The effects of urbanization on global Plasmodium vivax malaria transmission

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Title:
The effects of urbanization on global Plasmodium vivax malaria transmission
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English
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QI, Qiuyin
Guerra, Carlos A.
Moyes, Catherine L.
Elyazar, Iqbal R F
Gething, Peter W.
Hay, Simon I
Tatem, Andrew J
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BioMed Central (Malaria Journal)
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Abstract:
Background: Many recent studies have examined the impact of urbanization on Plasmodium falciparum malaria endemicity and found a general trend of reduced transmission in urban areas. However, none has examined the effect of urbanization on Plasmodium vivax malaria, which is the most widely distributed malaria species and can also cause severe clinical syndromes in humans. In this study, a set of 10,003 community-based P. vivax parasite rate (PvPR) surveys are used to explore the relationships between PvPR in urban and rural settings. Methods: The PvPR surveys were overlaid onto a map of global urban extents to derive an urban/rural assignment. The differences in PvPR values between urban and rural areas were then examined. Groups of PvPR surveys inside individual city extents (urban) and surrounding areas (rural) were identified to examine the local variations in PvPR values. Finally, the relationships of PvPR between urban and rural areas within the ranges of 41 dominant Anopheles vectors were examined. Results: Significantly higher PvPR values in rural areas were found globally. The relationship was consistent at continental scales when focusing on Africa and Asia only, but in the Americas, significantly lower values of PvPR in rural areas were found, though the numbers of surveys were small. Moreover, except for the countries in the Americas, the same trends were found at national scales in African and Asian countries, with significantly lower values of PvPR in urban areas. However, the patterns at city scales among 20 specific cities where sufficient data were available were less clear, with seven cities having significantly lower PvPR values in urban areas and two cities showing significantly lower PvPR in rural areas. The urban–rural PvPR differences within the ranges of the dominant Anopheles vectors were generally, in agreement with the regional patterns found. Conclusions: Except for the Americas, the patterns of significantly lower P. vivax transmission in urban areas have been found globally, regionally, nationally and by dominant vector species here, following trends observed previously for P. falciparum. To further understand these patterns, more epidemiological, entomological and parasitological analyses of the disease at smaller spatial scales are needed. Keywords: Plasmodium vivax, Urbanization, Dominant Anopheles vectors, Mapping
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Publication of this article was funded in part by the University of Florida Open-Access publishing Fund. In addition, requestors receiving funding through the UFOAP project are expected to submit a post review, final draft of the article to UF's institutional repository, IR@UF, (www.uflib.ufl.edu/UFir) at the time of funding. The institutional Repository at the University of Florida community, with research, news, outreach, and educational materials.
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Qi et al. Malaria Journal 2012, 11:403 http://www.malariajournal.com/content/11/1/403; Pages 1-11
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doi:10.1186/1475-2875-11-403 Cite this article as: Qi et al.: The effects of urbanization on global Plasmodium vivax malaria transmission. Malaria Journal 2012 11:403.

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Additional file 1 : Table A1 .1: Results of Wilcoxon Signed Rank tests on Pv PR values between GRUMP UE defined urban (U) and rural(R) survey pairs for the dominant Anopheles vectors of human malaria in Asia Pacific region Dominant Anopheles vector species No. pairs U>R U
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Table A1 .2 : Results of Wilcoxon Signed Rank tests on Pv PR values between GRUMP UE defined urban (U) and rural(R) survey pairs for the domina nt Anopheles vectors of human malaria in Africa, Europe and the Middle East Dominant Anopheles vector species No. pairs U>R U
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Table A1 .3 : Results of Wilcoxon Signed Rank tests on Pv PR values between GRUMP UE defined urban (U) and rural(R) survey pairs for the dominant Anopheles vectors of human malaria in the Americas Dominant Anopheles vector species No. pairs U>R U


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RESEARCHOpenAccessTheeffectsofurbanizationonglobal Plasmodium vivax malariatransmissionQiuyinQi1*,CarlosAGuerra2,CatherineLMoyes2,IqbalRFElyazar3,PeterWGething2,SimonIHay2,5andAndrewJTatem1,4,5AbstractBackground: Manyrecentstudieshaveexaminedtheimpactofurbanizationon Plasmodiumfalciparum malaria endemicityandfoundageneraltrendofreducedtransmissioninurbanareas.However,nonehasexaminedthe effectofurbanizationon Plasmodiumvivax malaria,whichisthemostwidelydistributedmalariaspeciesandcan alsocausesevereclinicalsyndromesinhumans.Inthisstudy,asetof10,003community-based P vivax parasite rate( Pv PR)surveysareusedtoexploretherelationshipsbetween Pv PRinurbanandruralsettings. Methods: The Pv PRsurveyswereoverlaidontoamapofglobalurbanextentstoderiveanurban/ruralassignment. Thedifferencesin Pv PRvaluesbetweenurbanandruralareaswerethenexamined.Groupsof Pv PRsurveysinside individualcityextents(urban)andsurroundingareas(rural)wereidentifiedtoexaminethelocalvariationsin Pv PR values.Finally,therelationshipsof Pv PRbetweenurbanandruralareaswithintherangesof41dominant Anopheles vectorswereexamined. Results: Significantlyhigher Pv PRvaluesinruralareaswerefoundglobally.Therelationshipwasconsistentat continentalscaleswhenfocusingonAfricaandAsiaonly,butintheAmericas,significantlylowervaluesof Pv PRin ruralareaswerefound,thoughthenumbersofsurveysweresmall.Moreover,exceptforthecountriesinthe Americas,thesametrendswerefoundatnationalscalesinAfricanandAsiancountries,withsignificantlylower valuesof Pv PRinurbanareas.However,thepatternsatcityscalesamong20specificcitieswheresufficientdata wereavailablewerelessclear,withsevencitieshavingsignificantlylower Pv PRvaluesinurbanareasandtwocities showingsignificantlylower Pv PRinruralareas.Theurban – rural Pv PRdifferenceswithintherangesofthedominant Anopheles vectorsweregenerally,inagreementwiththeregionalpatternsfound. Conclusions: ExceptfortheAmericas,thepatternsofsignificantlylower P vivax transmissioninurbanareashave beenfoundglobally,regionally,nationallyandbydominantvectorspecieshere,followingtrendsobserved previouslyfor P falciparum .Tofurtherunderstandthesepatterns,moreepidemiological,entomologicaland parasitologicalanalysesofthediseaseatsmallerspatialscalesareneeded. Keywords: Plasmodiumvivax ,Urbanization,Dominant Anopheles vectors,MappingBackgroundTheworldpopulationhasundergoneunprecedented growthalongwithrapidurbanization.Slightlymorethan 50%ofthepopulation(3.6billion)isnowlivinginurban areascomparedtoonly30%(0.7billion)in1950[1].By 2050,itisprojectedthaturbandwellerswillaccountfor approximately67%(6.3billion)oftheworldtotal population,whilemostoftheestimatedgrowthwillbe concentratedinlessdevelopedregions,particularlyin AsiaandAfrica[1].Thesesubstantialtransitionshave significantpublichealthimplicationsassociatedwith changesinthesocialandphysicalenvironmentand accesstopublichealthservices[2-6]. Althoughlargeheterogeneityexists,itiscommonly acceptedthattheprocessofurbanizationreducesmalariatransmission,primarilybecauseurbanenvironments (e.g.thelackofsuitablebreedingsites,thepollutionof existinglarvalhabitats,etc.)aregenerallyunsuitablefor *Correspondence: qiuyinqi@ufl.edu1DepartmentofGeographyandEmergingPathogensInstitute,Universityof Florida,Gainesville,FL,USA Fulllistofauthorinformationisavailableattheendofthearticle 2012Qietal.;licenseeBioMedCentralLtd.ThisisanOpenAccessarticledistributedunderthetermsoftheCreative CommonsAttributionLicense(http://creativecommons.org/licenses/by/2.0),whichpermitsunrestricteduse,distribution,and reproductioninanymedium,providedtheoriginalworkisproperlycited.Qi etal.MalariaJournal 2012, 11 :403 http://www.malariajournal.com/content/11/1/403

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malariavectors[7-9].Otherexplanationsincludebetter accesstohealthcareservicesandanincreasedratioof humanstomosquitoes[7,10,11].However,thereisconcernregardingurbanmalariainlessdevelopedregions, typicallythoseundergoingrapidandunprecedented urbanization[12,13]. Betweenthetwodominantparasitespeciesofhuman malaria, Plasmodiumfalciparum hasattractedthefocus ofmostresearchbecauseofitshighmortalityandintensivetransmissioninAfrica[14]. Plasmodiumvivax malaria,incontrast,iscommonlyconsideredasa “ benign ” infectionandlargelyoverlookedbyresearchers,government,andfundingagencies.Increasingevidencehas shownthat P vivax isneitherrarenorbenign,however. Itisestimatedthat2.85billionpeoplewereatriskof P vivax infectionin2009,with91%(2.59billion)ofthem livinginCentralandSouthEastAsia[15],andthat P vivax isthemostwidelydistributed(geographically) malariaspeciesofhumans.Furthermore,althoughthe infectionwith P vivax malariaisrarelydirectlyfatal,it cancausesevereclinicalsyndromes[16,17]. Recentstudieshaveexaminedtheimpactof urbanizationon P falciparum malariaendemicityand diseaseburdenestimation[7-9,13,18].Variousurbanextentmapshavebeenusedtocomparethedifferencesin P falciparum malariaendemicitybetweenurbansettlementsandruralareas[18];excludetheurbanextentsof citiesidentifiedasmalariafreeinthemappingofmalaria transmissionlimits[19,20];downgradeendemicclasses inestimatesofmalariaburden[9,21];andpredict P falciparum malariaendemicitybasedongeo-statistical models[22,23].However,accordingtoourbestknowledge,noknownresearchhasexaminedtheeffectof urbanizationon P vivax malariaoversimilarlylarge scales.Inaddition,theregionsofhighest P vivax transmissioninAsiaarecomposedofaconsiderablygreater rangeofvectorspeciesandspeciescomplexesthanseen inAfrica,where P falciparum transmissionisprincipallyconcentrated[24-27],andurbanizationmayimpact eachofthesevectorspeciesdifferently,dependenton theirpreferencesandbionomics.Forexample, Anopheles culicifacies wasreportedtobethevectorresponsiblefor 60-65%malariacasesinurbanenvironmentsofIndia [28]andshowssignificantenvironmenttoleranceand adaptability[29,30],whilelarvaeof Anophelesstephensi werefoundinvariousdomesticcontainersandcollectionsofwaterrelatedtoconstructionandindustrialsites incities[31,32].Therefore,thereisaneedtoexamine theeffectsofurbanizationon P vivax transmissionby dominantvectorspeciestodiscernwhetherdifferential impactsareevident. Heregeo-referenced P vivax parasiterate( Pv PR)surveysandurbanextentmapsareintegratedtoexamine theimpactofurbanizationon P vivaxmalaria transmissionatvariousspatialscales(global,regional, nationalandatthecitylevel).Furthermore,distribution mapsofdominant Anopheles vectorsareusedtoexplore therelationshipsbetweenurbanization, Anopheles vectorsand P vivax malariatransmission.MethodsDatasets TheMAPPvPRdatabaseAswith P falciparum malaria,parasiterate(PR)is themostcommonlyreportedandconsistentmetricof P vivax malariaendemicity[33].Atotalof10,003 community-based P vivax parasiterate( Pv PR)surveys takenbetween1985and2010wereobtainedbytheMalariaAtlasProject(MAP[34]).Thelogisticallyintensive processofsearchingfor,identifyingandgeo-locatingthe Pv PRsurveyshasbeendocumentedelsewhere[35].All these Pv PRsurveysweregeo-referencedtopreciselocationsandnotduplicatedwithinthreemonthsatthe samesite.Asummaryofsomeofthekeyfeaturesofthe Pv PRsurveydataispresentedinTable1.Ofthesurveys, 410(4.1%)wereintheAmericas,1,651(16.5%)inAfrica, SaudiArabiaandYemen(Africa+),and7,942(79.4%)in CentralandSouthEastAsia(Asia+).Approximatelyhalf (51%)ofthe Pv PRvaluesarezeroandthemajorityof thesurveyswereundertakenafter2000.Thesample sizesofthesesurveysvaries,withmostofthem(76%) arebeinglargerthan50.Amongthe95 P vivax malaria endemiccountries( Pv MECs)[15], Pv PRdatawereavailablefor53(12intheAmericas,19inAfrica+and22in Asia+).Thereare8,588discrete Pv PRsurveylocations andthedistributionofthemareshowninFigure1, overlaidontheinternationallimitsof P vivax malaria transmission[15],withmostofthesurveypointslocated inSoutheastAsiaandtheHornofAfrica.GlobalurbanmapAlthoughurbanizationhasbeenoneofthemostimportanttransformationsofourworldfordecades,thereis stilllittleconsensusonthedefinitionsofwhatconsists anurbanareaandurbanizationamongnationaland internationalbodies[2].Suchambiguityhasleadtothe constructionofseveralglobalurbanmaps(e.g.,Digital ChartoftheWorld(DCW)[36],GlobalRuralUrban MappingProject(GRUMP)[37],AdvancedVeryHigh ResolutionRadiometer(AVHRR)GlobalLandCover Classificationurbanlandcoverclass[38],Defense MeteorologicalSatelliteProgram-OperationalLinescan System(DMSP-OLS)[39],andModerateResolution ImagingSpectroradiometer(MODIS)LandCoverProductBinaryData[40,41])derivedfromsatelliteimagery [42].AsdiscussedinTatemetal.[42],allofthese globalurbanmapsdemonstratedadifferentrangeofQi etal.MalariaJournal 2012, 11 :403 Page2of11 http://www.malariajournal.com/content/11/1/403

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inaccuraciesandlimitations,however,theGRUMP urbanextentmapwasconsideredtobemostaccuratein matchingoriginalurbanassignmentsof P falciparum malariasurveys[18].Therefore,theGRUMPurbanextent(GRUMP-UE)mapwasusedheretodistinguish Pv PRsurveystakeninurbanareasfromthoseinrural areas.Thisurbanextentmapwasdevelopedbythe CentreforInternationalEarthScienceInformationNetwork(CIESIN)at1km1kmspatialresolutionin 2004,utilizinginformationfromsatellitenight-time lights(NTL),Landsatsatellitesensorimageryandother geographicaldata[43].DominantAnophelesvectormapsThedistributionsandbionomicsofdominant Anopheles vectorsplayanimportantroleinmalariatransmission andarethetargetsofvectorcontrol[44].Vectorspecies normallydisplayarangeofecologicalandbehavioural characteristics.Forexample,unlikeothermalariavectors,anurbanenvironmentisfavoredbythe “ urbanvector ” Anophelesstephensi [45].Toassesstheimpactof urbanizationon P vivax malariatransmissionbydominant Anopheles vectors,expert-opiniondistributionmaps ofglobaldominantvectorspecies(DVS)ofmalariawere obtainedfromtheMalariaAtlasProject[25-27,34]. Thesemapswereconstructedthroughexhaustive searchesofliteratureandrefinementthroughopinion andexperienceby Anopheles experts[27].Atotalof41 mapsofDVSwereavailable,ofwhich,19wereinthe Asia-Pacificregion[26],13inAfrica,Europeandthe MiddleEast[25],andnineintheAmericas[27].Analysis UrbanizationandP.vivaxmalariatransmissionToquantifythepatternsof P vivax malariatransmission betweenurbanandruralareasatglobal,regionaland nationalscales,setsofspatiallyandtemporallyassociatedurban – ruralpairsof Pv PRvalueswereobtained andtested.Firstly,allthegeo-referenced Pv PRsurveys wereoverlaidontotheGRUMP-UEmaptoderivean urban/ruralassignment.Followingpreviousapproaches [18],foreach Pv PRsurveyassignedasurban,allthe rural Pv PRsurveystakenwithin100kmandfiveyears wereidentified.Then,theidentifiedrural Pv PRvalues wereaveragedandassignedtothaturban Pv PRsurvey tomakespatiallyandtemporallyassociatedurban – rural Pv PRvaluepairs[18].Giventhehighlyskeweddistributionof Pv PRvaluesintheMAPdatabase[35],theWilcoxonSignedRank[46],anonparametrictestforpaired variables,wasusedtodetermineifsignificantdifferences between Pv PRvaluesinurbanandruralareasexisted. Thesetestswereundertakenglobally,byregion(Africa+, Americas,Asia+)andbycountry(thoseforwhichat leasttenurban – rural Pv PRsurveypairsexisted)to examineifthepatternsof P vivax malariatransmission betweenurbanandruralareasweresignificant. Asthechoiceofspatialandtemporallimits(100km andfiveyears)isarbitraryinobtainingurban – ruralpairs of Pv PRvalues,arobustnessanalysiswasconducted. Setsofurban – rural Pv PRpairswereobtainedthrough applyingvariousspatialandtemporallimits(100km andtwoyears;50kmandfiveyears;50kmandtwo years),andtestedundertheWilcoxonSignedRanktest, respectively.Inaddition,themeannumberofrural Table1Summaryofthe Pv PRsurveysbyregionAfrica+AmericasAsia+Total Pv PRvalues Numberofzerorecords1,2991933,6315,123 Mean Pv PR(%)0.603.253.553.05 Median Pv PR(%)0.000.610.510.00 Timeperiodofsurveys 1985-19992252231,3281,776 2000-20101,4261876,6148,227 Samplesize 1-509111511,3162,378 >507402596,6267,625 Median(IQR)48(34 – 109)87(37 – 210)120(67 – 281)107(53 – 236) Recordsofsurveys GRUMP-UEdefinedurban444617551,260 GRUMP-UEdefinedrural1,2033497,2418,743 Discretegeographiclocations1,4242916,8738,588 Total1,6514107,94210,003Africa+=Africa,SaudiArabiaandYemen;Asia+=CentralandSouthEastAsia.Qi etal.MalariaJournal 2012, 11 :403 Page3of11 http://www.malariajournal.com/content/11/1/403

