High prevalence of Plasmodium falciparum and soil-transmitted helminth co-infections in a periurban community in Kwara State, Nigeria

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ContentslistsavailableatScienceDirect

Journal

of

Infection

and

Public

Health

jo u r n al ho me p ag e :h t t p : / /w w w . e l s e v i e r . c o m / l o c a t e / j i p h

High

prevalence

of

Plasmodium

falciparum

and

soil-transmitted

helminth

co-infections

in

a

periurban

community

in

Kwara

State,

Nigeria

Olarewaju

A. Babamale

a

_,

_Uade

_S.

_Ugbomoiko

a,∗

_,

_Jorg

_Heukelbach

b,c

a_Parasitology_Unit,_Department_of_Zoology,_University_of_Ilorin,_Ilorin,_Nigeria

b_College_of_Public_Health,_Medical_and_Veterinary_Sciences,_Division_of_Tropical_Health_and_Medicine,_James_Cook_University,_Townsville,_Queensland,

Australia

c_Department_of_Community_Health,_School_of_Medicine,_Federal_University_of_Ceará,_Brazil

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received13November2016

Receivedinrevisedform10February2017 Accepted25March2017 Keywords: Malaria Soil-transmittedhelminths Interaction Prevalence Nigeria

a

b

s

t

r

a

c

t

Prevalenceofmalariaandsoil-transmittedhelminthinfections,andtheburdenofdiseaseareenormous insub-SaharanAfrica.Co-infectionsaggravatetheclinicaloutcome,butarecommonduetoanoverlap ofendemicareas.Across-sectionalsurveywasconductedtoassessprevalence,intensityofinfectionand associationbetweenmalariaandsoil-transmittedhelminthinfectionsinatypicalperiurbancommunity inKwaraState.FreshbloodandfaecalsampleswereexaminedusingthickbloodﬁlmandKato-Katz smeartechniques.

Atotalof383/471studyparticipants(81.3%)wereinfectedwithatleastoneparasitespecies,withthe followingprevalencesandmeaninfectionintensities:Plasmodiumfalciparum63.7%(2313.6parasites/␮l); Ascarislumbricoides63.1%(3152.1epg);Trichuristrichiura53.3%(1043.5epg);andhookworms30.1% (981.7epg).Sixty-threepercentofthestudypopulationwereco-infectedwithtwoormoreparasite species.TheprevalenceofascariasiswassigniﬁcantlyhigherinindividualsinfectedwithP.falciparum (adjustedOR:5.87;95%CI:3.30–10.42).HeavyA.lumbricoidesandT.trichiurainfectionswereassociated withhighP.falciparumparasitaemia.Co-endemicityofmalariaandsoiltransmittedhelminthinfections isanimportantpublichealthprobleminthestudyarea.Multi-targetintegratedapproachesfocusingon diseaseinterventionareessentialtomitigatemorbiditycausedbymultipleinfections.

©2017TheAuthors.PublishedbyElsevierLimitedonbehalfofKingSaudBinAbdulazizUniversity forHealthSciences.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense(http:// creativecommons.org/licenses/by-nc-nd/4.0/).

Introduction

Despite intensive control measures performed worldwide,

malariastillcausesaserioushealthburdeninmanytropicaland

subtropicalcountries,withtheDemocraticRepublicoftheCongo

andNigeriaaccountingformorethan35%ofglobalmalariadeaths

[1].Commonly,there is a geographical overlap of regionswith

highmalariaendemicity,andtheoccurrenceofNeglected

Tropi-calDiseases(NTDs),suchassoil-transmittedhelminthinfections.

Asa consequence,co-infections are expected tobe a common

phenomenon,ratherthananexception,mainlyinresource-poor

communities[2–5].

Whilesinglemalariainfectionsareoftenseriousandevenfatal

especiallyinchildren,intestinalhelminthinfectionsmayalsoresult

∗ Correspondingauthor.

E-mailaddress:samugbomoiko@yahoo.com(U.S.Ugbomoiko).

inseriousclinicaloutcomes.Consequently,socialandclinical

con-sequencesofmultipleinfectionsareheavilyincreased,ascompared

tosingleinfections[5–8].

In Nigeria, soil-transmitted helminth infections and malaria

are recognized major public health problems [3,9]. Endemic

areas aremostly sustained byecological, behavioral and

socio-environmental conditions that favor parasite development and

transmission,andincludehighlyvulnerablepopulations[5,9,21].

