205(25.3)
66(19.3)
185(54.1)
91(26.6)
103(22.1)
250(53.5)
114(24.4)
SexofChild
Male
Female
374(46.2)
435(53.8) 156(45.6)
186(54.4) 218(46.7)
249(53.3)
Parity
1stChild
2–3
≥ 4
109(13.5)
403(49.8)
297(36.7)
50(14.6)
172(50.3)
120(35.1)
59(12.6)
231(49.5)
177(37.9)
Maritalstatus
Nevermarried
Married/livingtogether
Divorced/separated/widowe
d
54(6.7)
592(73.2)
163(20.2)
33(9.7)
231(67.5)
78(22.8)
21(4.5)
361(77.3)
85(18.2)
MaternalEducationstatus
None
Primary
Secondary
Tertiary
6(0.7)
98(12.1)
157(19.4)
548(67.7)
6(1.8)
45(13.2)
62(18.1)
229(67.0)
0(0.0)
53(11.4)
95(20.3)
319(68.3)
MaternalEmployment
Employed
Non-employed
485(60.0)
324(40.1) 193(56.4)
149(43.6) 292(62.5)
175(37.5)
WealthQuintile
Lowest
Second
Middle
Fourth
Highest
162(20.0)
121(15.0)
141(17.4)
257(31.8)
128(15.8)
71(20.8)
49(14.3)
59(17.3)
107(31.3)
56(16.4)
91(19.5)
72(15.4)
82(17.6)
150(32.1)
72(15.4)
ResidenceType
Urban
Rural
324(40.1)
485(60.0) 135(39.5)
207(60.5) 189(40.5)
278(59.5)
MaternalBMI
Low(BMI < 18.5)
Normal(BMI18.5–24.9)
Overweight/obese(BMI ≥
25)
65(8.1)
510(63.1)
233(28.8)
37(10.8)
211(61.7)
94(27.5)
28(6.0)
299(64.2)
139(29.8)
TookIronSupplements
Yes
No
576(88.3)
76(11.7) 247(90.8)
25(9.2) 329(86.6)
51(13.4)
TookFolateSupplements
Yes
No
330(50.6)
322(49.4) 137(50.4)
135(49.6) 193(50.8)
187(49.2)
No.ofANCvisits
Inadequate(< 5)
Adequate(≥ 5)
317(48.6)
335(51.4) 129(47.4)
143(52.6) 188(49.5)
192(50.5)
PrevalenceofmaternalanaemiaandLBWamongHIVpregnantwomeninZimbabwe,2015
AsillustratedinFig.4,theprevalenceofmaternalanaemiaamongHIVpositivepregnantwomeninZimbabwe
was42.3%whiletheoverallprevalenceoflowbirthweightinZimbabwein2015was16.3%(Fig.5).Thiswas

9
higherinwomenthathadnoanaemia(17.6%)comparedtothosewithanaemia(14.6%),nonethelessthe
differenceswerenotstatisticallysignificant(p = 0.264).
FactorsassociatedwithLBW
Inbivariateanalysis,LBWamongmotherswaspredictedbysexofchild,maritalstatus,wealthquintile,residence
typeandmaternalBMIstatus(p < 0.05).Intheadjusted(multivariable)model,maternalBMI,sexofchildand
parityweresignificantlyassociatedwithLBW.
TheriskofLBWdecreasedwithanincreaseinmaternalBMI;withlowerriskamongwomenwithhigherBMIi.e.
overweight/obese(RR0.41;95%CI0.22–0.74)andthosewhowereofanormalweight(RR0.71;95%CI0.45–
1.12)comparedtounderweightwomen.FemaleinfantshadahigherriskofLBWcomparedwithmaleinfants(RR
1.64;95%CI1.13–2.40).Additionally,theriskofLBWdecreasedwithincreasingparity,wherebythesecondor
thirdborninfanthavea38%lesslikelihoodofLBW,whilefourthorabovehad50%lessriskofLBW.Moreover,
theriskofLBWdecreasedwithfrequentANCvisits(17%lowerriskforthosewith5ormoreANCvisits)(RR0.78;
95%CI0.55–1.09).Maternalanaemia,maternaloccupation,wealthquintile,residencetype,maternaleducation,
ironsupplementintake,folatesupplementintakeandmaritalstatuswerenotstatisticallysignificantinthe
multivariablemodel.However,womenwithanaemiahada25%lesslikelihoodtogivebirthtobabieswithLBW
(RR0.75;95%CI0.53–1.05)comparedwithmotherswithoutanaemia.AlsothemoretheANCvisits,theless
likelihoodofLBWinfantsi.e.adequatevisits(> 5)(RR0.78;95%CI0.55–1.09).Thereisalsoadecreasedriskof
LBWamong25–34yearagedmothersandthose35andabove(22%and7%respectively)comparedtothoseof
theyoungeragegroup,15–24years.