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surveyspairedtoeachurbansurveyandtheoverlaprate ( P numberofruralsurveyspairedtoeachurbansurvey/totalnumberofruralsurveys)foreachspatialand temporallimitwerecalculatedtoassesstheeffectsof overlappingruralsurveysinthesamplepairs. Toexaminelocalvariations(cityscale)in Pv PR, groupsof Pv PRsurveysinsideindividualcityextents (urban)andsurroundingareas(rural)wereidentified andtested.Citieswheremorethaneight Pv PRsurveys (toprovideareasonablenumberofcitiesfortesting)fell insidetheirurbanextentswerefirstidentified.Foreach city,rural Pv PRsurveysthatfellwithin100kmofthe centroidoftheurbanextentwerefoundandassignedto thatcity.Followingthis,foreachcity, Pv PRvalues withinitsurbanextentandsurroundingruralareawere comparedandtestedusingtheWilcoxonRankSumtest.DominantAnophelesvectorsTheimpactofurbanizationonmalariaendemicitymay varybydominant Anopheles vectorsofhumanmalaria. Totestthis, Pv PRvaluesbetweenurbanandruralareas withintheextentsof41dominant Anopheles vector wereexamined. Setsofspatiallyandtemporallyassociatedurban – rural pairsof Pv PRvalueswithintheextentsofeachdominant Anopheles vectorwereextractedandtestedseparately. Thegeo-referenced Pv PRsurveyswerefirstlyoverlaid ontotheGRUMP-UEmaptoderiveanurban/ruralassignment.Foreachdominant Anopheles vector,allthe Pv PRsurveysthatfellwithinitsextentwereextracted. Foreachurban Pv PRsurvey,alloftherural Pv PRsurveystakenwithin100kmandfiveyearswereagainidentified,averagedandassignedtothaturban Pv PRsurvey tomakeasetofspatiallyandtemporallyassociated urban – rural Pv PRvaluepairs[18].Thissetofurban – rural Pv PRvaluepairswerethensubjecttotheWilcoxon SignedRanktesttodetermineifsignificantdifferencesin Pv PRbetweenurbanandruralareasexisted.ResultsUrbanizationand P vivax malariatransmissionAmongthe Pv PRsurveys,1,260wereclassifiedasurban and8,743wereclassifiedasruralbasedontheGRUMPUEmap(Table1).Themeansamplesizewas278for theurbansurveysand230fortheruralsurveys,which arecomparable.Table2showstheresultsofthe WilcoxonSignedRanktestsbetweenurbanandrural pairsof Pv PRvaluesdefinedbyGRUMP-UE.Significantlyhigher Pv PRvaluesinruralareaswerefoundgloballyandintheAfrica+andAsia+regions,whileinthe Figure1 Theglobalspatiallimitsof P vivax malariatransmissionin2009[ 15 ]. Panel A showsthespatiallimitsof P vivax malariarisk definedby P vivax annualparasiteincidence( Pv API)data.Areasweredefinedasstable(darkgrey,where Pv API 0.1per1,000pa),unstable (mediumgrey,where Pv API<0.1per1,000pa)andnorisk(lightgrey,where Pv API=0per1,000pa).Thecommunity-based Pv PRsurveysare plottedandcoloredbasedontheirvalues(red,where Pv PR>7%;yellow,3%< Pv PR<7%;lightblue, Pv PR<3%)withzero-valuedsurveys showninwhite.Panel B andPanel C areclose-upsforregionswithplentyof Pv PRsurveyswithPanelBshowingtheareaaroundJakarta, IndonesiaandPanel C showingtheareasaroundSorong,Indonesia. Qi etal.MalariaJournal 2012, 11 :403 Page4of11 http://www.malariajournal.com/content/11/1/403

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Americas,significantlylowervaluesof Pv PRinrural areaswerefound.The Z valuesindicate,however,that thedifferencesobservedintheAmericasareweaker thaninotherregions.Moreover,thenumbersofsurveys availableweremuchsmallerintheAmericas. Thosecountrieswithatleasttenurban – rural Pv PR valuepairsandtheothercountriescombinedforeach region(Africa+,AmericasandAsia+)weretestedfurther andtheresultsarepresentedinTable2.Thetrends foundinmostofthecountriesinAfrica+(Ethiopia, Yemen)andAsia+(Bangladesh,Indonesia,India, Cambodia,Nepal,Thailand,Vietnam)wereconsistent withtheglobalandregionalfindings,withsignificantly lowervaluesof Pv PRinurbanareas.Therelationships foundbetweenurbanandrural Pv PRvaluesforthe othercountriesinAfrica+(SudanandotherAfrican countries)andAsia+(Afghanistan,China,Pakistanand otherAsiancountries)werenotsignificant.Thereare twocountries(GhanaandZambia)inAfricathathave sufficient Pv PRsurveysbutareofentirelyzerovalues, sowerenotlisted.TheresultsfortheAmericasare certainlynotasconclusiveastherelationshipsfoundin theotherregions,withonecountry(Brazil)showing significanthigherurban Pv PRvalues,anothercountry (Mexico)showingthereverseandtheotherAmerican countriesshowinginsignificantdifferences,thougheach wereonlybasedonasmallnumberof Pv PRpairs. Therobustnessanalysis(Table3)suggeststhatthe overlaprateofruralsurveysdecreasesasthespatialand temporallimitscontract,whilethepatternsof Pv PRbetweenurbanandruralareasatglobalandregionalscales aregenerallyconsistent.Thus,themethodusedtodeterminetherelationshipof P vivax malariatransmission betweenurbanandruralareasisrobustandtheeffects ofoverlappingruralsurveysontheresultsareminimal. Figure2showstheboxplotsforurbanandrural Pv PR surveysforindividualcitieswhoseextentsweredefined bytheGRUMP-UE.Theresultsindicatethatthepatternsamongthe20citiesexaminedwerelessconsistent withtheglobal,regionalandnationalpatternsfound. Sevencities(Alamata,Ethiopia;Jakarta,Batam,Kupang, JambiandAmbon,Indonesia;Rourkela,India)were foundtohavesignificantlylower Pv PRvaluesintheir urbanextentsthanthesurroundingruralareas;twocities(Qandahar,Afghanistan;Ariquemes,Brazil)were foundtohavesignificantlylower Pv PRvaluesintheir Table2ResultsofWilcoxonSignedRanktestson Pv PRvaluesbetweenGRUMP-UEdefinedurban(U)andrural(R) surveypairsforcountries,regionsandtheWorldRegionNo. pairs U>RU
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surroundingruralareas(thoughagain,thenumbersof surveysweresmall).Theremainderwereeitherinsignificantorofzero Pv PRvalues.Dominant Anopheles vectorsFigure3ApresentstheresultsofWilcoxonSignedRank testson Pv PRvaluesbetweenGRUMP-UEdefined urbanandruralsurveypairsstratifiedbythedominant Anopheles vectorsofhumanmalariaintheAsia-Pacific region.Inthisregion,thepatternsoflower P vivax malariatransmissioninurbanareasarenoticeableandconsistent,withsignificantlyhigherrural Pv PRvaluesfound formostofthedominant Anopheles vectordistributions (17outof19).Furthermore,insignificantdifferencesbetweenurbanandruralareas( Anophelesbalabacensis and Anopheleslesteri )werefoundinregionswithsmall numbersofsurveypairs. Figure3BshowstheresultsofWilcoxonSignedRank testson Pv PRvaluesbetweenurbanandruralsurvey pairsstratifiedbythedominant Anopheles vectordistributionsinAfrica,EuropeandtheMiddleEast. Pv PR surveyswereonlyavailablefornine(ofthe13)dominant Anopheles vectors.Theconsistentpatternsoflower Pv PRvaluesinurbanareasarenotasevidentasinAsiaPacificregion.Thedifferencesof Pv PRbetweenurban andruralareasarefoundtobestatisticallysignificant foronlyfour(outofnine)dominant Anopheles vectors ( Anophelesarabiensis Anophelesfunestus Anopheles nili and Anophelessergentii ).Theotherswereinsignificant,whiletwoofthem( Anophelesmelas and Anopheles sacharovi )haveinsufficientnumberof Pv PRsurveys. Figure3CpresentstheresultsofWilcoxonSigned Ranktestsforanalysesstratifiedbydominant Anopheles vectorsintheAmericas.Fortwo(outofnine)ofthe dominant Anopheles vectorsno Pv PRsurveysfellwithin theirextents.Unlikethepatternsexhibitedintheother regions,consistentlyhigher Pv PRvaluesinurbanareas wereobservedinthisregion,withmostofthedominant Anopheles vectors( Anophelesalbitarsis Anopheles darlingi Anophelesmarajoara and Anophelesnuneztovari )showingsignificantlyhigherurban Pv PRvalues. However,thenumbersofsurveypairsinthisregionare generallysmall. Moredetailedstatisticalresultsforthethreeregions areprovidedinAdditionalfile1.DiscussionTherapidurbantransformationofthedevelopingworld [47]hasandwillcontinuetohaveaprofoundinfluence onthemalarialandscape.Theneedforaccurateand contemporarydescriptionsofpopulationsatrisk(PAR) hasleadtoseveralattemptstoquantifytheimpactof urbanizationon P falciparum malariatransmission [9,13,18].Knowledgeislackinghoweverregardingthe relationshipbetweenurbanizationand P vivax malaria transmission.Inthisstudy,themostcontemporaryand comprehensivedatabaseof Pv PRsurveyswasusedto explorethedifferencesin P vivax transmissionbetween urbanandruralareas. Lower P vivax malariatransmissioninurbanareas thansurroundingruralareaswasfoundglobally,andin theAfrica+andAsia+regions(Table2),whichcorroboratespreviousfindingsthattheurbanenvironmentis typicallynotsuitableformalariamosquitovectors[7-9]. Theconsistentpatternsofsignificantlylowerurban Pv PRvaluesfoundatthenationalscaleinmostofthe countriesinAfrica+andAsia+furthersupportsthese findings(Table2).However,theurban – ruralsurvey pairsforeachregionaredominatedbyafewcountries (e.g.,Indonesiaaccountsfor65%oftheAsiapairsand Sudanaccountsfor45%oftheAfricapairs),whichmake thepatternsfoundatregionalscalelessinformative. Distinctandinconsistentresultswerefoundinthe Americas,withhigher Pv PRvaluesinurbanareasatthe continentalscaleandforoneparticularcountry(Brazil) atthenationalscale.Thisresultisprobablyduetothe lackof Pv PRsurveysinthisregion,assurveysfromthe regiononlyaccountfor4.1%ofthe Pv PRglobal Table3RobustnessanalysisoftheWilcoxonSignedRanktestsonurban – rural Pv PRvaluepairsderivedfromvarious spatialandtemporallimitsRegion100km5years100km2years50km5years50km2years ZP-valueZP-valueZP-valueZP-value Africa+ Š 5.670<0.001*** Š 5.623<0.001*** Š 5.644<0.001*** Š 5.397<0.001*** Americas2.3070.021**1.6800.094*0.4860.6310.7300.471 Asia+ Š 11.194<0.001*** Š 11.065<0.001*** Š 9.080<0.001*** Š 9.005<0.001*** World Š 11.732<0.001*** Š 11.555<0.001*** Š 10.052<0.001*** Š 9.757<0.001*** No.pairs1,1891,1061,1561,106 MeanNo.R49.65342.28731.81327.061 Overlaprate6.7525.3494.2063.423Africa+=Africa,SaudiArabiaandYemen;Asia+=CentralandSouthEastAsia;MeanNo.R=Meannumberofruralsurveysforeachurban – ruralpair;Overlaprate = numberofruralsurveyspairedtoeachurbansurvey/totalnumberofruralsurveys(***=P<0.01,**=P<0.05,*=P<0.1).Qi etal.MalariaJournal 2012, 11 :403 Page6of11 http://www.malariajournal.com/content/11/1/403

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database.Gettingextremeresultsismorelikelywhen thenumbersofsurveysaresmallandonlytherural Pv PRsurveyswereaveraged.Thereisalsoevidencesuggestingthathighermalariatransmissioninsomeareas ofBrazilwasactuallyaresultofrapidurbanization,duringwhichsettlementswerebuiltclosetoforestboundariesoralongriversidesandthusresultingingreater exposuretothemalariaparasiteforresidents[48]. Figure2indicatesthatconsiderableheterogeneity existswhenexaminingindividualcities,withtwocities (outoftwenty)showingsignificantlylower Pv PRintheir surroundingruralareas,andsevencitiesshowingsignificantlylowerprevalenceinurbanareas.Thus,onlynine ofthetwentycitiesexaminedshowedsignificantdifferencesintransmissionbetweenurbanandruralareas, andthreeshowedzeroprevalencebothwithinand Figure2 Boxplotsshowingthedifferencesin Pv PRvaluesbetweenGRUMP-UEdefinedurbanandruralsurveysforcities. (*)denotes thesignificantlevelofthetestresults(***=P<0.01,**=P<0.05,*=P<0.1). Qi etal.MalariaJournal 2012, 11 :403 Page7of11 http://www.malariajournal.com/content/11/1/403

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aroundtheurbanareas.Comparedto P falciparum [18], therefore,thepatternsof Pv PRbetweenurbanandrural areasexhibitahigherlevelofheterogeneity.Severalpossiblereasonsinclude:1)thewidertransmissionlimitsof P vivax [15],butlowertransmissionintensitywithmany zero Pv PRvaluesinthedatabase;2)thewidedistribution inAsiaandhighprevalenceofDuffynegativityinAfrica [49,50];3)relativelyfewer Pv PRsurveysavailablein theMAPdatabasecomparedwithatotalof22,212 P falciparum parasiterate( Pf PR)surveysin2010[23]. The Pv PRdifferencesbetweenurbanandruralsettings withintherangesofthedominant Anopheles vectors Figure3 Barchartsshowingthetestresultsforthedominant Anopheles vectorsofhumanmalaria. Panel A showstheresultsofWilcoxon SignedRanktestson Pv PRvaluesbetweenGRUMP-UEdefinedurban(U)andrural(R)surveypairsforthedominant Anopheles vectorsofhuman malariainAsia-Pacificregion.Panel B showstheresultsforthedominant Anopheles vectorsinAfrica,EuropeandtheMiddleEast.Panel C shows theresultsofWilcoxonSignedRanktestsforthedominant Anopheles vectorsintheAmericas.(#)denotesthatavectorspeciesisnowrecognized asaspeciescomplex.(*)denotesthesignificantlevelofthetest(***=P<0.01,**=P<0.05,*=P<0.1). Qi etal.MalariaJournal 2012, 11 :403 Page8of11 http://www.malariajournal.com/content/11/1/403

PAGE 9

generallyfollowsthepatternsfoundineachregion.This ispartlybecausevectorspeciesthathadsufficient urban – rural Pv PRpairswithintheirextentsusually coveralargeportionoftheregion.Anissueraisedhere isthatthedistributionsofmostofthevectorspecies overlapsubstantiallywitheachother.Thus,drawingconclusionsaboutthepatternsofindividualvectorspeciesis difficultwithoutconsideringsuchoverlap.However, accordingtoexpert-opiniondistributionmapsofglobal DVS[25-27],thespatialrelationshipsamongthose vectorspeciesareextremelycomplexandtheinteraction effectsofthemarebeyondthescopeofthisanalysis. TheGRUMP-UEwasusedtodefineurbanareashere, thoughseveralalternativeglobalurbanmapsexist[42]. Everyglobalmapsuffersfromdifferenterrorsanduncertainties[42],andtheGRUMP-UEmapexhibitsoverestimationoflargeurbanareaextents,duetothe bloomingeffectofNTLimagery[42,51].Thissuggests thatthe Pv PRurbanvaluesthatweresignificantlyhigher thannearbyruralonesfoundintheAmericasandseveralotherindividualcitiescouldactuallybelocatedin surroundinglowerpopulationdensityareas,assignificantlyhighermalariaprevalenceandentomologicinoculationratesinperi-urbanareascomparedtourban centershavebeenfoundinanumberofstudies [9,13,18].Toassessbrieflythispotentialbiasinthe GRUMP-UEmap,urbanextentsmappedusingModerateResolutionImagingSpectroradiometer(MODIS)satellitesensorimagery[40,41]wereutilizedtoderivean alternative,moreconservative,urbanassignmentforthe Pv PRsurveys.Again,setsofspatiallyandtemporally associatedurban – ruralpairsof Pv PRvalueswere extractedandtested.Theresultsshowthat,duetothe moreconservativenatureoftheclassification,andthe factthatonlyintenselyurbanareasweremapped [40,41],farfewer Pv PRsurveyswereidentifiedasurban andthedifferencesin Pv PRbetweenurbanandrural areasweregenerallynotsignificant(seeAdditionalfile 2).Suchresultshighlightthedifferingoutcomesthatcan occurthroughusingdifferingdefinitionsofurban,and thattheeffectsofurbanizationon P vivax transmission mayextendbeyondthebordersofintenselyurbanareas formostoftheregionsasageneraltrendofdecreased Pv PRwasfoundinurbanareas.Anotherissueisthat theGRUMP-UEmapwasproducedin2004andsome Pv PRsurveysmaybemisclassifiedastheurbanextent changesthroughtime.However,globalurbanmapsthat areupdatedregularlyorthatquantifyurbanextent changedonotcurrentlyexist.Furthermore,themajority ofthe Pv PRsurveyswereconductedbetween2000and 2010(Table1).Thus,itisreasonabletousethesingle time-pointGRUMP-UEmapinthisanalysis. Arangeofhuman-inducedenvironmentalchanges (e.g.,deforestation,urbanization,watercontrolprojects andclimatechange)havebeenidentifiedasdriversof ‘ emerging ’ and ‘ reemerging ’ diseasesandthetransmission ofvector-borneandotherinfectiousdiseases[52-55]. Urbanizationisusuallyrecognizedasoneoftheprimary factorsaffectingvector-bornediseases[56]asitcannot onlyprovideresidentswithbetteraccesstohealthcareand interventions[4,5],andanenvironmentgenerallyless favorableformanydiseasevectors[7,8],butcanalsomodifylandusestoexposehumanstonewpathogensandvectors[57].Whileglobalandregional-scaleresultshere showageneraltrendofdecreased P vivax transmissionin urbanareas,theheterogeneousimpactsofurbanization on P vivax malariatransmissionatthecityscalefoundin theseanalysessupportincreasingconcernsofurbanmalariaproblemsindevelopingcountries.Urbanizationin theseregionsisoftenassociatedwithpoverty,poorwater suppliesandsanitationinperi-urbanareas,providing breadingsitesforcertainvectors[12].Althoughmalaria vectorsaregenerallynotfavouredbyurbanenvironments, thereisevidencehighlightingthepotentialofmalariavectorsinadaptingtourbanenvironments[58-60].Forexample, Anophelesgambiaes s .wasfoundbreedingin pollutedwaterbodiesinLagos,Nigeria[59].Furthermore,manystudiessuggestedthaturbanagricultureisanother importantsourceforprovidingfavourablebreedingsites formalariavectorsincities[61-64].Increasedmalaria prevalenceisoftenfoundincommunitieswithinadistanceof1kmfromirrigatedurbanagricultureinAccra, Ghana[64],forexample.Thus,malariatransmissionin urbanareasexhibitsconsiderablespatialheterogeneity bothbetweenandwithincities,dependingonfactorssuch asproximitytopossiblevectorbreedinghabitats, urbanizationlevelandsocio-economicstatus[7,65].Futureworkshouldaimtoelucidatethesedriversthrough examinationofthedisparityof P vivax malariatransmissionbetweenandwithincitiesusingdetailedhousehold prevalencesurveysandhigherresolutionurbanmaps. Ingeneral,theresultsherehighlightaconsistent relationshipatlargescalesbetweenurbanareasand lower P vivax transmission,mirroringresultsfound for P falciparum ,andpointingtowardsglobaldeclines in P vivax transmissionasurbanizationpermanently altersthereceptivityofmanyareas.Thefindingssuggest thatthesetrendswilllikelycontinuetocatalyzemalaria declinesonthepathtoamalariafreefuture.AdditionalfilesAdditionalfile1: ResultsofWilcoxonSignedRanktestson Pv PR valuesbetweenGRUMP-UEdefinedurban(U)andrural(R)survey pairsforthedominant Anopheles vectorsofhumanmalaria. Additionalfile2: ResultsofWilcoxonSignedRanktestson Pv PR valuesbetweenMODISdefinedurban(U)andrural(R)surveypairs forcontinents,countriesandtheWorld.Qi etal.MalariaJournal 2012, 11 :403 Page9of11 http://www.malariajournal.com/content/11/1/403