Previousstudiesinschoolchildrenrevealedantagonisticeffects

inhelminth-schistosomecoinfection[5].However,

epidemiolog-ical surveillance and spatial congruence of both malaria and

helminthiasesremainpoorlydeﬁnedinNigeria.Thisbaseline

infor-mationisnecessaryforcost-effectivecontrolmeasuresthatrather

targetmultiplediseasesthanasingleinfections.Thepresentstudy

investigatedmalariaandsoil-transmittedhelminthinfectionsina

communityinnorthcentralNigeria.

https://doi.org/10.1016/j.jiph.2017.03.002

1876-0341/©2017TheAuthors.PublishedbyElsevierLimitedonbehalfofKingSaudBinAbdulazizUniversityforHealthSciences.Thisisanopenaccessarticleunder theCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).

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Materialsandmethods

Studyareaandpopulation

A community-based study was conducted in Ogele, a

typi-cal peri-urbanarea. Ogele is a small linear settlement,located

alongtheoldOgbomoshoroad,about13kmfromIlorin,thestate

capitalofKwaraState.Theclimateistropical,withwell-deﬁned

wet(April–October)and dry(November–March)seasons (mean

annual precipitation of >1.100mm). The community is located

inthetransitionalzonebetweenrainforestandsavannah

grass-land.

The inhabitants belong mainly to the Yoruba ethnic group,

withasmallproportionofHausa,NupeandFulaniethnicgroups.

Thevast majority(95%) areMuslimswitha fewChristians and

membersoftraditionalreligions[10].Peoplearemainlypeasant

farmers,andgrowcropssuchascassava,maize,vegetablesand

yam.

Generally,sanitationstatusispoor.Mosthousesaredevoidof

toiletsandadequateventilation,withdumpsiteslocatedcloseto

humanhabitations.Thecommunityisinadequatelyprovidedwith

essentialamenities,suchaselectricityandportablewatersupply.

Thereisone primaryschool,a secondary schoolanda primary

healthcarecentre.

Datacollectionandlaboratoryprocedures

First,weperformedacensusinthecommunity,consistingof

ahouse-to-housesurvey.ThepopulationinOgelewasestimated

toamount619.Individualswithhistoryofanthelminthicand

anti-malarialtreatment(pastthreeweeks)andthoselivingforlessthan

threemonthsinthestudyareawereexcluded.Historyoftreatment

wasconﬁrmedbyexaminationofdrugsand/ormedical

prescrip-tions.

Therecruitmentofparticipantsanddatacollectionwere

con-ducted betweenJanuaryand May2015(end ofdry seasonand

beginningofrainyseason).

Duringhousevisits,participantswereinstructedonhowand

whenthesamples(stoolandblood)weretobetaken.Pre-tested

questionnaireswere administered to obtainsocio-demographic

variables.

Thickandthinbloodsmearswerepreparedonadifferentslide

fromcapillary blood obtainedfrom the3rd ﬁngerof left hand

byﬁngerprickusingasterilelancet.Bloodsmearswerestained

withGiemsaandexaminedundertheoilimmersionmicroscope

objective.Thicksmearwasusedtodiagnosepresenceof

malar-ialinfectionandparasitaemiaload,andthinsmearwasusedto

identifythetypeofPlasmodiumspecies.Thenumberofparasites

permicroliterofbloodwascalculatedasdescribedinCheesbrough

[11].Atleastonehundredﬁeldswereexaminedbeforeanegative

resultwasreported.

Stoolsampleswerecollectedinlabeledwide-mouth

screwed-capped containers and processed for microscopic examination,

usingKato-Katzthicksmearmethod[12].Kato-Katzslideswere

examinedattheParasitologyLaboratoryofUniversityofIlorinfor

thepresenceofhelmintheggs,withinaweekafterpreparation.

Toestimateintensityofinfection,eggcountsperslidewere

con-vertedtoeggpergramoffaeces(epg)bymultiplyingnumberof

eggsontheslide by24.The meandensityof theepgoffaeces

wasusedto classifythepattern ofinfection aslight, moderate

andheavyinfection,asdeﬁnedbyWHO[13].Allbloodandstool

slideswereexaminedbytwoinvestigatorswhowereblindedtothe

results,andwherepositive/negativediscrepancyoccurred,slides

werecounter-readbyathirdexperiencedparasitologist(USU),who

wasblindedregardingthetwopreviousresults.

Table1

Demographiccharacteristicsofthestudypopulation(n=471).