10
Table2
RiskfactorsforLBWamongHIVinfectedpregnantwomeninZimbabwe,2015
Variables UnadjustedRR(95%
CI)
p-value AdjustedRR(95%CI) p-value
MaternalAnaemia(Hb,
g/dl)
Non-anemic(> 12.0)
Anemic(≤ 12.0)
Ref
0.83(0.59–1.18) 0.304 Ref
0.75(0.53–1.05) 0.097
MaternalAge
15–24
25–34
≥ 35
Ref
0.78(0.53–1.14)
0.93(0.59–1.46)
0.194
0.747 Ref
1.27(0.80–2.04)
1.87(0.96–3.65)
0.312
0.067
SexofChild
Male
Female
Ref
1.60(1.14–2.27) 0.007* Ref
1.64(1.13–2.40) 0.010*
Parity
1stChild
2–3
≥ 4
Ref
0.67(0.45–1.01)
0.66(0.43–1.02)
0.054
0.060 Ref
0.62(0.39–1.00)
0.50(0.26–0.95)
0.051
0.034*
Maritalstatus
Nevermarried
Married/livingtogether
Divorced/separated/wi
dowed
Ref
0.63(0.41− .97)
0.50(0.27–0.92)
0.035*
0.026*
Ref
0.80(0.47–1.35)
0.61(0.30–1.22)
0.399
0.160
MaternalEducation
status
None
Primary
Secondary
Tertiary
Ref
0.73(0.22–2.43)
0.50(0.15–1.67)
0.44(0.14–1.39)
0.614
0.259
0.160
Ref
0.49(0.16–1.92)
0.30(0.08–1.18)
0.30(0.08–1.05)
0.283
0.085
0.060
MaternalEmployment
Non-employed
Employed
Ref
0.91(0.66–1.27) 0.585 Ref
1.02(0.71–1.46) 0.927
WealthQuintile
Lowest
Second
Middle
Fourth
Highest
Ref
1.09(0.66–1.78)
0.93(0.55–1.58)
0.69(0.43–1.10)
0.51(0.28–0.93)
0.738
0.799
0.120
0.029*
Ref
1.54(0.90–2.63)
1.20(0.68–2.13)
0.83(0.38–1.79)
0.53(0.20–1.42)
0.120
0.531
0.602
0.202
ResidenceType
Urban
Rural
Ref
1.48(1.06–2.07) 0.022* Ref
0.73(0.36–1.48) 0.399
MaternalBMI
Low(BMI < 18.5)
Normal(BMI18.5–
24.9)
Overweight/obese
(BMI ≥ 25)
Ref
0.67(0.43–1.04)
0.43(0.25–0.73)
0.072
0.002* Ref
0.71(0.45–1.12)
0.41(0.22–0.74)
0.144
0.003*
TookIronSupplements
No
Yes
Ref
0.68(0.44–1.06) 0.088 Ref
0.73(0.46–1.15) 0.177
TookFolateSupplements
No
Yes
Ref
0.77(0.55–1.09) 0.141 Ref
0.79(0.55–1.13) 0.190
No.ofANCvisits
Inadequate(< 5)
Adequate(≥ 5)
Ref
0.78(0.55–1.09) 0.146 Ref
0.83(0.60–1.15) 0.265
Note:RRisrelativerisk;CIisconfidenceinterval;*significantatp < 0.05
Discussion
ThisstudyinvestigatedtheassociationbetweenmaternalanaemiaandLBWamongHIVinfectedpregnant
womenaged15–49yearsinZimbabwe.Theresultsdemonstratedthatmaternalanaemiawasnotassociatedwith
LBW.WomenwithanaemiahadlowerriskofLBWcomparedtonon-anaemicwomen.MaternalBMIstatus,sexof