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Abbreviations Africa+:Africa,SaudiArabiaandYemen;Asia+:CentralandSouthEastAsia; DVS:Dominantvectorspecies;GRUMP:GlobalRuralUrbanMappingProject; GRUMP-UE:GRUMPurbanextent;MAP:MalariaAtlasProject; Pf PR: P falciparum parasiterate; Pv API: P vivax annualparasiteincidence; Pv PR: P vivax parasiterate; Pv MECs: P vivax malariaendemiccountries. Competinginterests Theauthorsdeclarethattheyhavenocompetinginterests. Authors'contributions AJTconceivedtheanalyses.QQandAJTdevelopedthestudydesignand QQconductedtheanalyses.CAG,CMMandIRFgatheredandprocessedthe malariaprevalencedata.PWG,CAGandSIHundertookconstructionofthe vivaxlimitsanddominantvectorspeciesdataset.Allauthorscontributedto thewritingofthemanuscript.Allauthorsreadandapprovedthefinal manuscript. Acknowledgements Thelargeglobalassemblyofparasiteprevalencedatawascritically dependentonthegenerouscontributionsofdatamadebyalargenumber ofpeopleinthemalariaresearchandcontrolcommunitiesandthese individualsarelistedontheMAPwebsite(http://www.map.ac.uk/ acknowledgements.html).AJTissupportedbygrantsfromtheBilland MelindaGatesFoundation(#49446and#1032350)(http://www. gatesfoundation.org)andNIH/NIAID(U19AI089674).SIHisfundedbya SeniorResearchFellowshipfromtheWellcomeTrust(#095066)thatalso supportsPWG.CLMisfundedbyaBiomedicalResourcesGrantfromthe WellcomeTrust(#091835).IRFEisfundedbygrantsfromtheUniversityof Oxford — LiKaShingFoundationGlobalHealthProgramandtheOxford TropicalNetwork.AJTandSIHalsoacknowledgesupportfromtheRAPIDD programoftheScience&TechnologyDirectorate,DepartmentofHomeland Security,andtheFogartyInternationalCenter,NationalInstitutesofHealth (http://www.fic.nih.gov).ThisworkformspartoftheoutputoftheMalaria AtlasProject(MAP,http://www.map.ox.ac.uk),principallyfundedbythe WellcomeTrust,UK(http://www.wellcome.ac.uk).Thefundershadnorolein studydesign,datacollectionandanalysis,decisiontopublish,orpreparation ofthemanuscript. Authordetails1DepartmentofGeographyandEmergingPathogensInstitute,Universityof Florida,Gainesville,FL,USA.2SpatialEcologyandEpidemiologyGroup, TinbergenBuilding,DepartmentofZoology,UniversityofOxford,South ParksRoad,Oxford,UK.3Eijkman-OxfordClinicalResearchUnit,Jalan DiponegoroNo.69,Jakarta10430,Indonesia.4DepartmentofGeography andEnvironment,UniversityofSouthampton,Highfield,Southampton,UK.5FogartyInternationalCenter,NationalInstitutesofHealth,Bethesda,MD 20892,USA. Received:18August2012Accepted:22November2012 Published:5December2012 References1.UnitedNations: Worldurbanizationprospect,the2011revision .NewYork: UnitedNations;2011. 2.VlahovD,GaleaS: Urbanization,urbanicity,andhealth. JUrbanHealth 2002, 79: S1 – S12. 3.VlahovD,FreudenbergN,ProiettiF,OmpadD,QuinnA,NandiV,GaleaS: Urbanasadeterminantofhealth. JUrbanHealth 2007, 84: 16 – 26. 4.DyeC: Healthandurbanliving. Science 2008, 319: 766 – 769. 5.UtzingerJ,KeiserJ: Urbanizationandtropicalhealth:thenandnow. AnnTropMedParasitol 2006, 100: 517 – 533. 6.MooreM,GouldP,KearyBS: Globalurbanizationandimpactonhealth. IntJHygEnvirHeal 2003, 206: 269 – 278. 7.RobertV,MacintyreK,KeatingJ,TrapeJ-F,DucheminJ-B,WarrenM, BeierJC: Malariatransmissioninurbansub-SaharanAfrica. AmJTropMedHyg 2003, 68: 169 – 176. 8.DonnellyM,McCallPJ,LengelerC,BatesI,D ’ AlessandroU,BarnishG, KonradsenF,KlinkenbergE,TownsonH,TrapeJ-F,HastingsI,MuteroC: Malariaandurbanizationinsub-SaharanAfrica. MalarJ 2005, 4: 12. 9.HaySI,GuerraCA,TatemAJ,AtkinsonPM,SnowRW: Urbanization, malariatransmissionanddiseaseburdeninAfrica. NatRevMicro 2005, 3: 81 – 90. 10.TrapeJF: Malariaandurbanizationincentralafrica:theexampleof brazzaville:partIV.Parasitologicalandserologicalsurveysinurbanand surroundingruralareas. TransRSocTropMedHyg 1987, 81: 26 – 33. 11.TrapeJF,ZoulaniA: MalariaandurbanizationinCentralAfrica:the exampleofBrazzaville:PartIII:Relationshipsbetweenurbanizationand theintensityofmalariatransmission. TransRSocTropMedHyg 1987, 81: 19 – 25. 12.KnudsenAB,SloffR: Vector-bornediseaseproblemsinrapidurbanization: newapproachestovectorcontrol. BullWorldHealthOrgan 1992, 70: 1 – 6. 13.KeiserJ,UtzingerJ,DeCastroMC,SmithTA,TannerM,SingerBH: Urbanizationinsub-SaharanAfricaandimplicationformalariacontrol. AmJTropMedHyg 2004,71: 118 – 127. 14.MendisK,SinaB,MarchesiniP,CarterR: Theneglectedburdenof Plasmodiumvivax malaria. AmJTropMedHyg 2001, 64: 97 – 106. 15.GuerraCA,HowesRE,PatilAP,GethingPW,VanBoeckelTP,TemperleyWH, KabariaCW,TatemAJ,ManhBH,ElyazarIRF,BairdJK,SnowRW,HaySI: Theinternationallimitsandpopulationatriskof plasmodiumvivax transmissionin2009. PLoSNeglTropDis 2010, 4: e774. 16.PriceRN,TjitraE,GuerraCA,YeungS,WhiteNJ,AnsteyNM: Vivaxmalaria: neglectedandnotbenign. AmJTropMedHyg 2007, 77: 79 – 87. 17.BairdJK: Neglectof Plasmodiumvivax malaria. TrendsParasitol 2007, 23: 533 – 539. 18.TatemA,GuerraC,KabariaC,NoorA,HayS: Humanpopulation,urban settlementpatternsandtheirimpacton Plasmodiumfalciparum malaria endemicity. MalarJ 2008, 7: 218. 19.GuerraCA,SnowRW,HaySI: Definingtheglobalspatiallimitsofmalaria transmissionin2005. AdvParasitol 2006, 62: 157 – 179. 20.GuerraCA,SnowRW,HaySI: Mappingtheglobalextentofmalariain 2005. TrendsParasitol 2006, 22: 353 – 358. 21.SnowRW,GuerraCA,NoorAM,MyintHY,HaySI: Theglobaldistribution ofclinicalepisodesof Plasmodiumfalciparum malaria. Nature 2005, 434: 214 – 217. 22.HaySI,GuerraCA,GethingPW,PatilAP,TatemAJ,NoorAM,KabariaCW, ManhBH,ElyazarIRF,BrookerS,SmithDL,MoyeedRA,SnowRW: Aworld malariamap: Plasmodiumfalciparum endemicityin2007. PLoSMed 2009, 6: e1000048. 23.GethingP,PatilA,SmithD,GuerraC,ElyazarI,JohnstonG,TatemA,HayS: Anewworldmalariamap: Plasmodiumfalciparum endemicityin2010. MalarJ 2011, 10: 378. 24.FoleyDH,RuedaLM,WilkersonRC: Insightintoglobalmosquitobiogeographyfromcountryspeciesrecords. JMedEntomol 2007, 44: 554 – 567. 25.SinkaM,BangsM,ManguinS,CoetzeeM,MbogoC,HemingwayJ,PatilA, TemperleyW,GethingP,KabariaC,OkaraR,VanBoeckelT,GodfrayHC, HarbachR,HayS: Thedominant Anophele svectorsofhumanmalariain Africa,EuropeandtheMiddleEast:occurrencedata,distributionmaps andbionomicprecis. ParasitVectors 2010, 3: 117. 26.SinkaM,BangsM,ManguinS,ChareonviriyaphapT,PatilA,TemperleyW, GethingP,ElyazarI,KabariaC,HarbachR,HayS: Thedominant Anopheles vectorsofhumanmalariaintheAsia-Pacificregion:occurrencedata, distributionmapsandbionomicprecis. ParasitVectors 2011, 4: 89. 27.SinkaM,Rubio-PalisY,ManguinS,PatilA,TemperleyW,GethingP,Van BoeckelT,KabariaC,HarbachR,HayS: Thedominant Anopheles vectorsof humanmalariaintheAmericas:occurrencedata,distributionmapsand bionomicprecis. ParasitVectors 2010, 3: 72. 28.SharmaVP: FightingmalariainIndia. Currentsci(Bangalore) 1998, 75: 1127. 29.SurendranSN,RamasamybR: Somecharacteristicsofthelarvalbreeding sitesof Anophelesculicifacies speciesBandEinSriLanka. JVectorDis 2005, 42: 39 – 44. 30.RobertsD: Mosquitoes(Diptera:Culicidae)breedinginbrackishwater: femaleovipositionalpreferencesorlarvalsurvival? JMedEntomol 1996, 33: 525 – 530. 31.BatraCP,MittalPK,AdakT,SubbaraoSK: EfficacyofAgniqueMMF monomolecularsurfacefilmagainst Anophelesstephensi breedingin urbanhabitatsinIndia. JAmMosquitoContr 2006, 22: 426 – 432. 32.BiswasD,DuttaR,GhoshS,ChatterjeeK,HatiA: Breedinghabitsof Anophelesstephensi ListoninanareaofCalcutta. IndianJMalariol 1992, 29: 195 – 198.Qi etal.MalariaJournal 2012, 11 :403 Page10of11 http://www.malariajournal.com/content/11/1/403

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33.GuerraCA,GikandiPW,TatemAJ,NoorAM,SmithDL,HaySI,SnowRW: TheLimitsandintensityof Plasmodiumfalciparum transmission: implicationsformalariacontrolandeliminationworldwide. PLoSMed 2008, 5: e38. 34.MalariaAtlasProject;www.map.ox.ac.uk. 35.GuerraCA,HayS,LucioparedesL,GikandiP,TatemA,NoorA,SnowR: Assemblingaglobaldatabaseofmalariaparasiteprevalenceforthe malariaatlasproject. MalarJ 2007, 6: 17. 36.DankoDM: Thedigitalchartoftheworldproject. PhotogrammEngRemS 1992, 58: 1125 – 1128. 37.BalkDL,DeichmannU,YetmanG,PozziF,HaySI,NelsonA: Determiningglobalpopulationdistribution:methods,applicationsand data. AdvParasitol 2006, 62: 119 – 156. 38.HansenM,DeFriesR,TownshendJRG,SohlbergR: 1kmlandcover classificationderivedfromAVHRR.CollegePark .Maryland:TheGlobalLand CoverFacility;1998. 39.ElvidgeCD,BaughKE,KihnEA,KroehlHW,DavisER: Mappingcitylights withnighttimedatafromtheDMSPoperationallinescansystem. PhotogrammEngRemS 1997, 63: 727 – 734. 40.SchneiderA,FriedlMA,PotereD: Anewmapofglobalurbanextentfrom MODISdata. EnvironResLett 2009, 4: 4. 41.SchneiderA,FriedlMA,PotereD: Monitoringurbanareasgloballyusing MODIS500mdata:Newmethodsanddatasetsbasedonurban ecoregions. RemoteSensEnviron 2010, 114: 1733 – 1746. 42.TatemAJ,NoorAM,HaySI: Assessingtheaccuracyofsatellitederived globalandnationalurbanmapsinKenya. RemoteSensEnviron 2005, 96: 87 – 97. 43.CenterforInternationEarthScienceInformationNetwork(CIESIN),Columbia University: Internationalfoodpolicyresearchinstitute(IFPRI),theworldband, centrointernationaldeagriculturatropical(CIAT) ,Globalrural – urban mappingproject(GRUMP):urbanextents.Palisades,NewYork:CIESIN, ColumbiaUniversity;2004. 44.HaySI,SinkaME,OkaraRM,KabariaCW,MbithiPM,TagoCC,BenzD, GethingPW,HowesRE,PatilAP,TemperleyWH,BangsMJ, ChareonviriyaphapT,ElyazarIRF,HarbachRE,HemingwayJ,ManguinS, MbogoCM,Rubio-PalisY,GodfrayHCJ: Developingglobalmapsofthe dominant Anopheles vectorsofhumanmalaria. PLoSMed 2010, 7: e1000209. 45.GuptaD,BhattR,SharmaR,GautamA,RajnikantAS: Intradomestic mosquitobreedingsourcesandtheirmanagement. IndianJMalariol 1992, 29: 41 – 46. 46.WilcoxonF:Individualcomparisonsbyrankingmethods. Biometrics 1945, 1: 761 – 764. 47.MontgomeryMR: Theurbantransformationofthedevelopingworld. Science 2008, 319: 761 – 764. 48.GoncalvesMJF,AlecrimWD: Non-plannedurbanizationasacontributing factorformalariaincidenceinManaus-Amazonas,Brazil. RevSalud Pblica 2004, 6: 156 – 166. 49.MillerLH,MasonSJ,ClydeDF,McGinnissMH: Theresistancefactorto Plasmodiumvivax inBlacks. NewEnglJMed 1976, 295: 302 – 304. 50.HowesRE,PatilAP,PielFB,NyangiriOA,KabariaCW,GethingPW, ZimmermanPA,BarnadasC,BeallCM,GebremedhinA,MenardD,Williams TN,WeatherallDJ,HaySI: Theglobaldistributionoftheduffyblood group. NatCommun 2011, 2: 266. 51.SuttonPC: Ascale-adjustedmeasureof “ Urbansprawl ” usingnighttime satelliteimagery. RemoteSensEnviron 2003, 86: 353 – 369. 52.WeissRA,McMichaelAJ: Socialandenvironmentalriskfactorsinthe emergenceofinfectiousdiseases. NatMed 2004, 10: 70 – 76. 53.McMichaelAJ: Environmentalandsocialinfluencesonemerging infectiousdiseases:past,presentandfuture. PhilosTransRSocLondBBiol Sci 2004, 359: 1049 – 1058. 54.PatzJA,DaszakP,TaborGM,AguirreAA,PearlM,EpsteinJ,WolfeND, KilpatrickAM,FoufopoulosJ,MolyneuxD,BradleyDJ: Unhealthy landscapes:policyrecommendationsonlandusechangeandinfectious diseaseemergence. EnvironHealthPerspect 2004, 112: 1092 – 1098. 55.VoraN: Impactofanthropogenicenviromentalalterationsonvectorbornediseases. MedscapeJMed 2008, 10: 238. 56.MolyneuxDH: Patternsofchangeinvectorbornediseases. AnnTropMed Parasitol 1997, 91: 827– 840. 57.NorrisDE: Mosquito-bornediseasesasaconsequenceoflanduse change. Ecohealth 2004, 1: 19 – 24. 58.ChineryWA: Effectsofecologicalchangesonthemalariavectors Anophelesfunestus andthe Anophelesgambiae complexofmosquitoes inAccra. Ghana.JTropMedHyg 1984, 87: 191 – 206. 59.AwololaTS,OduolaAO,ObansaJB,ChukwurarNJ,UnyimaduJP: Anophelesgambiaes s .breadinginpollutedwaterbodiesinurban Lagos,southwesternNigeria. JVectorDis 2007, 44: 241 – 244. 60.Antonio-NkondjioC,SimardF,Awono-AmbeneP,NgassamP,TotoJ-C, TchuinkamT,FontenilleD: Malariavectorsandurbanizationinthe equatorialforestregionofsouthCameroon. TransRSocTropMedHyg 2005, 99: 347 – 354. 61.AfraneYA,KlinkenbergE,DrechselP,Owusu-DaakuK,GarmsR,KruppaT: Doesirrigatedurbanagricultureinfluencethetransmissionofmalariain thecityofKumasi,Ghana? ActaTrop 2004, 89: 125 – 134. 62.MatthysB,VounatsouP,RasoG,TschannenAB,BecketEG,GosoniuL, CisseG,TannerM,N ’ goranEK,UtzingerJ: Urbanfarmingandmalariarisk factorsinamedium-sizedtowninCted ’ Ivoire. AmJTropMedHyg 2006, 75: 1223 – 1231. 63.KlinkenbergE,McCallP,WilsonM,AmerasingheF,DonnellyM: Impactof urbanagricultureonmalariavectorsinAccra.Ghana. MalarJ 2008, 7: 151. 64.StolerJ,WeeksJR,GetisA,HillAG: Distancethresholdfortheeffectof urbanagricultureonelevatedself-reportedmalariaprevalenceinAccra. Ghana. AmJTropMedHyg 2009, 80: 547 – 554. 65.MendezF,CarrasquillaG,MuozA: Riskfactorsassociatedwithmalaria infectioninanurbansetting. TransRSocTropMedHyg 2000, 94: 367 – 371.doi:10.1186/1475-2875-11-403 Citethisarticleas: Qi etal. : Theeffectsofurbanizationonglobal Plasmodiumvivax malariatransmission. MalariaJournal 2012 11 :403. Submit your next manuscript to BioMed Central and take full advantage of: € Convenient online submission € Thorough peer review € No space constraints or color “gure charges € Immediate publication on acceptance € Inclusion in PubMed, CAS, Scopus and Google Scholar € Research which is freely available for redistribution Submit your manuscript at www.biomedcentral.com/submit Qi etal.MalariaJournal 2012, 11 :403 Page11of11 http://www.malariajournal.com/content/11/1/403


!DOCTYPE art SYSTEM 'http:www.biomedcentral.comxmlarticle.dtd'
ui 1475-2875-11-403
ji 1475-2875
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dochead Research
bibl
title
p The effects of urbanization on global it Plasmodium vivax malaria transmission
aug
au id A1 ca yes snm Qifnm Qiuyininsr iid I1 email qiuyinqi@ufl.edu
A2 Guerrami ACarlosI2 carlos.guerraloaiza@zoo.ox.ac.uk
A3 MoyesLCatherinecatherine.moyes@zoo.ox.ac.uk
A4 ElyazarFIqbal RI3 iqbal.elyazar@gmail.com
A5 GethingWPeterpeter.gething@zoo.ox.ac.uk
A6 HayISimonI5 simon.hay@zoo.ox.ac.uk
A7 TatemJAndrewI4 andy.tatem@gmail.com
insg
ins Department of Geography and Emerging Pathogens Institute, University of Florida, Gainesville, FL, USA
Spatial Ecology and Epidemiology Group, Tinbergen Building, Department of Zoology, University of Oxford, South Parks Road, Oxford, UK
Eijkman-Oxford Clinical Research Unit, Jalan Diponegoro No. 69, Jakarta, 10430, Indonesia
Department of Geography and Environment, University of Southampton, Highfield, Southampton, UK
Fogarty International Center, National Institutes of Health, Bethesda, MD, 20892, USA
source Malaria Journal
issn 1475-2875
pubdate 2012
volume 11
issue 1
fpage 403
url http://www.malariajournal.com/content/11/1/403
xrefbib pubidlist pubid idtype doi 10.1186/1475-2875-11-403pmpid 23217010
history rec date day 18month 8year 2012acc 22112012pub 5122012
cpyrt 2012collab Qi et al.; licensee BioMed Central Ltd.note This is an Open Access article distributed under the terms of the Creative Commons Attribution License (
http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
kwdg
kwd
Plasmodium vivax
Urbanization
Dominant Anopheles vectors
Mapping
abs
sec
st
Abstract
Background
Many recent studies have examined the impact of urbanization on Plasmodium falciparum malaria endemicity and found a general trend of reduced transmission in urban areas. However, none has examined the effect of urbanization on Plasmodium vivax malaria, which is the most widely distributed malaria species and can also cause severe clinical syndromes in humans. In this study, a set of 10,003 community-based P. vivax parasite rate (PvPR) surveys are used to explore the relationships between PvPR in urban and rural settings.