Characteristic No(%)

Gender

Male 228(48.4)

Female 243(51.6)

Age(years):median(range) 23(3–64)

Toiletfacilities

Cesspit/pit 114(24.2)

None 357(75.8)

Mainsourceofwatersupply

Borehole/well 233(49.5)

Stream/pond 238(50.5)

Education

Primaryeducationcompleted 208(44.1)

Primaryeducationnotcompleted 263(55.9) Bednet(ITN)use

Yes 140(29.7)

No 331(70.3)

Parasiteinfectionpattern

Singleinfection 118(25.1)

Doubleinfection 54(11.5)

Multipleinfection 211(44.8)

Dataanalysis

Categoricalvariablesarepresentedasratios(%),andcontinuous variableswithmeansandtheirstandarddeviations(SD). Differ-encesintheprevalenceandintensityofinfectionbetweenages andsexesweretestedusingtheChisquared(categoricalvariables) andonewayANOVAtests(continuousvariables).Asstratified anal-yseshaveshownaconsiderableinfluenceofageandsexregarding andinfectionintensitieswerestratifiedbysexandage.Statistical analyseswereperformedusingExcel(WindowsCorporation, Red-mond,WA,USA)andSPSSversion16(SPSSInc.,Chicago,IL,USA). Prevalence,simplelogisticregressionanalysiswasappliedto deter-mineassociationbetweentheparasitesspeciesadjustedwithage andsex.

Results

Atotalof508peoplewereeligible(70.6%oftargetpopulation); 25hadahistoryofanthelminthicandantimalarialtreatmentinthe pastthreeweeks,and12hadbeenlivingforlessthanthreemonths inthestudyareaandwereexcluded;resultinginastudypopulation of471individuals.Ofthese228(48.4%)weremalesand243(51.6%) females,withamedianageof23years.Morethanhalfofthe pop-ulationwereilliterate;onlyabout1/4hadaccesstoITNbednets, andthevastmajorityhadnotreceivedanyanthelminthictreatment withinthelast3weeks.Detaileddemographiccharacteristicsofthe studypopulationaresummarizedinTable1.

Prevalence of Plasmodium falciparum infection was highest

(64%),followedbyascariasis (63%),trichuriasis(53%)and

hook-worm infection(30%,Table2).Alow prevalenceofPlasmodium

vivax(0.03%)wasrecordedinthestudyarea.Atotalof383(81.3%)

wereco-infectedwithoneormoreparasitespecies.

The prevalence and intensity of each of the four parasite

speciesfollowedsimilarpatterns,andvariedsigniﬁcantlywithage

(Tables2and3).Withtheexceptionofhookworminfection,which

showedasigniﬁcantsteadyincreasewithage,highestprevalences

wereobservedin11–20year-olds.

Infection densities are detailed in Table 3. Soil-transmitted

helminthinfectionsweremoreprevalentandshowedsigniﬁcantly

higherinfectionintensityamongmales.Infectiondensityofmalaria

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Table2

PrevalenceofPlasmodiumfalciparumandofsoil-transmittedhelminthinfections,stratiﬁedbyageandsex(n=471). Parasitespecies

N Plasmodiumfalciparum(%) Ascarislumbricoides(%) Trichuristrichiura(%) Hookworms(%) Agegroup(years)

≤5 58 42(72.4) 19(51.5) 13(22.4) 1(1.7) 6–10 45 39(64.4) 34(75.4) 32(71.1) 1(2.2) 11–20 110 77(70.0) 86(78.2) 71(64.5) 5(4.5) 21–30 112 75(67.0) 83(74.1) 72(64.3) 32(28.6) 31–40 40 11(27.5) 24(60.0) 20(50.0) 26(65.0) 40+ 106 66(62.3) 51(48.1) 43(40.6) 77(72.6) pValue <0.0001 <0.0001 <0.0001 <0.0001 Sex Male 228 148(64.9) 167(73.2) 141(61.8) 81(35.5) Female 243 152(62.6) 130(53.5) 110(45.3) 61(25.1) pvalue 0.595 <0.0001 <0.0001 0.014 Total 471 300(63.7) 297(63.1) 251(53.3) 142(30.1) Table3

Meanintensity(±standarddeviation)ofPlasmodiumspeciesandsoil-transmittedhelminths,stratiﬁedbyageandsex.