11
childandparitywerefoundtobesignificantriskfactorsofLBWamonginfantsofHIVinfectedwomeninthe
multivariableanalysis.WomenwithnormalweightandthoseobeseoroverweighthadlowerriskofhavingLBW
infantscomparedtounderweightwomen(lowBMIof< 18.5).Itwasfoundthatfemaleinfantshadahigherriskof
LBWasopposedtomaleinfantsandthatasparityincreased,theriskofLBWdecreased.
Theprevalenceofanaemiainthiscross-sectionalstudywas42.3%amongstHIVinfectedwomen,whilethe
prevalenceofLBWamonganaemicwomenwas14.6%.Otherstudieshavereportedprevalenceofmaternal
anaemiaamongstHIVpositivewomenindevelopingcountriesrangingbetween14–62%[10,16,4].Theoverall
LBWprevalenceinZimbabweinthisstudypopulationofHIVpositiveinfectedwomenin2015was16.3%.The
LBWprevalencereportedinthisstudyishighercomparedto15%reportedfortheSSAregion,9%inMalawi[3],
andaprevalenceof9.5%amongthegeneralpopulationofwomenofreproductiveageinZimbabweasreported
inthe2010–2011DemographicandHealthSurveyreport[14].Theseresultsdemonstrateanincreasein
prevalencefrom2011to2015.TheincreaseinLBWprevalenceintheZimbabweansettingasexplainedby
Feresu,Harlow&Woelkispossiblyduetolimiteddataandalackofunderstandingofthepredictorsassociated
withLBW,especiallytheroleofHIVwhichstillneedstobecharacterizedinthecontextofLBWpatterns[3].This
increasingtrendisparticularlyconcerninggiventheimpactofLBWonthedevelopmentaloutcomesofthe
infants.LBWincreasestheriskoflearningdifficulties,cerebralpalsy,visualandauditorydeficitsamonginfants
[18].
ObstetricFactors
MaternalanaemiawasnotassociatedwithLBWinthisstudy.Similarly,KaderandPereraalsoreportedno
associationbetweenLBWandmaternalanaemia[18].Ameta-analysisofstudiesinvestigatingprevalence,risk
factorsandLBWamonganaemicwomenlivingwithHIValsoreportednoassociationbetweenmaternalanaemia
andLBW[4].Theyexplainedthataphysiologicaldecreaseinhaemoglobinlevelsduringlatepregnancymaybedue
tonormalredcellsandplasmavolumeexpansionsanddoesnotnecessarilyimplythatoneisanaemicwhichmay
explainthelackofassociation.Studieshavereportedconflictingfindings.Ontheotherhand,somestudieshave
foundthatpregnantwomenwithhighplasmavolumeshavegivenbirthtoinfantswithahigherbirthweightthan
average[4].Incontrast,Fowkesandcolleaguesreportedaninverseassociationbetweenbirthweightand
haemoglobinlevelsduringlatestagesofpregnancywherebybirthweightofinfantswassignificantlylargeramong