Methods
The PvPR surveys were overlaid onto a map of global urban extents to derive an urban/rural assignment. The differences in PvPR values between urban and rural areas were then examined. Groups of PvPR surveys inside individual city extents (urban) and surrounding areas (rural) were identified to examine the local variations in PvPR values. Finally, the relationships of PvPR between urban and rural areas within the ranges of 41 dominant Anopheles vectors were examined.
Results
Significantly higher PvPR values in rural areas were found globally. The relationship was consistent at continental scales when focusing on Africa and Asia only, but in the Americas, significantly lower values of PvPR in rural areas were found, though the numbers of surveys were small. Moreover, except for the countries in the Americas, the same trends were found at national scales in African and Asian countries, with significantly lower values of PvPR in urban areas. However, the patterns at city scales among 20 specific cities where sufficient data were available were less clear, with seven cities having significantly lower PvPR values in urban areas and two cities showing significantly lower PvPR in rural areas. The urban–rural PvPR differences within the ranges of the dominant Anopheles vectors were generally, in agreement with the regional patterns found.
Conclusions
Except for the Americas, the patterns of significantly lower P. vivax transmission in urban areas have been found globally, regionally, nationally and by dominant vector species here, following trends observed previously for P. falciparum. To further understand these patterns, more epidemiological, entomological and parasitological analyses of the disease at smaller spatial scales are needed.
bdy
Background
The world population has undergone unprecedented growth along with rapid urbanization. Slightly more than 50% of the population (3.6 billion) is now living in urban areas compared to only 30% (0.7 billion) in 1950
abbrgrp
abbr bid B1 1
. By 2050, it is projected that urban dwellers will account for approximately 67% (6.3 billion) of the world total population, while most of the estimated growth will be concentrated in less developed regions, particularly in Asia and Africa
1
. These substantial transitions have significant public health implications associated with changes in the social and physical environment and access to public health services
B2 2
B3 3
B4 4
B5 5
B6 6
.
Although large heterogeneity exists, it is commonly accepted that the process of urbanization reduces malaria transmission, primarily because urban environments (e.g. the lack of suitable breeding sites, the pollution of existing larval habitats, etc.) are generally unsuitable for malaria vectors
B7 7
B8 8
B9 9
. Other explanations include better access to health care services and an increased ratio of humans to mosquitoes
7
B10 10
B11 11
. However, there is concern regarding urban malaria in less developed regions, typically those undergoing rapid and unprecedented urbanization
B12 12
B13 13
.
Between the two dominant parasite species of human malaria, Plasmodium falciparum has attracted the focus of most research because of its high mortality and intensive transmission in Africa
B14 14
. Plasmodium vivax malaria, in contrast, is commonly considered as a “benign” infection and largely overlooked by researchers, government, and funding agencies. Increasing evidence has shown that P. vivax is neither rare nor benign, however. It is estimated that 2.85 billion people were at risk of P. vivax infection in 2009, with 91% (2.59 billion) of them living in Central and South East Asia
B15 15
, and that P. vivax is the most widely distributed (geographically) malaria species of humans. Furthermore, although the infection with P. vivax malaria is rarely directly fatal, it can cause severe clinical syndromes
B16 16
B17 17
.
Recent studies have examined the impact of urbanization on P. falciparum malaria endemicity and disease burden estimation
7
8
9
13
B18 18
. Various urban extent maps have been used to compare the differences in P. falciparum malaria endemicity between urban settlements and rural areas
18
; exclude the urban extents of cities identified as malaria free in the mapping of malaria transmission limits
B19 19
B20 20
; downgrade endemic classes in estimates of malaria burden
9
B21 21
; and predict P. falciparum malaria endemicity based on geo-statistical models
B22 22
B23 23
. However, according to our best knowledge, no known research has examined the effect of urbanization on P. vivax malaria over similarly large scales. In addition, the regions of highest P. vivax transmission in Asia are composed of a considerably greater range of vector species and species complexes than seen in Africa, where P. falciparum transmission is princi-pally concentrated
B24 24
B25 25
B26 26
B27 27
, and urbanization may impact each of these vector species differently, dependent on their preferences and bionomics. For example, Anopheles culicifacies was reported to be the vector responsible for 60-65% malaria cases in urban environments of India
B28 28
and shows significant environment tolerance and adaptability
B29 29
B30 30
, while larvae of Anopheles stephensi were found in various domestic containers and collections of water related to construction and industrial sites in cities
B31 31
B32 32
. Therefore, there is a need to examine the effects of urbanization on P. vivax transmission by dominant vector species to discern whether differential impacts are evident.
Here geo-referenced P. vivax parasite rate (PvPR) surveys and urban extent maps are integrated to examine the impact of urbanization on P. vivax malaria transmission at various spatial scales (global, regional, national and at the city level). Furthermore, distribution maps of dominant Anopheles vectors are used to explore the relationships between urbanization, Anopheles vectors and P. vivax malaria transmission.
Methods
Datasets
The MAP PvPR database
As with P. falciparum malaria, parasite rate (PR) is the most commonly reported and consistent metric of P. vivax malaria endemicity
B33 33
. A total of 10,003 community-based P. vivax parasite rate (PvPR) surveys taken between 1985 and 2010 were obtained by the Malaria Atlas Project (MAP
B34 34
). The logistically intensive process of searching for, identifying and geo-locating the PvPR surveys has been documented elsewhere
B35 35
. All these PvPR surveys were geo-referenced to precise locations and not duplicated within three months at the same site. A summary of some of the key features of the PvPR survey data is presented in Table 
tblr tid T1 1. Of the surveys, 410 (4.1%) were in the Americas, 1,651 (16.5%) in Africa, Saudi Arabia and Yemen (Africa+), and 7,942 (79.4%) in Central and South East Asia (Asia+). Approximately half (51%) of the PvPR values are zero and the majority of the surveys were undertaken after 2000. The sample sizes of these surveys varies, with most of them (76%) are being larger than 50. Among the 95 P. vivax malaria endemic countries (PvMECs)
15
, PvPR data were available for 53 (12 in the Americas, 19 in Africa+ and 22 in Asia+). There are 8,588 discrete PvPR survey locations and the distribution of them are shown in Figure 
figr fid F1 1, overlaid on the international limits of P. vivax malaria transmission
15
, with most of the survey points located in Southeast Asia and the Horn of Africa.
table
Table 1
caption
b Summary of the
Pv
PR surveys by region
tgroup align left cols 5
colspec center colname c1 colnum 1 colwidth 1*
c2 2
c3 3
c4 4
c5
thead valign top
row rowsep
entry
Africa+
Americas
Asia+
Total
tfoot
Africa+ =Africa, Saudi Arabia and Yemen; Asia+ =Central and South East Asia.
tbody
Pv
PR values
Number of zero records
1,299
193
3,631
5,123
Mean PvPR (%)
char .
0.60
3.25
3.55
3.05
Median PvPR (%)
0.00
0.61
0.51
0.00
Time period of surveys
1985-1999
225
223
1,328
1,776
2000-2010
1,426
187
6,614
8,227
Sample size
1-50
911
151
1,316
2,378
>50
740
259
6,626
7,625
Median (IQR)
48 (34–109)
87 (37–210)
120 (67–281)
107 (53–236)
Records of surveys
GRUMP-UE defined urban
444
61
755
1,260
GRUMP-UE defined rural
1,203
349
7,241
8,743
Discrete geographic locations
1,424
291
6,873
8,588
Total
1,651
410
7,942
10,003
fig Figure 1The global spatial limits of P. vivax malaria transmission in 2009
15text
The global spatial limits of P .vivax malaria transmission in 2009[15]. Panel A shows the spatial limits of P. vivax malaria risk defined by P. vivax annual parasite incidence (PvAPI) data. Areas were defined as stable (dark grey, where PvAPI ≥0.1 per 1,000 pa), unstable (medium grey, where PvAPI < 0.1 per 1,000 pa) and no risk (light grey, where PvAPI = 0 per 1,000 pa). The community-based PvPR surveys are plotted and colored based on their values (red, where PvPR 7%; yellow, 3% < itPv/itPR <7%; light blue, itPv/itPR < 3%) with zero-valued surveys shown in white. Panel bB/b and Panel bC/b are close-ups for regions with plenty of itPv/itPR surveys with Panel B showing the area around Jakarta, Indonesia and Panel bC/b showing the areas around Sorong, Indonesia./p
/textgraphic file="1475-2875-11-403-1"//fig
/sec
sec
st
pGlobal urban map/p
/st
pAlthough urbanization has been one of the most important transformations of our world for decades, there is still little consensus on the definitions of what consists an urban area and urbanization among national and international bodies
abbrgrp
abbr bid="B2"2/abbr
/abbrgrp. Such ambiguity has lead to the construction of several global urban maps (e.g., Digital Chart of the World (DCW)
abbrgrp
abbr bid="B36"36/abbr
/abbrgrp, Global Rural Urban Mapping Project (GRUMP)
abbrgrp
abbr bid="B37"37/abbr
/abbrgrp, Advanced Very High Resolution Radiometer (AVHRR) Global Land Cover Classification urban land cover class
abbrgrp
abbr bid="B38"38/abbr
/abbrgrp, Defense Meteorological Satellite Program-Operational Linescan System (DMSP-OLS)
abbrgrp
abbr bid="B39"39/abbr
/abbrgrp, and Moderate Resolution Imaging Spectroradiometer (MODIS) Land Cover Product Binary Data
abbrgrp
abbr bid="B40"40/abbr
abbr bid="B41"41/abbr
/abbrgrp) derived from satellite imagery
abbrgrp
abbr bid="B42"42/abbr
/abbrgrp. As discussed in Tatem et al.
abbrgrp
abbr bid="B42"42/abbr
/abbrgrp, all of these global urban maps demonstrated a different range of inaccuracies and limitations, however, the GRUMP urban extent map was considered to be most accurate in matching original urban assignments of itP/it. itfalciparum/it malaria surveys
abbrgrp
abbr bid="B18"18/abbr
/abbrgrp. Therefore, the GRUMP urban extent (GRUMP-UE) map was used here to distinguish itPv/itPR surveys taken in urban areas from those in rural areas. This urban extent map was developed by the Centre for International Earth Science Information Network (CIESIN) at 1 km × 1 km spatial resolution in 2004, utilizing information from satellite night-time lights (NTL), Landsat satellite sensor imagery and other geographical data
abbrgrp
abbr bid="B43"43/abbr
/abbrgrp./p
/sec
sec
st
pDominant itAnopheles/it vector maps/p
/st
pThe distributions and bionomics of dominant itAnopheles/it vectors play an important role in malaria transmission and are the targets of vector control
abbrgrp
abbr bid="B44"44/abbr
/abbrgrp. Vector species normally display a range of ecological and behavioural characteristics. For example, unlike other malaria vectors, an urban environment is favored by the “urban vector” itAnopheles stephensi/it
abbrgrp
abbr bid="B45"45/abbr
/abbrgrp. To assess the impact of urbanization on itP/it. itvivax/it malaria transmission by dominant itAnopheles/it vectors, expert-opinion distribution maps of global dominant vector species (DVS) of malaria were obtained from the Malaria Atlas Project
abbrgrp
abbr bid="B25"25/abbr
abbr bid="B26"26/abbr
abbr bid="B27"27/abbr
abbr bid="B34"34/abbr
/abbrgrp. These maps were constructed through exhaustive searches of literature and refinement through opinion and experience by itAnopheles/it experts
abbrgrp
abbr bid="B27"27/abbr
/abbrgrp. A total of 41 maps of DVS were available, of which, 19 were in the Asia-Pacific region
abbrgrp
abbr bid="B26"26/abbr
/abbrgrp, 13 in Africa, Europe and the Middle East
abbrgrp
abbr bid="B25"25/abbr
/abbrgrp, and nine in the Americas
abbrgrp
abbr bid="B27"27/abbr
/abbrgrp./p
/sec
/sec
sec
st
pAnalysis/p
/st
sec
st
pUrbanization and itP/it. itvivax/it malaria transmission/p
/st
pTo quantify the patterns of itP/it. itvivax/it malaria transmission between urban and rural areas at global, regional and national scales, sets of spatially and temporally associated urban–rural pairs of itPv/itPR values were obtained and tested. Firstly, all the geo-referenced itPv/itPR surveys were overlaid onto the GRUMP-UE map to derive an urbanrural assignment. Following previous approaches
abbrgrp
abbr bid="B18"18/abbr
/abbrgrp, for each itPv/itPR survey assigned as urban, all the rural itPv/itPR surveys taken within 100 km and five years were identified. Then, the identified rural itPv/itPR values were averaged and assigned to that urban itPv/itPR survey to make spatially and temporally associated urban–rural itPv/itPR value pairs
abbrgrp
abbr bid="B18"18/abbr
/abbrgrp. Given the highly skewed distribution of itPv/itPR values in the MAP database
abbrgrp
abbr bid="B35"35/abbr
/abbrgrp, the Wilcoxon Signed Rank
abbrgrp
abbr bid="B46"46/abbr
/abbrgrp, a nonparametric test for paired variables, was used to determine if significant differences between itPv/itPR values in urban and rural areas existed. These tests were undertaken globally, by region (Africa+, Americas, Asia+) and by country (those for which at least ten urban–rural itPv/itPR survey pairs existed) to examine if the patterns of itP/it. itvivax/it malaria transmission between urban and rural areas were significant./p
pAs the choice of spatial and temporal limits (100 km and five years) is arbitrary in obtaining urban–rural pairs of itPv/itPR values, a robustness analysis was conducted. Sets of urban–rural itPv/itPR pairs were obtained through applying various spatial and temporal limits (100 km and two years; 50 km and five years; 50 km and two years), and tested under the Wilcoxon Signed Rank test, respectively. In addition, the mean number of rural surveys paired to each urban survey and the overlap rate (∑ number of rural surveys paired to each urban surveytotal number of rural surveys) for each spatial and temporal limit were calculated to assess the effects of overlapping rural surveys in the sample pairs./p
pTo examine local variations (city scale) in itPv/itPR, groups of itPv/itPR surveys inside individual city extents (urban) and surrounding areas (rural) were identified and tested. Cities where more than eight itPv/itPR surveys (to provide a reasonable number of cities for testing) fell inside their urban extents were first identified. For each city, rural itPv/itPR surveys that fell within 100 km of the centroid of the urban extent were found and assigned to that city. Following this, for each city, itPv/itPR values within its urban extent and surrounding rural area were compared and tested using the Wilcoxon Rank Sum test./p
/sec
sec
st
pDominant itAnopheles/it vectors/p
/st
pThe impact of urbanization on malaria endemicity may vary by dominant itAnopheles/it vectors of human malaria. To test this, itPv/itPR values between urban and rural areas within the extents of 41 dominant itAnopheles/it vector were examined./p