N Plasmodiumspp. A.lumbricoides T.trichiura Hookworms

Age ≤5 58 2948.36±2280.64 724.28±1375.78 280.66±675.76 13.24±100.84 6–10 45 2579.51±2804.84 3856.67±3474.93 1013.42±1278.45 47.47±318.42 11–20 110 2374.95±2339.08 4461.18±3886.44 1457.95±1294.59 123.65±638.46 21–30 112 2114.12±2495.29 3795.48±3508.36 1373.48±1427.96 1003.86±1757.14 31–40 40 1099.20±2133.38 2423.92±2664.21 1072.82±1222.95 2248.30±1976.55 41+ 106 1664.45±1910.17 2418.09±3351.76 821.66±1170.32 2297.05±2141.84 pValue 0.018 <0.0001 <0.0001 <0.0001 Sex Male 228 2376.91±5582.36 4055.90±3733.42 1254.81±1338.44 1236.28±1896.90 Female 243 2254.28±4908.77 2304.16±3056.20 845.27±1214.01 742.74±1578.62 Total 471 2313.64±5240.38 3152.14±3508.45 1043.52±1290.76 981.65±1755.55 pValue 0.890 0.001 0.001 0.002

About 23% of individuals were infected with two parasite species,and52%ofthosewithmultipleinfectionswereinfected withthreeparasitespecies,withthemostprominentcombination ofP.falciparum,AscarislumbricoidesandTrichuristrichiura.Outof 300subjectspositiveforP.falciparum,3(1%),49(16.3%)and158 (52.7%)werenotco-infectedwithA.lumbricoides,T.trichiuraand hookworms,respectively.57%,30.3%and11.7%ofparticipantshad light,moderateandheavyAscarisinfection.Similarly,8.7%,25%and 13%hadlight,moderateandheavyhookworminfection respec-tively.

Logistic regression analysis on the independent association betweenco-infections, controlledby sexand age is detailed in Table4. Ahighly signiﬁcantassociationwas observedbetween

increasingparasiteloadsofascariasisandtrichuriasis.Parasitaemia

loadofP.falciparumalsoincreased(Table5).

Discussion

Ourstudyevidencedahighprevalenceofco-infectionofmalaria

and soil transmittedhelminth infections in a typicalperiurban

communityinNigeria.Malaria,ascariasis,trichuriasisand

hook-worminfectionswereverycommon.Prevalenceandintensityof

ascariasisandtrichuriasiswereassociatedwithseveremalaria.The

datareiteratetheWorldHealthOrganization’sinsistence foran

integratedapproachtoimprovetropicaldiseasesurveillanceand

control[14].

Co-infectionswithdifferentspeciesweretherule—morethan

4/5of the participantshad infections by two or more parasite

species.TheoccurrenceofA.lumbricoides,T.trichiuraand

hook-wormshasbeenreportedpreviouslyinchildrenandadults,and

theseinfections indeed are consideredsome ofthe most

com-monparasiticdiseasesofmankind[5,21,22].Clinicalimplications

aretremendous—forexample,childrenwithparasiticco-infections

andhighparasiteloadstendtosuffermorecommonlyfromreduced

cognitivefunctions,malnutrition,growthretaradationand

iron-deﬁciencyanemia[5–8].Previoussurveysamongschoolchildren

inresource-poorcommunitiesinsub-SaharanAfricashowedthat

polyparasitismisindeedacommonphenomenoninmanyareas,

withvulnerablepopulationsexposedtohighestrisks.Similarto

manyinfectiousdiseases,highriskpopulationsforco-infections

usuallysharelowsocio-economiccharacteristics[2,4,5,15].

Ourﬁndingsofchildrenbeingahighriskgroupformalaria

infec-tionhavebeenwidelyreportedpreviouslyfromendemicregions

[16,17].Distributionbysexwasaspreviouslyreportedinthe

south-westofNigeria[18,19]andothermalaria-endemicregions[20].The

parasitedensityofP.falciparuminrespecttosexandagefollowed

asimilarpattern;withintheyoungeragegrouptherewasa

con-sistentlyhigherprevalenceandparasitedensitythanintheadult

group.Thisobservationhasearlier beenreportedbyRasoetal.

[20]inastudyofmultipleparasiteinfectionsinruralCôted’Ivoire

andotherstudiesinmalariaendemicregions,andreasonswere

attributedmainlytohigherexposureandimmunologicalfactors

[2,14].MalesweretwicelikelytobeinfectedwithA.lumbricoides

thantheirfemalecounterparts.Thesepredictionswereconsistent

withreportsfromotherendemicregions[5,34,35].