12
anaemicwomenincomparisonwithnon-anaemicwomen[19].Contrarytothesefindings,Kader&Pereraand
RahmatifoundanassociationbetweenanaemiaandLBW,howeveronlywithinthefirsttrimesterofthe
pregnancynotthesecondandthirdtrimesters,whileHaiderfoundanassociationonlyinthefirsttrimester[18,4,
21].Fromthisstandpoint,itisspeculatedthattheseverityofanaemiawithinthethreegestationperiodsof
pregnancyshouldbeconsidered.However,thisstudydidnotstratifyanaemiaintheanalysisbygestationperiod
(first,secondandthirdtrimester)duetothesmallproportionofwomenwithanaemiawithinthesamplewhich
wouldresultinextremelywideconfidenceintervalsandlowerprecisionofthefindings.
ThepresentstudyalsoconfirmedthefindingsabouttherelationshipbetweenmaternalBMIandLBWwhichwas
statisticallysignificant.Womenwithpoornutritionalstatus,reflectedinlowBMI(< 18.5)hadahigherriskofLBW
infantscomparedtowomenwithanormalweight(18.5–24.9)andthosewhowereoverweight/obese(≥ 25.0).
ThisisconsistentwithapreviousstudybyKaderandPererawhoreportedthatwomenwithlowBMI < 18.5had
49%riskofhavingLBWinfants[18].AhigherriskofLBWwasalsoreportedamongstwomenwithalowerBMI(<
18.5)inBangladesh[22].AplausiblereasonisthatlowBMI(underweight)isamarkerofmarginaltissuenutrient
reservesandapredictorofprotein-energymalnutritionleadingtofetalunder-nutrition,whichinturnaffects
foetalgrowth[5].Also,lowBMIamongHIVpositivewomenisinducedbyreduceddietaryintake,malabsorption
ofnutrientsandmetabolicalterationswithintheearlystagesofinfectionwhichaffectsthefoetus’development
[23].However,otherstudiesfoundahigherriskofLBWamongoverweightorobesewomen,althoughno
plausibleexplanationswereprovidedfortheirfindings[25].
Socio-demographicFactors
FemaleinfantshadahigherriskofLBWcomparedtomalesinourstudy.Overalltheseresultsaresimilarto
findingsreportedinotherstudiesindicatinghighriskofLBWamongfemaleinfantscomparedtotheirmale
counterparts[26,27].However,otherstudiesreportednostatisticallysignificantassociationbetweensexofchild
andLBW[24].Nevertheless,apopularexplanationfortheassociationisthatfemaleinfantsarebiologically
predisposedtohaveLBW[25].
Anotherkeyfindinginourstudywasthatasparityincreased(i.e.fourormorechildren),theriskofLBW
decreased.Thesefindingsaredirectlyinlinewithotherfindingsthathaveshownthatthemorechildrenthata
womanhas,thelowertheriskofLBWwitheachsuccessivebirth[25,27,9].Boghossian&Laughonhighlightthat

13
birthweightincreaseswithparity(upto4or5births)butdeclinesthereafter[27].Apossibleexplanationforthis
varyingrelationshipbetweenparityandbirthweightistheprimingofawoman’sbodybythefirstpregnancyin
whichthebodybecomesmoreefficientwitheachsubsequentpregnancy.Howeverasthewomanages,her
reproductivelifespandecreasesthereforethebodybecomeslessefficientandispronetogivingbirthtoalow
birthweightinfant[27].Nevertheless,inpriorcross-sectionalstudies,thesedifferencesbetweenbirthweightby
paritymaybeduetomethodologicalissuessuchasselectionbias[27].
ThefindingssuggestedthatLBWwasnotassociatedwithmaternalage,maternaleducationandmaternal
employment.Thesefindingsareinconsistentwithfindingsfromotherstudiesthatreportedthatlowbirthweightis
statisticallysignificantwithmaternalageaswellasmaternaleducationandemployment[29,2,18].
TheassociationbetweenLBWandwealthquintile,residencetype,ironandfolatesupplementintake,and
frequencyofantenatalcarevisitswereestablishedbyotherstudies.Thesefindingsareinconsistentwithfindings
fromthisstudy[29,18].
PriorstudiesindicatethatthereisanassociationbetweenmaritalstatusandLBW[30,31,32].Marriageis
reportedtobeanadvantageoussocialtieforthegrowthofthefoetusduringthewoman’spregnancyduetothe
supportrenderedtoherbyapartner[30].Thecurrentstudydoesnothowevershowastatisticallysignificant
relationshipbetweenmaritalstatusandLBW.Thiscouldbeexplainedbyselectionbiasinthedata;asexpected
mostpregnantwomenareofamarriedstatusinZimbabwe[3].
StudyImplications
Thefindingsofthisstudyhavepublichealthimplicationstranscending.AnassociationbetweenLBWandanaemic
womenwasnotconfirmedinthisstudy.However,theprevalenceofLBWishighamongthisvulnerable
populationofHIV-positivewomencomparedtothegeneralpopulationofpregnantwomen,warrantingmore
attentiontotheirnutritionalandhealthneedsgiventhehighriskespeciallyamongwomenwhowere
underweight.Moreover,considerationofHIVstatusasariskfactorforanaemiaandLBWneedstobeconsidered
whenprovidingthecontinuumofcaretowomenforhealthiermaternalandneonateoutcomes[18].Therefore,
nutritionalguidelinesshouldbeprovidedaswellasrelevantnutrientsupplementstowomenduringpregnancyto
reducetheriskofLBW.ManaginghighlevelsofanaemiaamongHIVinfectedpregnantwomencanbedone
throughprovisionofappropriatenutritiousfoods.Inaddition,itisimperativetoespeciallytargetfirsttime