pSets of spatially and temporally associated urban–rural pairs of itPv/itPR values within the extents of each dominant itAnopheles/it vector were extracted and tested separately. The geo-referenced itPv/itPR surveys were firstly overlaid onto the GRUMP-UE map to derive an urbanrural assignment. For each dominant itAnopheles/it vector, all the itPv/itPR surveys that fell within its extent were extracted. For each urban itPv/itPR survey, all of the rural itPv/itPR surveys taken within 100 km and five years were again identified, averaged and assigned to that urban itPv/itPR survey to make a set of spatially and temporally associated urban–rural itPv/itPR value pairs
abbrgrp
abbr bid="B18"18/abbr
/abbrgrp. This set of urban–rural itPv/itPR value pairs were then subject to the Wilcoxon Signed Rank test to determine if significant differences in itPv/itPR between urban and rural areas existed./p
/sec
/sec
/sec
sec
st
pResults/p
/st
sec
st
pUrbanization and itP/it. itvivax/it malaria transmission/p
/st
pAmong the itPv/itPR surveys, 1,260 were classified as urban and 8,743 were classified as rural based on the GRUMP-UE map (Table 
tblr tid="T1"1/tblr). The mean sample size was 278 for the urban surveys and 230 for the rural surveys, which are comparable. Table 
tblr tid="T2"2/tblr shows the results of the Wilcoxon Signed Rank tests between urban and rural pairs of itPv/itPR values defined by GRUMP-UE. Significantly higher itPv/itPR values in rural areas were found globally and in the Africa+ and Asia+ regions, while in the Americas, significantly lower values of itPv/itPR in rural areas were found. The itZ/it values indicate, however, that the differences observed in the Americas are weaker than in other regions. Moreover, the numbers of surveys available were much smaller in the Americas./p
table id="T2"
title
pTable 2/p
/title
caption
p
bResults of Wilcoxon Signed Rank tests on /bb
itPv/it
/bbPR values between GRUMP-UE defined urban (U) and rural (R) survey pairs for countries, regions and the World/b
/p
/caption
tgroup align="left" cols="8"
colspec align="center" colname="c1" colnum="1" colwidth="1*"/
colspec align="center" colname="c2" colnum="2" colwidth="1*"/
colspec align="center" colname="c3" colnum="3" colwidth="1*"/
colspec align="center" colname="c4" colnum="4" colwidth="1*"/
colspec align="center" colname="c5" colnum="5" colwidth="1*"/
colspec align="center" colname="c6" colnum="6" colwidth="1*"/
colspec align="center" colname="c7" colnum="7" colwidth="1*"/
colspec align="center" colname="c8" colnum="8" colwidth="1*"/
thead valign="top"
row rowsep="1"
entry align="center" colname="c1" morerows="1"
p
bRegion/b
/p
/entry
entry align="center" colname="c2" morerows="1"
p
bNo. pairs/b
/p
/entry
entry align="center" colname="c3" nameend="c4" namest="c3"
p
bU > R/b
/p
/entry
entry align="center" colname="c5" nameend="c6" namest="c5"
p
bU < R/b
/p
/entry
entry align="center" colname="c7" morerows="1"
p
bZ/b
/p
/entry
entry align="center" colname="c8" morerows="1"
p
bP-value/b
/p
/entry
/row
row rowsep="1"
entry align="center" colname="c3"
p
bNo. pairs/b
/p
/entry
entry align="center" colname="c4"
p
bRank sum/b
/p
/entry
entry align="center" colname="c5"
p
bNo. pairs/b
/p
/entry
entry align="center" colname="c6"
p
bRank sum/b
/p
/entry
/row
/thead
tfoot
pAfrica+ =Africa, Saudi Arabia and Yemen; Asia+ =Central and South East Asia (*** = P < 0.01, ** = P < 0.05, * = P < 0.1)./p
/tfoot
tbody valign="top"
row rowsep="1"
entry colname="c1"
p
bAfrica+/b
/p
/entry
entry align="center" colname="c2"
p
b428/b
/p
/entry
entry align="center" colname="c3"
p
b33/b
/p
/entry
entry align="center" colname="c4"
p
b1,432/b
/p
/entry
entry align="center" colname="c5"
p
b86/b
/p
/entry
entry align="center" colname="c6"
p
b5,708/b
/p
/entry
entry align="center" colname="c7"
p
b−5.670/b
/p
/entry
entry align="center" colname="c8"
p
b<0.001***/b
/p
/entry
/row
row rowsep="1"
entry align="center" colname="c1"
pEthiopia/p
/entry
entry align="center" colname="c2"
p80/p
/entry
entry align="center" colname="c3"
p18/p
/entry
entry align="center" colname="c4"
p587/p
/entry
entry align="center" colname="c5"
p61/p
/entry
entry align="center" colname="c6"
p2,573/p
/entry
entry align="center" colname="c7"
p−4.853/p
/entry
entry align="center" colname="c8"
p<0.001***/p
/entry
/row
row rowsep="1"
entry align="center" colname="c1"
pSudan/p
/entry
entry align="center" colname="c2"
p192/p
/entry
entry align="center" colname="c3"
p7/p
/entry
entry align="center" colname="c4"
p47/p
/entry
entry align="center" colname="c5"
p9/p
/entry
entry align="center" colname="c6"
p89/p
/entry
entry align="center" colname="c7"
p−1.086/p
/entry
entry align="center" colname="c8"
p0.286/p
/entry
/row
row rowsep="1"
entry align="center" colname="c1"
pYemen/p
/entry
entry align="center" colname="c2"
p35/p
/entry
entry align="center" colname="c3"
p7/p
/entry
entry align="center" colname="c4"
p41/p
/entry
entry align="center" colname="c5"
p13/p
/entry
entry align="center" colname="c6"
p169/p
/entry
entry align="center" colname="c7"
p−2.389/p
/entry
entry align="center" colname="c8"
p0.018**/p
/entry
/row
row rowsep="1"
entry align="center" colname="c1"
pOther countries/p
/entry
entry align="center" colname="c2"
p13/p
/entry
entry align="center" colname="c3"
p1/p
/entry
entry align="center" colname="c4"
p2/p
/entry
entry align="center" colname="c5"
p3/p
/entry
entry align="center" colname="c6"
p8/p
/entry
entry align="center" colname="c7"
p−1.095/p
/entry
entry align="center" colname="c8"
p0.361/p
/entry
/row
row rowsep="1"
entry colname="c1"
p
bAmericas/b
/p
/entry
entry align="center" colname="c2"
p
b49/b
/p
/entry
entry align="center" colname="c3"
p
b23/b
/p
/entry
entry align="center" colname="c4"
p
b636/b
/p
/entry
entry align="center" colname="c5"
p
b19/b
/p
/entry
entry align="center" colname="c6"
p
b263/b
/p
/entry
entry align="center" colname="c7"
p
b2.307/b
/p
/entry
entry align="center" colname="c8"
p
b0.021**/b
/p
/entry
/row
row rowsep="1"
entry align="center" colname="c1"
pBrazil/p
/entry
entry align="center" colname="c2"
p22/p
/entry
entry align="center" colname="c3"
p15/p
/entry
entry align="center" colname="c4"
p135/p
/entry
entry align="center" colname="c5"
p3/p
/entry
entry align="center" colname="c6"
p36/p
/entry
entry align="center" colname="c7"
p2.156/p
/entry
entry align="center" colname="c8"
p0.032**/p
/entry
/row
row rowsep="1"
entry align="center" colname="c1"
pMexico/p
/entry
entry align="center" colname="c2"
p10/p
/entry
entry align="center" colname="c3"
p1/p
/entry
entry align="center" colname="c4"
p10/p
/entry
entry align="center" colname="c5"
p9/p
/entry
entry align="center" colname="c6"
p45/p
/entry
entry align="center" colname="c7"
p−1.784/p
/entry
entry align="center" colname="c8"
p0.067*/p
/entry
/row
row rowsep="1"
entry align="center" colname="c1"
pOther countries/p
/entry
entry align="center" colname="c2"
p17/p
/entry
entry align="center" colname="c3"
p7/p
/entry
entry align="center" colname="c4"
p72/p
/entry
entry align="center" colname="c5"
p7/p
/entry
entry align="center" colname="c6"
p33/p
/entry
entry align="center" colname="c7"
p1.224/p
/entry
entry align="center" colname="c8"
p0.232/p
/entry
/row
row rowsep="1"
entry colname="c1"
p
bAsia+/b
/p
/entry
entry align="center" colname="c2"
p
b712/b
/p
/entry
entry align="center" colname="c3"
p
b127/b
/p
/entry
entry align="center" colname="c4"
p
b50,971/b
/p
/entry
entry align="center" colname="c5"
p
b517/b
/p
/entry
entry align="center" colname="c6"
p
b156,719/b
/p
/entry
entry align="center" colname="c7"
p
b−11.194/b
/p
/entry
entry align="center" colname="c8"
p
b<0.001***/b
/p
/entry
/row
row rowsep="1"
entry align="center" colname="c1"
pAfghanistan/p
/entry
entry align="center" colname="c2"
p68/p
/entry
entry align="center" colname="c3"
p23/p
/entry
entry align="center" colname="c4"
p1,023/p
/entry
entry align="center" colname="c5"
p42/p
/entry
entry align="center" colname="c6"
p1,122/p
/entry
entry align="center" colname="c7"
p−0.323/p
/entry
entry align="center" colname="c8"
p0.749/p
/entry
/row
row rowsep="1"
entry align="center" colname="c1"
pBangladesh/p
/entry
entry align="center" colname="c2"
p27/p
/entry
entry align="center" colname="c3"
p1/p
/entry
entry align="center" colname="c4"
p27/p
/entry
entry align="center" colname="c5"
p26/p
/entry
entry align="center" colname="c6"
p351/p
/entry
entry align="center" colname="c7"
p−3.892/p
/entry
entry align="center" colname="c8"
p<0.001***/p
/entry
/row
row rowsep="1"
entry align="center" colname="c1"
pChina/p
/entry
entry align="center" colname="c2"
p26/p
/entry
entry align="center" colname="c3"
p8/p
/entry
entry align="center" colname="c4"
p146/p
/entry
entry align="center" colname="c5"
p18/p
/entry
entry align="center" colname="c6"
p205/p
/entry
entry align="center" colname="c7"
p−0.749/p
/entry
entry align="center" colname="c8"
p0.461/p
/entry
/row
row rowsep="1"
entry align="center" colname="c1"
pIndonesia/p
/entry
entry align="center" colname="c2"
p462/p
/entry
entry align="center" colname="c3"
p74/p
/entry
entry align="center" colname="c4"
p18,926/p
/entry
entry align="center" colname="c5"
p328/p
/entry
entry align="center" colname="c6"
p62,077/p
/entry
entry align="center" colname="c7"
p−9.256/p
/entry
entry align="center" colname="c8"
p<0.001***/p
/entry
/row
row rowsep="1"
entry align="center" colname="c1"
pIndia/p
/entry
entry align="center" colname="c2"
p26/p
/entry
entry align="center" colname="c3"
p4/p
/entry
entry align="center" colname="c4"
p60/p
/entry
entry align="center" colname="c5"
p22/p
/entry
entry align="center" colname="c6"
p291/p
/entry
entry align="center" colname="c7"
p−2.933/p
/entry
entry align="center" colname="c8"
p0.003***/p
/entry
/row
row rowsep="1"
entry align="center" colname="c1"
pCambodia/p
/entry
entry align="center" colname="c2"
p12/p
/entry
entry align="center" colname="c3"
p1/p
/entry
entry align="center" colname="c4"
p6/p
/entry
entry align="center" colname="c5"
p11/p
/entry
entry align="center" colname="c6"
p72/p
/entry
entry align="center" colname="c7"
p−2.589/p
/entry
entry align="center" colname="c8"
p0.007***/p
/entry
/row
row rowsep="1"
entry align="center" colname="c1"
pNepal/p
/entry
entry align="center" colname="c2"
p18/p
/entry
entry align="center" colname="c3"
p2/p
/entry
entry align="center" colname="c4"
p35/p
/entry
entry align="center" colname="c5"
p16/p
/entry
entry align="center" colname="c6"
p136/p
/entry
entry align="center" colname="c7"
p−2.199/p
/entry
entry align="center" colname="c8"
p0.021**/p
/entry
/row
row rowsep="1"
entry align="center" colname="c1"
pPakistan/p
/entry
entry align="center" colname="c2"
p11/p
/entry
entry align="center" colname="c3"
p6/p
/entry
entry align="center" colname="c4"
p38/p
/entry
entry align="center" colname="c5"
p5/p
/entry
entry align="center" colname="c6"
p28/p
/entry
entry align="center" colname="c7"
p0.444/p
/entry
entry align="center" colname="c8"
p0.700/p
/entry
/row
row rowsep="1"
entry align="center" colname="c1"
pThailand/p
/entry
entry align="center" colname="c2"
p12/p
/entry
entry align="center" colname="c3"
p1/p
/entry
entry align="center" colname="c4"
p2/p
/entry
entry align="center" colname="c5"
p11/p
/entry
entry align="center" colname="c6"
p76/p
/entry
entry align="center" colname="c7"
p−2.903/p
/entry
entry align="center" colname="c8"
p0.001***/p
/entry
/row
row rowsep="1"
entry align="center" colname="c1"
pVietnam/p
/entry
entry align="center" colname="c2"
p23/p
/entry
entry align="center" colname="c3"
p0/p
/entry
entry align="center" colname="c4"
p0/p
/entry
entry align="center" colname="c5"
p21/p
/entry
entry align="center" colname="c6"
p231/p
/entry
entry align="center" colname="c7"
p−4.014/p
/entry
entry align="center" colname="c8"
p<0.001***/p
/entry
/row
row rowsep="1"
entry align="center" colname="c1"
pOther countries/p
/entry
entry align="center" colname="c2"
p29/p
/entry
entry align="center" colname="c3"
p7/p
/entry
entry align="center" colname="c4"
p124/p
/entry
entry align="center" colname="c5"
p17/p
/entry
entry align="center" colname="c6"
p176/p
/entry
entry align="center" colname="c7"
p−0.743/p
/entry
entry align="center" colname="c8"
p0.466/p
/entry
/row
row rowsep="1"
entry align="center" colname="c1"
p
bWorld/b
/p
/entry
entry align="center" colname="c2"
p
b1,189/b
/p
/entry
entry align="center" colname="c3"
p
b183/b
/p
/entry
entry align="center" colname="c4"
p
b84,784/b
/p
/entry
entry align="center" colname="c5"
p
b622/b
/p
/entry
entry align="center" colname="c6"
p
b239,631/b
/p
/entry
entry align="center" colname="c7"
p
b−11.732/b
/p
/entry
entry align="center" colname="c8"
p
b<0.001***/b
/p
/entry
/row
/tbody
/tgroup
/table
pThose countries with at least ten urban–rural itPv/itPR value pairs and the other countries combined for each region (Africa+, Americas and Asia+) were tested further and the results are presented in Table 
tblr tid="T2"2/tblr. The trends found in most of the countries in Africa+ (Ethiopia, Yemen) and Asia+ (Bangladesh, Indonesia, India, Cambodia, Nepal, Thailand, Vietnam) were consistent with the global and regional findings, with significantly lower values of itPv/itPR in urban areas. The relationships found between urban and rural itPv/itPR values for the other countries in Africa+ (Sudan and other African countries) and Asia+ (Afghanistan, China, Pakistan and other Asian countries) were not significant. There are two countries (Ghana and Zambia) in Africa that have sufficient itPv/itPR surveys but are of entirely zero values, so were not listed. The results for the Americas are certainly not as conclusive as the relationships found in the other regions, with one country (Brazil) showing significant higher urban itPv/itPR values, another country (Mexico) showing the reverse and the other American countries showing insignificant differences, though each were only based on a small number of itPv/itPR pairs./p
pThe robustness analysis (Table 
tblr tid="T3"3/tblr) suggests that the overlap rate of rural surveys decreases as the spatial and temporal limits contract, while the patterns of itPv/itPR between urban and rural areas at global and regional scales are generally consistent. Thus, the method used to determine the relationship of itP/it. itvivax/it malaria transmission between urban and rural areas is robust and the effects of overlapping rural surveys on the results are minimal./p
table id="T3"
title
pTable 3/p
/title
caption
p
bRobustness analysis of the Wilcoxon Signed Rank tests on urban–rural /bb
itPv/it
/bbPR value pairs derived from various spatial and temporal limits/b
/p
/caption
tgroup align="left" cols="9"
colspec align="center" colname="c1" colnum="1" colwidth="1*"/
colspec align="center" colname="c2" colnum="2" colwidth="1*"/
colspec align="center" colname="c3" colnum="3" colwidth="1*"/
colspec align="center" colname="c4" colnum="4" colwidth="1*"/
colspec align="center" colname="c5" colnum="5" colwidth="1*"/
colspec align="center" colname="c6" colnum="6" colwidth="1*"/
colspec align="center" colname="c7" colnum="7" colwidth="1*"/
colspec align="center" colname="c8" colnum="8" colwidth="1*"/
colspec align="center" colname="c9" colnum="9" colwidth="1*"/
thead valign="top"
row rowsep="1"
entry align="center" colname="c1" morerows="1"
p
bRegion/b
/p
/entry
entry align="center" colname="c2" nameend="c3" namest="c2"
p
b100 km 5 years/b
/p
/entry
entry align="center" colname="c4" nameend="c5" namest="c4"
p
b100 km 2 years/b
/p
/entry
entry align="center" colname="c6" nameend="c7" namest="c6"
p
b50 km 5 years/b
/p
/entry
entry align="center" colname="c8" nameend="c9" namest="c8"
p
b50 km 2 years/b
/p
/entry
/row
row rowsep="1"
entry align="center" colname="c2"
p
bZ/b
/p
/entry
entry align="center" colname="c3"
p
bP-value/b
/p
/entry
entry align="center" colname="c4"
p
bZ/b
/p
/entry
entry align="center" colname="c5"
p
bP-value/b
/p
/entry
entry align="center" colname="c6"
p
bZ/b
/p
/entry