ThehighprevalenceinA.lumbricoidesandTtrichiuraare

indica-tive of the similar transmission pattern reported by different

authors[5,23–25].Theoccurrenceofascariasisandtrichuriasiswas

observedtopeakintheyoungagegroupof11–20years,anditwas

peculiartootherstudiesinseverallocalities[26,27].Thismightbe

aresultofdevelopmentofprotectiveimmunityduetorepeated

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Table4

LogisticregressionanalysisofinteractionofPlasmodiumspeciesandsoil-transmittedhelminths,adjustedbyageandsex.

Outcomeparasitespecies Exposurevariables N(%) Adjustedoddsratio 95%CI pValue

Plasmodiumfalciparum A.lumbricoides 232(77.3) 5.867 3.304–10.418 <0.0001

T.trichiura 192(64.0) 1.630 0.826–2.474 0.201 Hookworm 86(28.7) 0.973 0.538–1.761 0.928 Malesex 148(64.9) 1.282 0.820–2.007 0.276 Age11–20years 115(69.7) 1.089 0.392–3.026 0.870 A.lumbricoides T.trichiura 230(77.4) 1.747 0.027–0.082 <0.0001 Hookworm 98(33.0) 0.347 0.164–0.733 0.005 Malesex 167(73.3) 1.721 1.029–2.879 0.039 Age11–20years 124(75.2) 3.704 1.079–12.71 0.037 T.trichiura Hookworm 79(55.6) 0.523 0.296–0.925 0.026 Malesex 141(61.8) 1.669 1.134–2.458 0.009 Age11–20years 105(63.6) 9.089 2.985–27.67 0.037

Hookworm Sex(male) 81(35.5) 2.567 1.498–4.400 0.001

Age11–20years 20(12.1) 0.063 0.002–0.048 <0.0001

Table5

Associationbetweenparasiteintensityofsoil-transmittedhelminthsandPlasmodiumfalciparuminco-infectedindividuals.

N Meanintensity(±SD)Plasmodiumfalciparum 95%CI ANOVA(one-way)

A.lumbricoides Uninfected 174 1353.66±2520.990 976.44–1730.87 Lightinfection 171 2339.67±2200.705 2007.46–2671.88 Moderateinfection 91 2556.92±2349.732 2067.5–3046.28 Heavyinfection 35 2813.77±2466.270 1966.58–3660.96 p<0.0001 T.trichiura Uninfected 220 1672.37±2495.251 1340.81–2003.92 Lightinfection 55 2368.22±2396.158 1720.45–3015.99 Moderateinfection 196 2390.86±2304.659 2066.20–2715.52 Heavyinfection 0 – – p=0.006 Hookworms Uninfected 329 2145.88±2577.542 1866.33±2425.44 Lightinfection 26 2007.54±2079.016 1167.81±2847.27 Moderateinfection 77 1872.78±2107.342 1394.47±2351.09 Heavyinfection 39 1650.90±1868.288 1045.27±2256.53 p=0.577

useofanthelminthicdrugsandimprovedhygiene.Similartoother studies,hookwormprevalenceincreasedwithage;thisalsomight duetoadropinimmunitywhichmightbeduetoaging[28].There

wasremarkablestatisticalsigniﬁcanceofoccurrenceofSTHswith

respecttosex;malestendtoshowhigherprevalences,basedon

dif-feringhealthcare-seekingbehavioranddisease-relatedexposure,

asdemonstratedinpreviousstudiesconductedindifferentparts

oftheworld[9,27–31].Someauthorssuggestedthataproportion

oftheelderlypopulationisathighriskofveryheavyhookworm

infection,duetoincreasedexposureorage-dependent immune

mechanisms[32].

Our data revealed that intestinal helminth infections were

associatedtoeachother,andco-occurrenceofparasiticdiseases

occurred frequently. Individuals co-infected with P. falciparum

weresigniﬁcantlymore likely toharbourA. lumbricoidesand T.

trichiurainfections, ascompared toindividualswithoutmalaria.

Similarly,individualsco-infectedwithA.lumbricoidesweretwice

likely tohave T. trichiura than individuals without. In fact,the

parasiticdiseasesunderstudysharesimilarriskfactorsfor

trans-missioninsuchlocalities,andarelinkedtolowsocio-economic

status.Inaddition,theparasitesmayinteractdirectlyininfected

hosts—polyparasitismandparasiteinteractionshavebeenreported

previouslyfromendemiccommunities[5,20,23,33].Further,the

distribution of malaria often overlaps geographically with the

presenceofNTDs,suchasintestinalhelminthinfections.Asa

con-sequence,polyparasitismisacommonphenomenoninhighrisk

groupslivinginendemicareas[2,3].Theassociationhasalsobeen

insinuatedasresultofimpairedimmunologicalstatusof

individu-alswithmultipleinfections[36].