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mothersasthefirstbirthwasfoundtobeassociatedwithLBW.
StrengthsandLimitationsoftheStudy
Thestudyislimitedbythecross-sectionaldesignofthestudy.Itisnotpossibletoestablishtemporalityinthis
studyi.e.whetherthemotherswereHIV-positiveduringpregnancyorafterdeliveryhencemakingitchallenging
todeterminewhichcamefirsttheoutcome(LBW)orHIVinfection.Naturally,theuseofsecondarydataisa
limitationasourstudyreliedontheaccuracyofwrittenorreportedrecordsfromthesurvey,thus,makingit
difficulttocontrolforthepossibilityofmisclassificationbiasduetorecallbiassincefactorssuchbirthweightof
infants,age,educationlevelandfamilyincomewereself-reportedintheZDHS.Forexample,maternalrecallwas
usedtoreportbirthweightsofinfantsintheabsenceofthechild’sdeliveryrecordintheZDHS[14].However,
theDHShasbeencollectingdatabysimilarmethodsformorethantwodecades,andtherehasbeen
improvementintherobustnessandreliabilityofdatasets[14].Anotherapparentlimitationofusingsecondary
dataisthatsomeimportantfactorswerenotassessed;thesurveydidnotincludevitalquestionstomeasure
maternalexposuretoART,infantHIVstatusatbirth,obstetriccomplicationsduringbirth,alternativestandard
anthropometricmeasuresforpregnancysuchaspre-pregnancyweightandweightgainduringpregnancy,and
progressionofHIVinfectionduringbirthwhichhavebeenreportedasriskfactorsofLBWinotherstudies[18,32,
33].However,thesecondaryanalysisallowedforcompletionofthestudywithinthelimitedacademictimeframe
andcameatnocostasnofeewasrequiredtoobtainaccesstotheDHSdataset.Additionally,theavailabilityand
useofalargesamplesizeofanationallyrepresentativedatasetwasanapparentstrengthenhancingthepower
ofthestudyandgeneralizationofthefindingstothepopulationofHIVpositivewomenofreproductiveagein
Zimbabwe.
ConclusionsAndRecommendations
TheprevalenceofanaemiaamongHIVpositivewomenishighduringpregnancyeventhoughmaternalanaemia
amongthisgroupofwomeninourstudywasnotassociatedwithLBW.LowBMI,femalesexandparityarekey
riskfactorsofLBWinneonatesborntoHIVinfectedwomen.InZimbabwe,wheretheprevalenceofHIVishigh
andrifeinaneconomicallychallengedera,itisworthnotingthatpolicy-makersandcliniciansshouldputinplace
strategiestoencouragefrequentANCvisitsbyHIVpregnantwomenanddevelopnutritionalguidelinestailoredto
thisgroupofwomen.Generally,akeyrecommendationforpracticeatpolicylevelisthathealthcareservice