entry align="center" colname="c7"
p
bP-value/b
/p
/entry
entry align="center" colname="c8"
p
bZ/b
/p
/entry
entry align="center" colname="c9"
p
bP-value/b
/p
/entry
/row
/thead
tfoot
pAfrica+ =Africa, Saudi Arabia and Yemen; Asia+ =Central and South East Asia; Mean No. R = Mean number of rural surveys for each urban–rural pair; Overlap rate = Σ number of rural surveys paired to each urban surveytotal number of rural surveys (*** = P < 0.01, ** = P < 0.05, * = P < 0.1)./p
/tfoot
tbody valign="top"
row rowsep="1"
entry align="center" colname="c1"
pAfrica+/p
/entry
entry align="center" colname="c2"
p−5.670/p
/entry
entry align="center" colname="c3"
p<0.001***/p
/entry
entry align="center" colname="c4"
p−5.623/p
/entry
entry align="center" colname="c5"
p<0.001***/p
/entry
entry align="center" colname="c6"
p−5.644/p
/entry
entry align="center" colname="c7"
p<0.001***/p
/entry
entry align="center" colname="c8"
p−5.397/p
/entry
entry align="center" colname="c9"
p<0.001***/p
/entry
/row
row rowsep="1"
entry align="center" colname="c1"
pAmericas/p
/entry
entry align="center" colname="c2"
p2.307/p
/entry
entry align="center" colname="c3"
p0.021**/p
/entry
entry align="center" colname="c4"
p1.680/p
/entry
entry align="center" colname="c5"
p0.094*/p
/entry
entry align="center" colname="c6"
p0.486/p
/entry
entry align="center" colname="c7"
p0.631/p
/entry
entry align="center" colname="c8"
p0.730/p
/entry
entry align="center" colname="c9"
p0.471/p
/entry
/row
row rowsep="1"
entry align="center" colname="c1"
pAsia+/p
/entry
entry align="center" colname="c2"
p−11.194/p
/entry
entry align="center" colname="c3"
p<0.001***/p
/entry
entry align="center" colname="c4"
p−11.065/p
/entry
entry align="center" colname="c5"
p<0.001***/p
/entry
entry align="center" colname="c6"
p−9.080/p
/entry
entry align="center" colname="c7"
p<0.001***/p
/entry
entry align="center" colname="c8"
p−9.005/p
/entry
entry align="center" colname="c9"
p<0.001***/p
/entry
/row
row rowsep="1"
entry align="center" colname="c1"
pWorld/p
/entry
entry align="center" colname="c2"
p−11.732/p
/entry
entry align="center" colname="c3"
p<0.001***/p
/entry
entry align="center" colname="c4"
p−11.555/p
/entry
entry align="center" colname="c5"
p<0.001***/p
/entry
entry align="center" colname="c6"
p−10.052/p
/entry
entry align="center" colname="c7"
p<0.001***/p
/entry
entry align="center" colname="c8"
p−9.757/p
/entry
entry align="center" colname="c9"
p<0.001***/p
/entry
/row
row rowsep="1"
entry align="center" colname="c1"
pNo. pairs/p
/entry
entry align="center" colname="c2" nameend="c3" namest="c2"
p1,189/p
/entry
entry align="center" colname="c4" nameend="c5" namest="c4"
p1,106/p
/entry
entry align="center" colname="c6" nameend="c7" namest="c6"
p1,156/p
/entry
entry align="center" colname="c8" nameend="c9" namest="c8"
p1,106/p
/entry
/row
row rowsep="1"
entry align="center" colname="c1"
pMean No. R/p
/entry
entry align="center" colname="c2" nameend="c3" namest="c2"
p49.653/p
/entry
entry align="center" colname="c4" nameend="c5" namest="c4"
p42.287/p
/entry
entry align="center" colname="c6" nameend="c7" namest="c6"
p31.813/p
/entry
entry align="center" colname="c8" nameend="c9" namest="c8"
p27.061/p
/entry
/row
row rowsep="1"
entry align="center" colname="c1"
pOverlap rate/p
/entry
entry align="center" colname="c2" nameend="c3" namest="c2"
p6.752/p
/entry
entry align="center" colname="c4" nameend="c5" namest="c4"
p5.349/p
/entry
entry align="center" colname="c6" nameend="c7" namest="c6"
p4.206/p
/entry
entry align="center" colname="c8" nameend="c9" namest="c8"
p3.423/p
/entry
/row
/tbody
/tgroup
/table
pFigure 
figr fid="F2"2/figr shows the boxplots for urban and rural itPv/itPR surveys for individual cities whose extents were defined by the GRUMP-UE. The results indicate that the patterns among the 20 cities examined were less consistent with the global, regional and national patterns found. Seven cities (Alamata, Ethiopia; Jakarta, Batam, Kupang, Jambi and Ambon, Indonesia; Rourkela, India) were found to have significantly lower itPv/itPR values in their urban extents than the surrounding rural areas; two cities (Qandahar, Afghanistan; Ariquemes, Brazil) were found to have significantly lower itPv/itPR values in their surrounding rural areas (though again, the numbers of surveys were small). The remainder were either insignificant or of zero itPv/itPR values./p
fig id="F2"titlepFigure 2/p/titlecaptionpBoxplots showing the differences in itPv/itPR values between GRUMP-UE defined urban and rural surveys for cities/p/captiontext
pbBoxplots showing the differences in /bbitPv /it/bbPR values between GRUMP-UE defined urban and rural surveys for cities./b (*) denotes the significant level of the test results (*** = P < 0.01, ** = P < 0.05, * = P < 0.1)./p
/textgraphic file="1475-2875-11-403-2"//fig
/sec
sec
st
pDominant itAnopheles/it vectors/p
/st
pFigure 
figr fid="F3"3A/figr presents the results of Wilcoxon Signed Rank tests on itPv/itPR values between GRUMP-UE defined urban and rural survey pairs stratified by the dominant itAnopheles/it vectors of human malaria in the Asia-Pacific region. In this region, the patterns of lower itP/it. itvivax/it malaria transmission in urban areas are noticeable and consistent, with significantly higher rural itPv/itPR values found for most of the dominant itAnopheles/it vector distributions (17 out of 19). Furthermore, insignificant differences between urban and rural areas (itAnopheles balabacensis/it and itAnopheles lesteri/it) were found in regions with small numbers of survey pairs./p
fig id="F3"titlepFigure 3/p/titlecaptionpBar charts showing the test results for the dominant itAnopheles/it vectors of human malaria/p/captiontext
pbBar charts showing the test results for the dominant /bbitAnopheles /it/bbvectors of human malaria./b Panel bA/b shows the results of Wilcoxon Signed Rank tests on itPv/itPR values between GRUMP-UE defined urban (U) and rural(R) survey pairs for the dominant itAnopheles/it vectors of human malaria in Asia-Pacific region. Panel bB/b shows the results for the dominant itAnopheles/it vectors in Africa, Europe and the Middle East. Panel bC/b shows the results of Wilcoxon Signed Rank tests for the dominant itAnopheles/it vectors in the Americas. (sup#/sup) denotes that a vector species is now recognized as a species complex. (*) denotes the significant level of the test (*** = P < 0.01, ** = P < 0.05, * = P < 0.1)./p
/textgraphic file="1475-2875-11-403-3"//fig
pFigure 
figr fid="F3"3B/figr shows the results of Wilcoxon Signed Rank tests on itPv/itPR values between urban and rural survey pairs stratified by the dominant itAnopheles/it vector distributions in Africa, Europe and the Middle East. itPv/itPR surveys were only available for nine (of the 13) dominant itAnopheles/it vectors. The consistent patterns of lower itPv/itPR values in urban areas are not as evident as in Asia-Pacific region. The differences of itPv/itPR between urban and rural areas are found to be statistically significant for only four (out of nine) dominant itAnopheles/it vectors (itAnopheles arabiensis/it, itAnopheles funestus/it, itAnopheles nili/it and itAnopheles sergentii/it). The others were insignificant, while two of them (itAnopheles melas/it and itAnopheles sacharovi/it) have insufficient number of itPv/itPR surveys./p
pFigure 
figr fid="F3"3C/figr presents the results of Wilcoxon Signed Rank tests for analyses stratified by dominant itAnopheles/it vectors in the Americas. For two (out of nine) of the dominant itAnopheles/it vectors no itPv/itPR surveys fell within their extents. Unlike the patterns exhibited in the other regions, consistently higher itPv/itPR values in urban areas were observed in this region, with most of the dominant itAnopheles/it vectors (itAnopheles albitarsis/it, itAnopheles darlingi/it, itAnopheles marajoara/it and itAnopheles nuneztovari/it) showing significantly higher urban itPv/itPR values. However, the numbers of survey pairs in this region are generally small./p
pMore detailed statistical results for the three regions are provided in Additional file
supplr sid="S1"1/supplr./p
suppl id="S1"
title
pAdditional file 1/p
/title
text
p
bResults of Wilcoxon Signed Rank tests on /bb
itPv /it
/bbPR values between GRUMP-UE defined urban (U) and rural(R) survey pairs for the dominant /bb
itAnopheles /it
/bbvectors of human malaria./b
/p
/text
file name="1475-2875-11-403-S1.docx"
pClick here for file/p
/file
/suppl
/sec
/sec
sec
st
pDiscussion/p
/st
pThe rapid urban transformation of the developing world
abbrgrp
abbr bid="B47"47/abbr
/abbrgrp has and will continue to have a profound influence on the malaria landscape. The need for accurate and contemporary descriptions of populations at risk (PAR) has lead to several attempts to quantify the impact of urbanization on itP/it. itfalciparum/it malaria transmission
abbrgrp
abbr bid="B9"9/abbr
abbr bid="B13"13/abbr
abbr bid="B18"18/abbr
/abbrgrp. Knowledge is lacking however regarding the relationship between urbanization and itP/it. itvivax/it malaria transmission. In this study, the most contemporary and comprehensive database of itPv/itPR surveys was used to explore the differences in itP/it. itvivax/it transmission between urban and rural areas./p
pLower itP/it. itvivax/it malaria transmission in urban areas than surrounding rural areas was found globally, and in the Africa+ and Asia+ regions (Table 
tblr tid="T2"2/tblr), which corroborates previous findings that the urban environment is typically not suitable for malaria mosquito vectors
abbrgrp
abbr bid="B7"7/abbr
abbr bid="B8"8/abbr
abbr bid="B9"9/abbr
/abbrgrp. The consistent patterns of significantly lower urban itPv/itPR values found at the national scale in most of the countries in Africa+ and Asia+ further supports these findings (Table 
tblr tid="T2"2/tblr). However, the urban–rural survey pairs for each region are dominated by a few countries (e.g., Indonesia accounts for 65% of the Asia pairs and Sudan accounts for 45% of the Africa pairs), which make the patterns found at regional scale less informative. Distinct and inconsistent results were found in the Americas, with higher itPv/itPR values in urban areas at the continental scale and for one particular country (Brazil) at the national scale. This result is probably due to the lack of itPv/itPR surveys in this region, as surveys from the region only account for 4.1% of the itPv/itPR global database. Getting extreme results is more likely when the numbers of surveys are small and only the rural itPv/itPR surveys were averaged. There is also evidence suggesting that higher malaria transmission in some areas of Brazil was actually a result of rapid urbanization, during which settlements were built close to forest boundaries or along riversides and thus resulting in greater exposure to the malaria parasite for residents
abbrgrp
abbr bid="B48"48/abbr
/abbrgrp./p
pFigure 
figr fid="F2"2/figr indicates that considerable heterogeneity exists when examining individual cities, with two cities (out of twenty) showing significantly lower itPv/itPR in their surrounding rural areas, and seven cities showing significantly lower prevalence in urban areas. Thus, only nine of the twenty cities examined showed significant differences in transmission between urban and rural areas, and three showed zero prevalence both within and around the urban areas. Compared to itP/it. itfalciparum/it
abbrgrp
abbr bid="B18"18/abbr
/abbrgrp, therefore, the patterns of itPv/itPR between urban and rural areas exhibit a higher level of heterogeneity. Several possible reasons include: 1) the wider transmission limits of itP/it. itvivax/it
abbrgrp
abbr bid="B15"15/abbr
/abbrgrp, but lower transmission intensity with many zero itPv/itPR values in the database; 2) the wide distribution in Asia and high prevalence of Duffy negativity in Africa
abbrgrp
abbr bid="B49"49/abbr
abbr bid="B50"50/abbr
/abbrgrp; 3) relatively fewer itPv/itPR surveys available in the MAP database compared with a total of 22,212 itP/it. itfalciparum/it parasite rate (itPf/itPR) surveys in 2010
abbrgrp
abbr bid="B23"23/abbr
/abbrgrp./p
pThe itPv/itPR differences between urban and rural settings within the ranges of the dominant itAnopheles/it vectors generally follows the patterns found in each region. This is partly because vector species that had sufficient urban–rural itPv/itPR pairs within their extents usually cover a large portion of the region. An issue raised here is that the distributions of most of the vector species overlap substantially with each other. Thus, drawing conclusions about the patterns of individual vector species is difficult without considering such overlap. However, according to expert-opinion distribution maps of global DVS
abbrgrp
abbr bid="B25"25/abbr
abbr bid="B26"26/abbr
abbr bid="B27"27/abbr
/abbrgrp, the spatial relationships among those vector species are extremely complex and the interaction effects of them are beyond the scope of this analysis./p
pThe GRUMP-UE was used to define urban areas here, though several alternative global urban maps exist
abbrgrp
abbr bid="B42"42/abbr
/abbrgrp. Every global map suffers from different errors and uncertainties
abbrgrp
abbr bid="B42"42/abbr
/abbrgrp, and the GRUMP-UE map exhibits overestimation of large urban area extents, due to the blooming effect of NTL imagery
abbrgrp
abbr bid="B42"42/abbr
abbr bid="B51"51/abbr
/abbrgrp. This suggests that the itPv/itPR urban values that were significantly higher than nearby rural ones found in the Americas and several other individual cities could actually be located in surrounding lower population density areas, as significantly higher malaria prevalence and entomologic inoculation rates in peri-urban areas compared to urban centers have been found in a number of studies
abbrgrp
abbr bid="B9"9/abbr
abbr bid="B13"13/abbr
abbr bid="B18"18/abbr
/abbrgrp. To assess briefly this potential bias in the GRUMP-UE map, urban extents mapped using Moderate Resolution Imaging Spectroradiometer (MODIS) satellite sensor imagery
abbrgrp
abbr bid="B40"40/abbr
abbr bid="B41"41/abbr
/abbrgrp were utilized to derive an alternative, more conservative, urban assignment for the itPv/itPR surveys. Again, sets of spatially and temporally associated urban–rural pairs of itPv/itPR values were extracted and tested. The results show that, due to the more conservative nature of the classification, and the fact that only intensely urban areas were mapped
abbrgrp
abbr bid="B40"40/abbr
abbr bid="B41"41/abbr
/abbrgrp, far fewer itPv/itPR surveys were identified as urban and the differences in itPv/itPR between urban and rural areas were generally not significant (see Additional file
supplr sid="S2"2/supplr). Such results highlight the differing outcomes that can occur through using differing definitions of urban, and that the effects of urbanization on itP/it. itvivax/it transmission may extend beyond the borders of intensely urban areas for most of the regions as a general trend of decreased itPv/itPR was found in urban areas. Another issue is that the GRUMP-UE map was produced in 2004 and some itPv/itPR surveys may be misclassified as the urban extent changes through time. However, global urban maps that are updated regularly or that quantify urban extent change do not currently exist. Furthermore, the majority of the itPv/itPR surveys were conducted between 2000 and 2010 (Table 
tblr tid="T1"1/tblr). Thus, it is reasonable to use the single time-point GRUMP-UE map in this analysis./p
suppl id="S2"
title
pAdditional file 2/p
/title
text
p
bResults of Wilcoxon Signed Rank tests on /bb
itPv /it
/bbPR values between MODIS defined urban (U) and rural(R) survey pairs for continents, countries and the World./b