Anotherimportantaspectofourﬁndingswastheinteractionof

severityofsoil-transmittedhelminthinfectionsandtheseverity

of malaria infection.Nacheret al. [37] reportedthat A.

lumbri-coidesandother soil-transmittedinfectionssuppressedcerebral

malaria, renalfailure,jaundiceand protectedagainsthighbody

temperature.ThelikelihoodofP.falciparuminfectionwasobserved

toincreasein patientswithhelminthinfections inalow

trans-missionarea[38].Incontrast,inourstudy,heavyascariasisand

trichuriasisinfectionswereassociatedwithhigherPlasmodium

par-asitaemia; while onthe otherside those withlight hookworm

infectionpresentedhighPlasmodiumparasitaemia.Increasein

Plas-modiumdensitywasfoundtoberelatedtothenumberofhelminth

species,rathertheintensityofhelminthinfection.Accordingtothe

reportofMwangietal.[39]fromahighmalariatransmissionarea,

helminthinfectionsweremostlikelyleadingtoanincreasedriskof

diseasefornon-severemalaria,whiledecreasingtheriskforsevere

malaria.

Our study is subject to limitations. As infections, especially

malaria,showseasonalvariations,interpretationofresultsshould

considerthecross-sectional study design.Speciﬁcally,data

col-lection covered the dry seasonand terminated at theonset of

therainyseason.Thus,malariaprevalenceandcoinfectionrates

aresupposedtobeunderestimated.Forlogisticreasons,onlyone

faecalsamplewascollected,whichmayhavecaused

underestima-tionofprevalencesofintestinalhelminthinfections.Inaddition,

theintensitiesofparasites encounteredmaybeunderestimated

becauseofrelativelylowsensitivityofKato-Katzdiagnosticmethod

employed.Forthissamereason,humanpinworminfectionwasnot

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Itwasnotthefocusofourstudy,toinvestigateclimatic,

envi-ronmentalandsocio-economicdeterminantsofparasiteinfections,

butrathertoprovideadatabaselineforplanningofintervention

measures,andforfutureresearch,includingsystematicstudieson

riskfactorsfordiseaseandco-infection.Ourresultscanbe

consid-eredrepresentativeforthepopulation,andforsimilarcommunities

intheregion.

Conclusions

Co-endemicityofmalariaandsoiltransmittedhelminth

infec-tionsisanimportanthealthprobleminthestudyarea,perpetuating

healthproblems particularlyofhighly vulnerablegroups inthe

population.

Thestudyprovidesevidenceforthepositiveimpactof

multi-target approaches focusing onintegrative disease intervention.

Interventionstargetingasinglehelminthinfectionshouldinclude

simultaneouslyincludemalarialinfection,andfocusonthe

reduc-tion of co-infections. For example, combining vector control

strategies(e.g.byuseoflong-lastinginsecticidalnets)withthe

administrationofanthelminthicdrugswillsigniﬁcantlyimprove

thewell-beingoftheentirepopulation.

Author’scontributions

BOAcollecteddata,participated in thedesignand statistical

analysis.USUconceivedanddesignedthestudy,performed

statisti-calanalysisanddraftedthemanuscript.JHconceivedanddesigned

thestudy,assistedwithstatisticalanalysisandhelpedtodraftthe

manuscript.Allauthorsreadandapprovedtheﬁnalmanuscript.

Funding

Nofundingsources.

Competinginterests

Nonedeclared.

Ethicalapproval

ThisstudywasapprovedbytheEthicalReviewBoardofIlorin

University,Ilorin,KwaraState.Priortothestudy,wevisitedthe

communityleaderstoseekfortheirconsent.Writtenconsentwas

obtainedfromstudyparticipantsorinthecaseofminorsfromtheir

guardians.

Acknowledgments

JH is class 1 research fellow from the Brazilian Research

Council (Conselho Nacional de Desenvolvimento Cientíﬁco e

Tecnológico—CNPq).

References

[1]World Health Organization. World Malaria Report; 2015. www.who.int/ malaria/publications/world-malaria-report.

[2]BrookerS,AkhwaleW,PullanR.EpidemiologyofPlasmodium-helminths coin-fectioninAfrica:populationsatrisk,potentialimpactonanemia,andprospects forcombiningcontrol.AmJTropMedHyg2007;77:88–98.