15
providersmayusefindingsofthisstudytodevelopscreeningtoolsthatcategorizeandplacethepregnant
womenintorisk-profilesbasedoncertainriskfactors;namelyfromthisstudybyBMIcategorizationofmother,
byexpectedsexofchildandparity.Onbasisofsuchcategorization,appropriateinterventionsthataddress
conditionsleadingtoelevatedanaemiaandLBWamongHIVinfectedpregnantwomencanbetargetedand
modified.
FutureresearchusingmorerobustdesignssuchasaprospectivestudycanfollowupHIVpositivewomenthrough
pregnancytoestablishtheassociationbetweenanaemiaandLBWamongHIVinfectedwomen,whilstcontrolling
forconfoundingbyHIVtreatmentduringthegestationperiodandearlierandobstetriccomplications.
Furthermore,theassociationbetweenHIVstatusoftheHIV-exposedinfantsatbirthshouldfurtherbeexplored.
InthecontextofZimbabwe,thepresentstudyhascontributedtotheunderstandingofthelinkbetweenanaemia
andLBWamongHIVinfectedpregnantwomenatpopulationlevel,factoringinotherpossibleriskfactors.No
priorresearchofthismagnitudehadeverbeenconductedonasampleofHIVpositivewomen,yetthecountryis
endowedwithmanypopulationdatasetsspanningbacktomanyseveralyears.Tothebestofcurrentknowledge,
insufficientsystemsarecurrentlyinplacetomonitorprogressbeingmadetowardsattainingtheUNgoalof
reducingtheprevalenceofLBWby30%by2025[2].Findingsfromthestudythereforeprovideastartingpoint
towardsamenablefactorstomodifyandallowthecountrytoprogresstowardstheUNtarget.Theresearch
findingsalsoprovidecuestohealthserviceprovidersandpolicymakersondeterminantstoconcentratenew
policyguidelinesorfutureresearchoninvolvingHIVinfectedwomentoavertLBW.Ingeneral,thehealthdelivery
systemneedstostrengthenawarenessonthepotentiallyhighriskofLBWcommonfromfirstbirthsand
importanceofanadequatenutritionaldietduringpregnancytoincreaseBMItonormallevels(18.5kg/m2-
24.9kg/m2)includingtheroleofarichdiettoreducelevelsofanaemiaamongHIVwomen.
Abbreviations
ANC–AntenatalCare
ART–Anti-retroviralTreatment
DHS-DemographicandHealthSurvey
HIV-HumanImmunodeficiencyVirus
LBW–LowBirthWeight

16
NBW–NormalBirthWeight
PMTCT-Preventionofmother-to-childtransmission
RR-RelativeRisk
SSA-Sub-SaharanAfrica
UNAIDS–JointUnitedNationsPrograminHIV/AIDS
WHO–WorldHealthOrganisation
ZDHS-ZimbabweDemographicandHealthSurvey
Declarations
EthicalApproval
EthicalapprovaltoconductthestudywasgrantedbyMonashUniversityHumanResearchEthicsCommittee
number:16716.Permissiontousethedatawasgrantedbythe2015ZDHSgatekeepers.Additionalapprovalby
theDHSwasobtainedtoaccessHIVdata.IntheZDHS,allindividualstudyparticipantsweremadeawarethat
participationinthecommunityhealthprofilewasvoluntary[15].Inthisstudy,confidentialityandprivacyofthe
subjectswasmaintainedbynotdisclosingtheirnamesormedicalhistory.Thedatasetwasstoredonaprotected
devicewithapassword,onlyallowingfortheauthorizedresearcher’saccess.
ConsentforPublication
Notapplicable
AvailabilityofDataandMaterials
ThedatathatsupportthefindingsofthisstudyareavailablefromtheDemographicandHealthSurveyProgram
(DHS)howeverrestrictionsapplytotheavailabilityofthesedata,whichwereusedwiththepermissionfromthe
DHSforthisstudy,andsoarenotpubliclyavailable.Dataarehoweveravailablefromtheauthorsupon
reasonablerequestandwiththepermissionoftheDHS.
CompetingInterests
Theauthorsdeclarethattheyhavenocompetinginterests.
Funding
None
AuthorContributions

17
DCconceptualized,analyzed,interpretedthedataandwrotetheoriginaldraftofthemanuscript.STwasthe
majorcontributortothesupervisionoftheconceptualization,writing,analysisandinterpretationofthestudy.TJB
supervisedthewriting,analysisandinterpretationprocess.NKandJWcontributedtothesupervision,
conceptualizationandthewritingofthemanuscript.
Allauthorsread,reviewed,editedandapprovedthefinaldraftofthemanuscript.
Acknowledgements
TheauthorswouldliketothanktheDHSprogramforprovidingaccesstothedatausedinthestudy.
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BirthWeightatMekelle H o s p i t a l  ,  NorthernEthiopia :ACros s  S e c t i o n alStudy.AmericanJourn a l
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pregnancies.SouthAfr i c a n  J o u r n alofObstetricsandGyn a e c o l o g y .2013;19(3):77.
Figures

21
Figure1
Flowchartofselectionofstudyparticipants

22
Figure2
Prevalenceofmaternalanaemia(%)amongHIVinfectedpregnantwomeninZimbabwe,2015

23
Figure3
Prevalenceoflowbirthweight(%)bymaternalanaemiastatusinZimbabwe,2015
Figure4
Notincludedwiththisversionofthemanuscript.
Figure5
Notincludedwiththisversionofthemanuscript.