/p
/text
file name="1475-2875-11-403-S2.docx"
pClick here for file/p
/file
/suppl
pA range of human-induced environmental changes (e.g., deforestation, urbanization, water control projects and climate change) have been identified as drivers of ‘emerging’ and ‘reemerging’ diseases and the transmission of vector-borne and other infectious diseases
abbrgrp
abbr bid="B52"52/abbr
abbr bid="B53"53/abbr
abbr bid="B54"54/abbr
abbr bid="B55"55/abbr
/abbrgrp. Urbanization is usually recognized as one of the primary factors affecting vector-borne diseases
abbrgrp
abbr bid="B56"56/abbr
/abbrgrp as it can not only provide residents with better access to healthcare and interventions
abbrgrp
abbr bid="B4"4/abbr
abbr bid="B5"5/abbr
/abbrgrp, and an environment generally less favorable for many disease vectors
abbrgrp
abbr bid="B7"7/abbr
abbr bid="B8"8/abbr
/abbrgrp, but can also modify land uses to expose humans to new pathogens and vectors
abbrgrp
abbr bid="B57"57/abbr
/abbrgrp. While global and regional-scale results here show a general trend of decreased itP/it. itvivax/it transmission in urban areas, the heterogeneous impacts of urbanization on itP/it. itvivax/it malaria transmission at the city scale found in these analyses support increasing concerns of urban malaria problems in developing countries. Urbanization in these regions is often associated with poverty, poor water supplies and sanitation in peri-urban areas, providing breading sites for certain vectors
abbrgrp
abbr bid="B12"12/abbr
/abbrgrp. Although malaria vectors are generally not favoured by urban environments, there is evidence highlighting the potential of malaria vectors in adapting to urban environments
abbrgrp
abbr bid="B58"58/abbr
abbr bid="B59"59/abbr
abbr bid="B60"60/abbr
/abbrgrp. For example, itAnopheles gambiae s/it.its/it. was found breeding in polluted water bodies in Lagos, Nigeria
abbrgrp
abbr bid="B59"59/abbr
/abbrgrp. Furthermore, many studies suggested that urban agriculture is another important source for providing favourable breeding sites for malaria vectors in cities
abbrgrp
abbr bid="B61"61/abbr
abbr bid="B62"62/abbr
abbr bid="B63"63/abbr
abbr bid="B64"64/abbr
/abbrgrp. Increased malaria prevalence is often found in communities within a distance of 1 km from irrigated urban agriculture in Accra, Ghana
abbrgrp
abbr bid="B64"64/abbr
/abbrgrp, for example. Thus, malaria transmission in urban areas exhibits considerable spatial heterogeneity both between and within cities, depending on factors such as proximity to possible vector breeding habitats, urbanization level and socio-economic status
abbrgrp
abbr bid="B7"7/abbr
abbr bid="B65"65/abbr
/abbrgrp. Future work should aim to elucidate these drivers through examination of the disparity of itP/it. itvivax/it malaria transmission between and within cities using detailed household prevalence surveys and higher resolution urban maps./p
pIn general, the results here highlight a consistent relationship at large scales between urban areas and lower itP/it. itvivax/it transmission, mirroring results found for itP/it. itfalciparum/it, and pointing towards global declines in itP/it. itvivax/it transmission as urbanization permanently alters the receptivity of many areas. The findings suggest that these trends will likely continue to catalyze malaria declines on the path to a malaria free future./p
/sec
sec
st
pAbbreviations/p
/st
pAfrica+: Africa, Saudi Arabia and Yemen; Asia+: Central and South East Asia; DVS: Dominant vector species; GRUMP: Global Rural Urban Mapping Project; GRUMP-UE: GRUMP urban extent; MAP: Malaria Atlas Project; itPf/itPR: itP/it. itfalciparum/it parasite rate; itPv/itAPI: itP/it. itvivax/it annual parasite incidence; itPv/itPR: itP/it. itvivax/it parasite rate; itPv/itMECs: itP/it. itvivax/it malaria endemic countries./p
/sec
sec
st
pCompeting interests/p
/st
pThe authors declare that they have no competing interests./p
/sec
sec
st
pAuthors' contributions/p
/st
pAJT conceived the analyses. QQ and AJT developed the study design and QQ conducted the analyses. CAG, CMM and IRF gathered and processed the malaria prevalence data. PWG, CAG and SIH undertook construction of the vivax limits and dominant vector species dataset. All authors contributed to the writing of the manuscript. All authors read and approved the final manuscript./p
/sec
/bdy
bm
ack
sec
st
pAcknowledgements/p
/st
pThe large global assembly of parasite prevalence data was critically dependent on the generous contributions of data made by a large number of people in the malaria research and control communities and these individuals are listed on the MAP website (
urlhttp:www.map.ac.ukacknowledgements.html/url). AJT is supported by grants from the Bill and Melinda Gates Foundation (#49446 and #1032350) (
urlhttp:www.gatesfoundation.org/url) and NIHNIAID (U19AI089674). SIH is funded by a Senior Research Fellowship from the Wellcome Trust (#095066) that also supports PWG. CLM is funded by a Biomedical Resources Grant from the Wellcome Trust (#091835). IRFE is funded by grants from the University of Oxford—Li Ka Shing Foundation Global Health Program and the Oxford Tropical Network. AJT and SIH also acknowledge support from the RAPIDD program of the Science & Technology Directorate, Department of Homeland Security, and the Fogarty International Center, National Institutes of Health (
urlhttp:www.fic.nih.gov/url). This work forms part of the output of the Malaria Atlas Project (MAP,
urlhttp:www.map.ox.ac.uk/url), principally funded by the Wellcome Trust, UK (
urlhttp:www.wellcome.ac.uk/url). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript./p
/sec
/ack
refgrpbibl id="B1"augaucnmUnited Nations/cnm/au/augsourceWorld urbanization prospect, the 2011 revision/sourcepublisherNew York: United Nations/publisherpubdate2011/pubdate/biblbibl id="B2"titlepUrbanization, urbanicity, and health/p/titleaugausnmVlahov/snmfnmD/fnm/auausnmGalea/snmfnmS/fnm/au/augsourceJ Urban Health/sourcepubdate2002/pubdatevolume79/volumefpageS1/fpagelpageS12/lpagexrefbibpubidlistpubid idtype="doi"10.1093jurban79.suppl_1.S1/pubidpubid idtype="pmcid"3456615/pubidpubid idtype="pmpid"12473694/pubid/pubidlist/xrefbib/biblbibl id="B3"titlepUrban as a determinant of health/p/titleaugausnmVlahov/snmfnmD/fnm/auausnmFreudenberg/snmfnmN/fnm/auausnmProietti/snmfnmF/fnm/auausnmOmpad/snmfnmD/fnm/auausnmQuinn/snmfnmA/fnm/auausnmNandi/snmfnmV/fnm/auausnmGalea/snmfnmS/fnm/au/augsourceJ Urban Health/sourcepubdate2007/pubdatevolume84/volumefpage16/fpagelpage26/lpagexrefbibpubid idtype="doi"10.1007s11524-007-9169-3/pubid/xrefbib/biblbibl id="B4"titlepHealth and urban living/p/titleaugausnmDye/snmfnmC/fnm/au/augsourceScience/sourcepubdate2008/pubdatevolume319/volumefpage766/fpagelpage769/lpagexrefbibpubidlistpubid idtype="doi"10.1126science.1150198/pubidpubid idtype="pmpid" link="fulltext"18258905/pubid/pubidlist/xrefbib/biblbibl id="B5"titlepUrbanization and tropical health: then and now/p/titleaugausnmUtzinger/snmfnmJ/fnm/auausnmKeiser/snmfnmJ/fnm/au/augsourceAnn Trop Med Parasitol/sourcepubdate2006/pubdatevolume100/volumefpage517/fpagelpage533/lpagexrefbibpubidlistpubid idtype="doi"10.1179136485906X97372/pubidpubid idtype="pmpid" link="fulltext"16899152/pubid/pubidlist/xrefbib/biblbibl id="B6"titlepGlobal urbanization and impact on health/p/titleaugausnmMoore/snmfnmM/fnm/auausnmGould/snmfnmP/fnm/auausnmKeary/snmfnmBS/fnm/au/augsourceInt J Hyg Envir Heal/sourcepubdate2003/pubdatevolume206/volumefpage269/fpagelpage278/lpagexrefbibpubid idtype="doi"10.10781438-4639-00223/pubid/xrefbib/biblbibl id="B7"titlepMalaria transmission in urban sub-Saharan Africa/p/titleaugausnmRobert/snmfnmV/fnm/auausnmMacintyre/snmfnmK/fnm/auausnmKeating/snmfnmJ/fnm/auausnmTrape/snmfnmJ-F/fnm/auausnmDuchemin/snmfnmJ-B/fnm/auausnmWarren/snmfnmM/fnm/auausnmBeier/snmfnmJC/fnm/au/augsourceAmJTrop Med Hyg/sourcepubdate2003/pubdatevolume68/volumefpage169/fpagelpage176/lpage/biblbibl id="B8"titlepMalaria and urbanization in sub-Saharan Africa/p/titleaugausnmDonnelly/snmfnmM/fnm/auausnmMcCall/snmfnmPJ/fnm/auausnmLengeler/snmfnmC/fnm/auausnmBates/snmfnmI/fnm/auausnmD’Alessandro/snmfnmU/fnm/auausnmBarnish/snmfnmG/fnm/auausnmKonradsen/snmfnmF/fnm/auausnmKlinkenberg/snmfnmE/fnm/auausnmTownson/snmfnmH/fnm/auausnmTrape/snmfnmJ-F/fnm/auausnmHastings/snmfnmI/fnm/auausnmMutero/snmfnmC/fnm/au/augsourceMalar J/sourcepubdate2005/pubdatevolume4/volumefpage12/fpagexrefbibpubidlistpubid idtype="doi"10.11861475-2875-4-12/pubidpubid idtype="pmcid"552321/pubidpubid idtype="pmpid" link="fulltext"15720713/pubid/pubidlist/xrefbib/biblbibl id="B9"titlepUrbanization, malaria transmission and disease burden in Africa/p/titleaugausnmHay/snmfnmSI/fnm/auausnmGuerra/snmfnmCA/fnm/auausnmTatem/snmfnmAJ/fnm/auausnmAtkinson/snmfnmPM/fnm/auausnmSnow/snmfnmRW/fnm/au/augsourceNat Rev Micro/sourcepubdate2005/pubdatevolume3/volumefpage81/fpagelpage90/lpagexrefbibpubid idtype="doi"10.1038nrmicro1069/pubid/xrefbib/biblbibl id="B10"titlepMalaria and urbanization in central africa: the example of brazzaville: part IV. Parasitological and serological surveys in urban and surrounding rural areas/p/titleaugausnmTrape/snmfnmJF/fnm/au/augsourceTrans R Soc Trop Med Hyg/sourcepubdate1987/pubdatevolume81/volumefpage26/fpagelpage33/lpagexrefbibpubid idtype="pmpid"3332057/pubid/xrefbib/biblbibl id="B11"titlepMalaria and urbanization in Central Africa: the example of Brazzaville: Part III: Relationships between urbanization and the intensity of malaria transmission/p/titleaugausnmTrape/snmfnmJF/fnm/auausnmZoulani/snmfnmA/fnm/au/augsourceTrans R Soc Trop Med Hyg/sourcepubdate1987/pubdatevolume81/volumefpage19/fpagelpage25/lpagexrefbibpubid idtype="pmpid"3455564/pubid/xrefbib/biblbibl id="B12"titlepVector-borne disease problems in rapid urbanization: new approaches to vector control/p/titleaugausnmKnudsen/snmfnmAB/fnm/auausnmSloff/snmfnmR/fnm/au/augsourceBull World Health Organ/sourcepubdate1992/pubdatevolume70/volumefpage1/fpagelpage6/lpagexrefbibpubidlistpubid idtype="pmcid"2393336/pubidpubid idtype="pmpid"1568273/pubid/pubidlist/xrefbib/biblbibl id="B13"titlepUrbanization in sub-Saharan Africa and implication for malaria control/p/titleaugausnmKeiser/snmfnmJ/fnm/auausnmUtzinger/snmfnmJ/fnm/auausnmDe Castro/snmfnmMC/fnm/auausnmSmith/snmfnmTA/fnm/auausnmTanner/snmfnmM/fnm/auausnmSinger/snmfnmBH/fnm/au/augsourceAm J Trop Med Hyg/sourcepubdate2004/pubdatevolume71/volumefpage118/fpagelpage127/lpagexrefbibpubid idtype="pmpid" link="fulltext"15331827/pubid/xrefbib/biblbibl id="B14"titlepThe neglected burden of Plasmodium vivax malaria/p/titleaugausnmMendis/snmfnmK/fnm/auausnmSina/snmfnmB/fnm/auausnmMarchesini/snmfnmP/fnm/auausnmCarter/snmfnmR/fnm/au/augsourceAm J Trop Med Hyg/sourcepubdate2001/pubdatevolume64/volumefpage97/fpagelpage106/lpagexrefbibpubid idtype="pmpid" link="fulltext"11425182/pubid/xrefbib/biblbibl id="B15"titlepThe international limits and population at risk of plasmodium vivax transmission in 2009/p/titleaugausnmGuerra/snmfnmCA/fnm/auausnmHowes/snmfnmRE/fnm/auausnmPatil/snmfnmAP/fnm/auausnmGething/snmfnmPW/fnm/auausnmVan Boeckel/snmfnmTP/fnm/auausnmTemperley/snmfnmWH/fnm/auausnmKabaria/snmfnmCW/fnm/auausnmTatem/snmfnmAJ/fnm/auausnmManh/snmfnmBH/fnm/auausnmElyazar/snmfnmIRF/fnm/auausnmBaird/snmfnmJK/fnm/auausnmSnow/snmfnmRW/fnm/auausnmHay/snmfnmSI/fnm/au/augsourcePLoS Negl Trop Dis/sourcepubdate2010/pubdatevolume4/volumefpagee774/fpagexrefbibpubidlistpubid idtype="doi"10.1371journal.pntd.0000774/pubidpubid idtype="pmcid"2914753/pubidpubid idtype="pmpid" link="fulltext"20689816/pubid/pubidlist/xrefbib/biblbibl id="B16"titlepVivax malaria: neglected and not benign/p/titleaugausnmPrice/snmfnmRN/fnm/auausnmTjitra/snmfnmE/fnm/auausnmGuerra/snmfnmCA/fnm/auausnmYeung/snmfnmS/fnm/auausnmWhite/snmfnmNJ/fnm/auausnmAnstey/snmfnmNM/fnm/au/augsourceAm J Trop Med Hyg/sourcepubdate2007/pubdatevolume77/volumefpage79/fpagelpage87/lpagexrefbibpubidlistpubid idtype="pmcid"2653940/pubidpubid idtype="pmpid" link="fulltext"18165478/pubid/pubidlist/xrefbib/biblbibl id="B17"titlepNeglect of Plasmodium vivax malaria/p/titleaugausnmBaird/snmfnmJK/fnm/au/augsourceTrends Parasitol/sourcepubdate2007/pubdatevolume23/volumefpage533/fpagelpage539/lpagexrefbibpubidlistpubid idtype="doi"10.1016j.pt.2007.08.011/pubidpubid idtype="pmpid" link="fulltext"17933585/pubid/pubidlist/xrefbib/biblbibl id="B18"titlepHuman population, urban settlement patterns and their impact on Plasmodium falciparum malaria endemicity/p/titleaugausnmTatem/snmfnmA/fnm/auausnmGuerra/snmfnmC/fnm/auausnmKabaria/snmfnmC/fnm/auausnmNoor/snmfnmA/fnm/auausnmHay/snmfnmS/fnm/au/augsourceMalar J/sourcepubdate2008/pubdatevolume7/volumefpage218/fpagexrefbibpubidlistpubid idtype="doi"10.11861475-2875-7-218/pubidpubid idtype="pmcid"2586635/pubidpubid idtype="pmpid" link="fulltext"18954430/pubid/pubidlist/xrefbib/biblbibl id="B19"titlepDefining the global spatial limits of malaria transmission in 2005/p/titleaugausnmGuerra/snmfnmCA/fnm/auausnmSnow/snmfnmRW/fnm/auausnmHay/snmfnmSI/fnm/au/augsourceAdv Parasitol/sourcepubdate2006/pubdatevolume62/volumefpage157/fpagelpage179/lpagexrefbibpubidlistpubid idtype="pmcid"3145102/pubidpubid idtype="pmpid" link="fulltext"16647970/pubid/pubidlist/xrefbib/biblbibl id="B20"titlepMapping the global extent of malaria in 2005/p/titleaugausnmGuerra/snmfnmCA/fnm/auausnmSnow/snmfnmRW/fnm/auausnmHay/snmfnmSI/fnm/au/augsourceTrends Parasitol/sourcepubdate2006/pubdatevolume22/volumefpage353/fpagelpage358/lpagexrefbibpubidlistpubid idtype="doi"10.1016j.pt.2006.06.006/pubidpubid idtype="pmcid"3111076/pubidpubid idtype="pmpid" link="fulltext"16798089/pubid/pubidlist/xrefbib/biblbibl id="B21"titlepThe global distribution of clinical episodes of Plasmodium falciparum malaria/p/titleaugausnmSnow/snmfnmRW/fnm/auausnmGuerra/snmfnmCA/fnm/auausnmNoor/snmfnmAM/fnm/auausnmMyint/snmfnmHY/fnm/auausnmHay/snmfnmSI/fnm/au/augsourceNature/sourcepubdate2005/pubdatevolume434/volumefpage214/fpagelpage217/lpagexrefbibpubidlistpubid idtype="doi"10.1038nature03342/pubidpubid idtype="pmcid"3128492/pubidpubid idtype="pmpid" link="fulltext"15759000/pubid/pubidlist/xrefbib/biblbibl id="B22"titlepA world malaria map: Plasmodium falciparum endemicity in 2007/p/titleaugausnmHay/snmfnmSI/fnm/auausnmGuerra/snmfnmCA/fnm/auausnmGething/snmfnmPW/fnm/auausnmPatil/snmfnmAP/fnm/auausnmTatem/snmfnmAJ/fnm/auausnmNoor/snmfnmAM/fnm/auausnmKabaria/snmfnmCW/fnm/auausnmManh/snmfnmBH/fnm/auausnmElyazar/snmfnmIRF/fnm/auausnmBrooker/snmfnmS/fnm/auausnmSmith/snmfnmDL/fnm/auausnmMoyeed/snmfnmRA/fnm/auausnmSnow/snmfnmRW/fnm/au/augsourcePLoS Med/sourcepubdate2009/pubdatevolume6/volumefpagee1000048/fpagexrefbibpubidlistpubid idtype="pmcid"2659708/pubidpubid idtype="pmpid" link="fulltext"19323591/pubid/pubidlist/xrefbib/biblbibl id="B23"titlepA new world malaria map: Plasmodium falciparum endemicity in 2010/p/titleaugausnmGething/snmfnmP/fnm/auausnmPatil/snmfnmA/fnm/auausnmSmith/snmfnmD/fnm/auausnmGuerra/snmfnmC/fnm/auausnmElyazar/snmfnmI/fnm/auausnmJohnston/snmfnmG/fnm/auausnmTatem/snmfnmA/fnm/auausnmHay/snmfnmS/fnm/au/augsourceMalar J/sourcepubdate2011/pubdatevolume10/volumefpage378/fpagexrefbibpubidlistpubid idtype="doi"10.11861475-2875-10-378/pubidpubid idtype="pmcid"3274487/pubidpubid idtype="pmpid" link="fulltext"22185615/pubid/pubidlist/xrefbib/biblbibl id="B24"titlepInsight into global mosquito biogeography from country species records/p/titleaugausnmFoley/snmfnmDH/fnm/auausnmRueda/snmfnmLM/fnm/auausnmWilkerson/snmfnmRC/fnm/au/augsourceJ Med Entomol/sourcepubdate2007/pubdatevolume44/volumefpage554/fpagelpage567/lpagexrefbibpubidlistpubid idtype="doi"10.16030022-2585(2007)44[554:IIGMBF]2.0.CO;2/pubidpubid