[3]HotezPJ,KamathA.Neglectedtropicaldiseasesinsub-SaharanAfrica:review oftheirprevalence, distribution,and diseaseburden. PLoSNeglTropDis 2009;3(8):e412,http://dx.doi.org/10.1371/journal.pntd.0000412.

[4]MazigoHD,WaihenyaR,LwamboNJ,MnyoneLL,MahandeAM,SeniJ,etal. Co-infectionswithPlasmodiumfalciparum,Schistosomamansoniandintestinal helminthesamongschoolchildreninendemicareasofNorthwesternTanzania. ParasitesVector2010;3:44.

[5]UgbomoikoUS,DalumoV,DanladiYK,HeukelbachJ,OfoezieIE.Concurrent urinaryandintestinalschistosomiasisandintestinalhelminthicinfectionsin schoolchildreninIlobu,South-westernNigeria.ActaTrop2012;123:16–21. [6]SaktiH,NokesC,HertantoWS,HendratnoS,HallA,BundyDAP.Evidenceforan

associationbetweenhookworminfectionandcognitivefunctioninIndonesian schoolchildren.TropMedIntHealth1999;4:322–34.

[7]FriedmanJF,KanzariaHK,McGarveyST.Humanschistosomiasisandanemia: therelationshipandpotentialmechanisms.TrendsParasitol2005;21:386–92. [8]Jardim-BotelhoA,BrookerS,GeigerSM,FlemingF,LopesACS,DiemertDJ,etal. AgepatternsinundernutritionandhelminthinfectioninaruralareaofBrazil: associationswithascariasisandhookworm.TropMedIntHth2008;13:458–67. [9]UgbomoikoUS,DalumoV,ObiezueRN,OfoezieIE.Socio-environmentalfactors inascariasisinfectionamongschool-agedchildreninIlobu,OsunState,Nigeria. TransRSocTropMedHyg2009;103:223–8.

[10]NationalPopulationCommission-NPC2006.

[11]CheesbroughM.Parasitologicaltests,districtlaboratorypracticesintropical Countries.PartI.England:CambridgeUniversityPress;1998.

[12]WorldHealthOrganization.Basiclaboratorymethodsinmedicalparasitology. WldHlthOrg;1991.p.25–8.

[13]WorldHealthOrganization.Worldmalariareport.WldHlthOrg;200232. [14]WorldHealthOrganization.Worldmalariareport.WldHlthOrg;201032. [15]BabamaleOA,ShittuO,DanladiYK,AbdulraheemJY.UgbomoikoUSpatternof

Plasmodium-intestinalhelminthco-infectionamongpregnantwomeninahigh transmissionzoneofmalariainNigeria.AsianPacJTropDis2016;6(6):424–8, http://dx.doi.org/10.1016/S2222-1808(16)61060-5.

[16]SmithJD,ChitnisCE,CraigAG,RobertsDJ,Hudson-TaylorDE,PetersonDS, etal.SwitchesinexpressionofPlasmodiumfalciparumvargenescorrelatewith changesinantigenicandcytoadherentphenotypesofinfectederythrocytes. Cell1995;82:101–10.

[17]RogierC,CommengesD,TrapeJ.Evidenceforanage-dependentpyrogenic thresholdofPlasmodiumfalciparumparasitaemiainhighlyendemic popula-tions.AmJTropMedHyg1996;54:613–9.

[18]OjurongbeO,OgungbamigbeTO,Fagbenro-BeyiokuAF,FendelR,KremsnerPG, KunJ.RapiddetectionofPfcrtandPfmdr1mutationsinPlasmodiumfalciparum isolatesbyFRETandinvivoresponsetochloroquineamongchildrenfrom Osogbo,Nigeria.MalarJ2007;6:41.

[19]OjurongbeO,AdegbayiAM,BolajiOS,AkindeleAA,AdeﬁoyeOA,AdeyebaOA. Asymptomaticfalciparummalariaandintestinalhelminthsco-infectionamong schoolchildreninOsogbo,Nigeria.JResMedSci2011;16:680–6.

[20]RasoG,LuginbuhlA,AdjouaCA,Tian-BiNT,SiluéKD,MatthysB,etal. Mul-tipleparasiteinfectionsandtheirrelationshiptoself-reportedmorbidityina communityofruralCoted’Ivoire.IntJEpidemiol2004;33:1092–102. [21]AsaoluSO,OfoezieIE,OdumuyiwaPA,SowemimoOA,OgunniyiTAB.Effectof

watersupplyandsanitationontheprevalenceandintensityofAscaris lum-bricoidesamongpre-schoolchildreninAjebandeleandIfewara,OsunState, Nigeria.TransRSocTropMedHyg2002;96:600–4.

[22]UgbomoikoUS,OfoezieIE.Multipleinfectiondiagnosisofintestinal helminthi-asisintheassessmentofhealthandenvironmentaleffectofdevelopment projectsinNigeria.JHelminthol2007;81:1–6.

[23]KeiserJ,N’GoranEK,TraoreM,LohourignonKL,SingerBH,LengelerC,etal. Poly-parasitismwithSchistosomamansoni,geohelminths,andintestinalprotozoa inruralC’tedôIvoire.JParasitol2002;88:461–6.

[24]NeedhamC,KimHT,HoaNV,CongLD,MichaelE,DrakeL,etal.Epidemiology ofsoiltransmittednematodeinfectioninHaNamProvince.VietnamTropMed IntHealth1998;3:904–12.

[25]Howard SC,Donnelly CA,Kabatereine NB,Ratard RC, Brooker S.Spatial andintensitydependentvariationsinassociationsbetweenmultiplespecies helminthsinfections.ActaTrop2002;83:141–9.

[26]GalvaniAP.Age-dependentepidemiologicalpatternsandstraindiversityin helminthsparasites.JParasitol2005;91:24–30.

[27]SmithH,DekaminskyR,NiwasS,SotoR,JollyP.Prevalenceandintensityof infectionsofAscarislumbricoidesandTrichuristrichiuraandassociated socio-demographicvariablesinfourruralHondurancommunities.MemInstOswaldo Cruz2001;96:303–14.

[28]BethonyJ,ChenJ, LinS,XiaoS,ZhanB,LiS,etal. Emergingpatternsof hookworminfection:inﬂuenceofagingontheintensityofNecator infec-tioninHainanprovince,People’sRepublicofChina.ClinInfectDis2002;35: 1336–44.

[29]TraubRJ,RobertsonDI,IrwinP,MenckeN,ThompsonA.Theprevalence, inten-sitiesandriskfactorsassociatedwithgeo-helminthinfectionintea-growing communitiesofAssam,India.AmJTropMedHealth2004;9:688–701. [30]CorralesLF,RicardoI,ChristineLM.Associationbetweenintestinalparasitic

infectionsandtypeofsanitationsysteminruralElSalvador.TropMedInt Health2006;11:1821–31.

[31]HotezPJ,BrookerS,BethonyJM,BottazziME,LoukasA,XiaoS.Hookworm infection.NEnglJMed2004;351:799–807.

[32]BrookerS,BethonyJ,HotezPJ.Humanhookworminfectioninthe21stcentury. AdvParasitol2004;58:197–288.

[33]TchuemTchuenteLA,BehnkeJM,GilbertFS,SouthgateVR,Vercruysse J. PolyparasitismwithSchistosomahaematobiumandsoiltransmittedhelminths infectionsamongschoolchildreninLoum,Cameroon.TropMedIntHealth 2003;8:975–86.

[34]FlemingFM,BrookerS,GeigerSM,CaldasIR,Correa-OliveiraR,HotezPJ,etal. Synergisticassociationsbetweenhookwormandotherhelminthspeciesina ruralcommunityinBrazil.TropMedIntHealth2006;11:56–64.

(6)

[35]YatichNJ,YiJ,AgbenyegaT,TurpinA,RaynerJC,StilesJK,etal.Malariaand intestinalhelminthco-infectionamongpregnantwomeninGhana:prevalence andriskfactors.AmJTropMedHyg2009;80:896–901.

[36]Correa-OliveiraR,GolgherGB,OliveiraGC,CarvalhoOS,MassaraCL,Caldas IR,etal.InfectionwithSchistosomamansonicorrelateswithalteredimmune responsestoAscarislumbricoidesandhookworm.ActaTrop2002;83:123–32. [37]NacherM,GayF,SinghasivanonP,KrudsoodS,TreeprasertsukS,MazierD,

etal.Ascarislumbricoidesinfectionisassociatedwithprotectionfromcerebral malaria.ParasiteImmunol2000;22:107–13.

[38]NacherM,SinghasivanonP,YimsamranS,ManibunyongW,Thanyavanich N,Wuthisen R, et al. Intestinal helminth infections are associated with increasedincidenceofPlasmodiumfalciparummalariainThailand.JParasitol 2002;88:55–8.

[39]MwangiTW,BethonyJM,BrookerS.Malariaandhelminthinteractionsin humans:anepidemiologicalviewpoint.AnnTropMedParasitol2006;100: 551–70.