idtype="pmpid"17695008/pubid/pubidlist/xrefbib/biblbibl id="B25"titlepThe dominant Anopheles vectors of human malaria in Africa, Europe and the Middle East: occurrence data, distribution maps and bionomic precis/p/titleaugausnmSinka/snmfnmM/fnm/auausnmBangs/snmfnmM/fnm/auausnmManguin/snmfnmS/fnm/auausnmCoetzee/snmfnmM/fnm/auausnmMbogo/snmfnmC/fnm/auausnmHemingway/snmfnmJ/fnm/auausnmPatil/snmfnmA/fnm/auausnmTemperley/snmfnmW/fnm/auausnmGething/snmfnmP/fnm/auausnmKabaria/snmfnmC/fnm/auausnmOkara/snmfnmR/fnm/auausnmVan Boeckel/snmfnmT/fnm/auausnmGodfray/snmfnmHC/fnm/auausnmHarbach/snmfnmR/fnm/auausnmHay/snmfnmS/fnm/au/augsourceParasit Vectors/sourcepubdate2010/pubdatevolume3/volumefpage117/fpagexrefbibpubidlistpubid idtype="doi"10.11861756-3305-3-117/pubidpubid idtype="pmcid"3016360/pubidpubid idtype="pmpid" link="fulltext"21129198/pubid/pubidlist/xrefbib/biblbibl id="B26"titlepThe dominant Anopheles vectors of human malaria in the Asia-Pacific region: occurrence data, distribution maps and bionomic precis/p/titleaugausnmSinka/snmfnmM/fnm/auausnmBangs/snmfnmM/fnm/auausnmManguin/snmfnmS/fnm/auausnmChareonviriyaphap/snmfnmT/fnm/auausnmPatil/snmfnmA/fnm/auausnmTemperley/snmfnmW/fnm/auausnmGething/snmfnmP/fnm/auausnmElyazar/snmfnmI/fnm/auausnmKabaria/snmfnmC/fnm/auausnmHarbach/snmfnmR/fnm/auausnmHay/snmfnmS/fnm/au/augsourceParasit Vectors/sourcepubdate2011/pubdatevolume4/volumefpage89/fpagexrefbibpubidlistpubid idtype="doi"10.11861756-3305-4-89/pubidpubid idtype="pmcid"3127851/pubidpubid idtype="pmpid" link="fulltext"21612587/pubid/pubidlist/xrefbib/biblbibl id="B27"titlepThe dominant Anopheles vectors of human malaria in the Americas: occurrence data, distribution maps and bionomic precis/p/titleaugausnmSinka/snmfnmM/fnm/auausnmRubio-Palis/snmfnmY/fnm/auausnmManguin/snmfnmS/fnm/auausnmPatil/snmfnmA/fnm/auausnmTemperley/snmfnmW/fnm/auausnmGething/snmfnmP/fnm/auausnmVan Boeckel/snmfnmT/fnm/auausnmKabaria/snmfnmC/fnm/auausnmHarbach/snmfnmR/fnm/auausnmHay/snmfnmS/fnm/au/augsourceParasit Vectors/sourcepubdate2010/pubdatevolume3/volumefpage72/fpagexrefbibpubidlistpubid idtype="doi"10.11861756-3305-3-72/pubidpubid idtype="pmcid"2936890/pubidpubid idtype="pmpid" link="fulltext"20712879/pubid/pubidlist/xrefbib/biblbibl id="B28"titlepFighting malaria in India/p/titleaugausnmSharma/snmfnmVP/fnm/au/augsourceCurrent sci (Bangalore)/sourcepubdate1998/pubdatevolume75/volumefpage1127/fpage/biblbibl id="B29"titlepSome characteristics of the larval breeding sites of Anopheles culicifacies species B and E in Sri Lanka/p/titleaugausnmSurendran/snmfnmSN/fnm/auausnmRamasamyb/snmfnmR/fnm/au/augsourceJ Vector Dis/sourcepubdate2005/pubdatevolume42/volumefpage39/fpagelpage44/lpage/biblbibl id="B30"titlepMosquitoes (Diptera: Culicidae) breeding in brackish water: female ovipositional preferences or larval survival/p/titleaugausnmRoberts/snmfnmD/fnm/au/augsourceJ Med Entomol/sourcepubdate1996/pubdatevolume33/volumefpage525/fpagelpage530/lpagexrefbibpubid idtype="pmpid"8699444/pubid/xrefbib/biblbibl id="B31"titlepEfficacy of Agnique MMF monomolecular surface film against Anopheles stephensi breeding in urban habitats in India/p/titleaugausnmBatra/snmfnmCP/fnm/auausnmMittal/snmfnmPK/fnm/auausnmAdak/snmfnmT/fnm/auausnmSubbarao/snmfnmSK/fnm/au/augsourceJ Am Mosquito Contr/sourcepubdate2006/pubdatevolume22/volumefpage426/fpagelpage432/lpagexrefbibpubid idtype="doi"10.29878756-971X(2006)22[426:EOAMMS]2.0.CO;2/pubid/xrefbib/biblbibl id="B32"titlepBreeding habits of Anopheles stephensi Liston in an area of Calcutta/p/titleaugausnmBiswas/snmfnmD/fnm/auausnmDutta/snmfnmR/fnm/auausnmGhosh/snmfnmS/fnm/auausnmChatterjee/snmfnmK/fnm/auausnmHati/snmfnmA/fnm/au/augsourceIndian J Malariol/sourcepubdate1992/pubdatevolume29/volumefpage195/fpagelpage198/lpagexrefbibpubid idtype="pmpid"1286735/pubid/xrefbib/biblbibl id="B33"titlepThe Limits and intensity of Plasmodium falciparum transmission: implications for malaria control and elimination worldwide/p/titleaugausnmGuerra/snmfnmCA/fnm/auausnmGikandi/snmfnmPW/fnm/auausnmTatem/snmfnmAJ/fnm/auausnmNoor/snmfnmAM/fnm/auausnmSmith/snmfnmDL/fnm/auausnmHay/snmfnmSI/fnm/auausnmSnow/snmfnmRW/fnm/au/augsourcePLoS Med/sourcepubdate2008/pubdatevolume5/volumefpagee38/fpagexrefbibpubidlistpubid idtype="doi"10.1371journal.pmed.0050038/pubidpubid idtype="pmcid"2253602/pubidpubid idtype="pmpid" link="fulltext"18303939/pubid/pubidlist/xrefbib/biblbibl id="B34"augaucnmMalaria Atlas Project/cnm/au/augurlhttp:www.map.ox.ac.uk/url/biblbibl id="B35"titlepAssembling a global database of malaria parasite prevalence for the malaria atlas project/p/titleaugausnmGuerra/snmfnmCA/fnm/auausnmHay/snmfnmS/fnm/auausnmLucioparedes/snmfnmL/fnm/auausnmGikandi/snmfnmP/fnm/auausnmTatem/snmfnmA/fnm/auausnmNoor/snmfnmA/fnm/auausnmSnow/snmfnmR/fnm/au/augsourceMalar J/sourcepubdate2007/pubdatevolume6/volumefpage17/fpagexrefbibpubidlistpubid idtype="doi"10.11861475-2875-6-17/pubidpubid idtype="pmcid"1805762/pubidpubid idtype="pmpid" link="fulltext"17306022/pubid/pubidlist/xrefbib/biblbibl id="B36"titlepThe digital chart of the world project/p/titleaugausnmDanko/snmfnmDM/fnm/au/augsourcePhotogramm Eng Rem S/sourcepubdate1992/pubdatevolume58/volumefpage1125/fpagelpage1128/lpage/biblbibl id="B37"titlepDetermining global population distribution: methods, applications and data/p/titleaugausnmBalk/snmfnmDL/fnm/auausnmDeichmann/snmfnmU/fnm/auausnmYetman/snmfnmG/fnm/auausnmPozzi/snmfnmF/fnm/auausnmHay/snmfnmSI/fnm/auausnmNelson/snmfnmA/fnm/au/augsourceAdv Parasitol/sourcepubdate2006/pubdatevolume62/volumefpage119/fpagelpage156/lpagexrefbibpubidlistpubid idtype="pmcid"3154651/pubidpubid idtype="pmpid" link="fulltext"16647969/pubid/pubidlist/xrefbib/biblbibl id="B38"augausnmHansen/snmfnmM/fnm/auausnmDeFries/snmfnmR/fnm/auausnmTownshend/snmfnmJRG/fnm/auausnmSohlberg/snmfnmR/fnm/au/augsource1 km land cover classification derived from AVHRR. College Park/sourcepublisherMaryland: The Global Land Cover Facility/publisherpubdate1998/pubdate/biblbibl id="B39"titlepMapping city lights with nighttime data from the DMSP operational linescan system/p/titleaugausnmElvidge/snmfnmCD/fnm/auausnmBaugh/snmfnmKE/fnm/auausnmKihn/snmfnmEA/fnm/auausnmKroehl/snmfnmHW/fnm/auausnmDavis/snmfnmER/fnm/au/augsourcePhotogramm Eng Rem S/sourcepubdate1997/pubdatevolume63/volumefpage727/fpagelpage734/lpage/biblbibl id="B40"titlepA new map of global urban extent from MODIS data/p/titleaugausnmSchneider/snmfnmA/fnm/auausnmFriedl/snmfnmMA/fnm/auausnmPotere/snmfnmD/fnm/au/augsourceEnviron Res Lett/sourcepubdate2009/pubdatevolume4/volumefpage4/fpage/biblbibl id="B41"titlepMonitoring urban areas globally using MODIS 500 m data: New methods and datasets based on urban ecoregions/p/titleaugausnmSchneider/snmfnmA/fnm/auausnmFriedl/snmfnmMA/fnm/auausnmPotere/snmfnmD/fnm/au/augsourceRemote Sens Environ/sourcepubdate2010/pubdatevolume114/volumefpage1733/fpagelpage1746/lpagexrefbibpubid idtype="doi"10.1016j.rse.2010.03.003/pubid/xrefbib/biblbibl id="B42"titlepAssessing the accuracy of satellite derived global and national urban maps in Kenya/p/titleaugausnmTatem/snmfnmAJ/fnm/auausnmNoor/snmfnmAM/fnm/auausnmHay/snmfnmSI/fnm/au/augsourceRemote Sens Environ/sourcepubdate2005/pubdatevolume96/volumefpage87/fpagelpage97/lpagexrefbibpubidlistpubid idtype="doi"10.1016j.rse.2005.02.001/pubidpubid idtype="pmcid"3350068/pubidpubid idtype="pmpid"22581985/pubid/pubidlist/xrefbib/biblbibl id="B43"augaucnmCenter for Internation Earth Science Information Network(CIESIN), Columbia University/cnm/au/augsourceInternational food policy research institute (IFPRI), the world band, centro international de agricultura tropical (CIAT)/sourcepublisherPalisades, New York: CIESIN, Columbia University/publisherseries
title
pGlobal rural–urban mapping project (GRUMP): urban extents/p
/title
/seriespubdate2004/pubdate/biblbibl id="B44"titlepDeveloping global maps of the dominant Anopheles vectors of human malaria/p/titleaugausnmHay/snmfnmSI/fnm/auausnmSinka/snmfnmME/fnm/auausnmOkara/snmfnmRM/fnm/auausnmKabaria/snmfnmCW/fnm/auausnmMbithi/snmfnmPM/fnm/auausnmTago/snmfnmCC/fnm/auausnmBenz/snmfnmD/fnm/auausnmGething/snmfnmPW/fnm/auausnmHowes/snmfnmRE/fnm/auausnmPatil/snmfnmAP/fnm/auausnmTemperley/snmfnmWH/fnm/auausnmBangs/snmfnmMJ/fnm/auausnmChareonviriyaphap/snmfnmT/fnm/auausnmElyazar/snmfnmIRF/fnm/auausnmHarbach/snmfnmRE/fnm/auausnmHemingway/snmfnmJ/fnm/auausnmManguin/snmfnmS/fnm/auausnmMbogo/snmfnmCM/fnm/auausnmRubio-Palis/snmfnmY/fnm/auausnmGodfray/snmfnmHCJ/fnm/au/augsourcePLoS Med/sourcepubdate2010/pubdatevolume7/volumefpagee1000209/fpagexrefbibpubidlistpubid idtype="doi"10.1371journal.pmed.1000209/pubidpubid idtype="pmcid"2817710/pubidpubid idtype="pmpid" link="fulltext"20161718/pubid/pubidlist/xrefbib/biblbibl id="B45"titlepIntradomestic mosquito breeding sources and their management/p/titleaugausnmGupta/snmfnmD/fnm/auausnmBhatt/snmfnmR/fnm/auausnmSharma/snmfnmR/fnm/auausnmGautam/snmfnmA/fnm/auausnmRajnikant/snmfnmAS/fnm/au/augsourceIndian J Malariol/sourcepubdate1992/pubdatevolume29/volumefpage41/fpagelpage46/lpagexrefbibpubid idtype="pmpid"1360910/pubid/xrefbib/biblbibl id="B46"titlepIndividual comparisons by ranking methods/p/titleaugausnmWilcoxon/snmfnmF/fnm/au/augsourceBiometrics/sourcepubdate1945/pubdatevolume1/volumefpage761/fpagelpage764/lpage/biblbibl id="B47"titlepThe urban transformation of the developing world/p/titleaugausnmMontgomery/snmfnmMR/fnm/au/augsourceScience/sourcepubdate2008/pubdatevolume319/volumefpage761/fpagelpage764/lpagexrefbibpubidlistpubid idtype="doi"10.1126science.1153012/pubidpubid idtype="pmpid" link="fulltext"18258903/pubid/pubidlist/xrefbib/biblbibl id="B48"titlepNon-planned urbanization as a contributing factor for malaria incidence in Manaus-Amazonas, Brazil/p/titleaugausnmGoncalves/snmfnmMJF/fnm/auausnmAlecrim/snmfnmWD/fnm/au/augsourceRev Salud Pública/sourcepubdate2004/pubdatevolume6/volumefpage156/fpagelpage166/lpage/biblbibl id="B49"titlepThe resistance factor to Plasmodium vivax in Blacks/p/titleaugausnmMiller/snmfnmLH/fnm/auausnmMason/snmfnmSJ/fnm/auausnmClyde/snmfnmDF/fnm/auausnmMcGinniss/snmfnmMH/fnm/au/augsourceNew Engl J Med/sourcepubdate1976/pubdatevolume295/volumefpage302/fpagelpage304/lpagexrefbibpubidlistpubid idtype="doi"10.1056NEJM197608052950602/pubidpubid idtype="pmpid" link="fulltext"778616/pubid/pubidlist/xrefbib/biblbibl id="B50"titlepThe global distribution of the duffy blood group/p/titleaugausnmHowes/snmfnmRE/fnm/auausnmPatil/snmfnmAP/fnm/auausnmPiel/snmfnmFB/fnm/auausnmNyangiri/snmfnmOA/fnm/auausnmKabaria/snmfnmCW/fnm/auausnmGething/snmfnmPW/fnm/auausnmZimmerman/snmfnmPA/fnm/auausnmBarnadas/snmfnmC/fnm/auausnmBeall/snmfnmCM/fnm/auausnmGebremedhin/snmfnmA/fnm/auausnmMenard/snmfnmD/fnm/auausnmWilliams/snmfnmTN/fnm/auausnmWeatherall/snmfnmDJ/fnm/auausnmHay/snmfnmSI/fnm/au/augsourceNat Commun/sourcepubdate2011/pubdatevolume2/volumefpage266/fpagexrefbibpubidlistpubid idtype="pmcid"3074097,3074097/pubidpubid idtype="pmpid" link="fulltext"21468018/pubid/pubidlist/xrefbib/biblbibl id="B51"titlepA scale-adjusted measure of “Urban sprawl” using nighttime satellite imagery/p/titleaugausnmSutton/snmfnmPC/fnm/au/augsourceRemote Sens Environ/sourcepubdate2003/pubdatevolume86/volumefpage353/fpagelpage369/lpagexrefbibpubid idtype="doi"10.1016S0034-4257(03)00078-6/pubid/xrefbib/biblbibl id="B52"titlepSocial and environmental risk factors in the emergence of infectious diseases/p/titleaugausnmWeiss/snmfnmRA/fnm/auausnmMcMichael/snmfnmAJ/fnm/au/augsourceNat Med/sourcepubdate2004/pubdatevolume10/volumefpage70/fpagelpage76/lpagexrefbibpubid idtype="doi"10.1038nm1150/pubid/xrefbib/biblbibl id="B53"titlepEnvironmental and social influences on emerging infectious diseases: past, present and future/p/titleaugausnmMcMichael/snmfnmAJ/fnm/au/augsourcePhilos Trans R Soc Lond B Biol Sci/sourcepubdate2004/pubdatevolume359/volumefpage1049/fpagelpage1058/lpagexrefbibpubidlistpubid idtype="doi"10.1098rstb.2004.1480/pubidpubid idtype="pmcid"1693387/pubidpubid idtype="pmpid" link="fulltext"15306389/pubid/pubidlist/xrefbib/biblbibl id="B54"titlepUnhealthy landscapes: policy recommendations on land use change and infectious disease emergence/p/titleaugausnmPatz/snmfnmJA/fnm/auausnmDaszak/snmfnmP/fnm/auausnmTabor/snmfnmGM/fnm/auausnmAguirre/snmfnmAA/fnm/auausnmPearl/snmfnmM/fnm/auausnmEpstein/snmfnmJ/fnm/auausnmWolfe/snmfnmND/fnm/auausnmKilpatrick/snmfnmAM/fnm/auausnmFoufopoulos/snmfnmJ/fnm/auausnmMolyneux/snmfnmD/fnm/auausnmBradley/snmfnmDJ/fnm/au/augsourceEnviron Health Perspect/sourcepubdate2004/pubdatevolume112/volumefpage1092/fpagelpage1098/lpagexrefbibpubidlistpubid idtype="doi"10.1289ehp.6877/pubidpubid idtype="pmcid"1247383/pubidpubid idtype="pmpid"15238283/pubid/pubidlist/xrefbib/biblbibl id="B55"titlepImpact of anthropogenic enviromental alterations on vector-borne diseases/p/titleaugausnmVora/snmfnmN/fnm/au/augsourceMedscape J Med/sourcepubdate2008/pubdatevolume10/volumefpage238/fpagexrefbibpubidlistpubid idtype="pmcid"2605134/pubidpubid idtype="pmpid"19099032/pubid/pubidlist/xrefbib/biblbibl id="B56"titlepPatterns of change in vector borne diseases/p/titleaugausnmMolyneux/snmfnmDH/fnm/au/augsourceAnn Trop Med Parasitol/sourcepubdate1997/pubdatevolume91/volumefpage827/fpagelpage840/lpagexrefbibpubidlistpubid idtype="doi"10.108000034989760581/pubidpubid idtype="pmpid" link="fulltext"9625939/pubid/pubidlist/xrefbib/biblbibl id="B57"titlepMosquito-borne diseases as a consequence of land use change/p/titleaugausnmNorris/snmfnmDE/fnm/au/augsourceEcohealth/sourcepubdate2004/pubdatevolume1/volumefpage19/fpagelpage24/lpagexrefbibpubid idtype="doi"10.1007s10393-004-0008-7/pubid/xrefbib/biblbibl id="B58"titlepEffects of ecological changes on the malaria vectors Anopheles funestus and the Anopheles gambiae complex of mosquitoes in Accra/p/titleaugausnmChinery/snmfnmWA/fnm/au/augsourceGhana. J Trop Med Hyg/sourcepubdate1984/pubdatevolume87/volumefpage191/fpagelpage206/lpage/biblbibl id="B59"titlepAnopheles gambiae s.s. breading in polluted water bodies in urban Lagos, southwestern Nigeria/p/titleaugausnmAwolola/snmfnmTS/fnm/auausnmOduola/snmfnmAO/fnm/auausnmObansa/snmfnmJB/fnm/auausnmChukwurar/snmfnmNJ/fnm/auausnmUnyimadu/snmfnmJP/fnm/au/augsourceJ Vector Dis/sourcepubdate2007/pubdatevolume44/volumefpage241/fpagelpage244/lpage/biblbibl id="B60"titlepMalaria vectors and urbanization in the equatorial forest region of south Cameroon/p/titleaugausnmAntonio-Nkondjio/snmfnmC/fnm/auausnmSimard/snmfnmF/fnm/auausnmAwono-Ambene/snmfnmP/fnm/auausnmNgassam/snmfnmP/fnm/auausnmToto/snmfnmJ-C/fnm/auausnmTchuinkam/snmfnmT/fnm/auausnmFontenille/snmfnmD/fnm/au/augsourceTrans R Soc Trop Med Hyg/sourcepubdate2005/pubdatevolume99/volumefpage347/fpagelpage354/lpagexrefbibpubidlistpubid idtype="doi"10.1016j.trstmh.2004.07.003/pubidpubid idtype="pmpid"15780341/pubid/pubidlist/xrefbib/biblbibl id="B61"titlepDoes irrigated urban agriculture influence the transmission of malaria in the city of Kumasi, Ghana/p/titleaugausnmAfrane/snmfnmYA/fnm/auausnmKlinkenberg/snmfnmE/fnm/auausnmDrechsel/snmfnmP/fnm/auausnmOwusu-Daaku/snmfnmK/fnm/auausnmGarms/snmfnmR/fnm/auausnmKruppa/snmfnmT/fnm/au/augsourceActa Trop/sourcepubdate2004/pubdatevolume89/volumefpage125/fpagelpage134/lpagexrefbibpubidlistpubid idtype="doi"10.1016j.actatropica.2003.06.001/pubidpubid idtype="pmpid" link="fulltext"14732235/pubid/pubidlist/xrefbib/biblbibl id="B62"titlepUrban farming and malaria risk factors in a medium-sized town in Côte d’Ivoire/p/titleaugausnmMatthys/snmfnmB/fnm/auausnmVounatsou/snmfnmP/fnm/auausnmRaso/snmfnmG/fnm/auausnmTschannen/snmfnmAB/fnm/auausnmBecket/snmfnmEG/fnm/auausnmGosoniu/snmfnmL/fnm/auausnmCisse/snmfnmG/fnm/auausnmTanner/snmfnmM/fnm/auausnmN’goran/snmfnmEK/fnm/auausnmUtzinger/snmfnmJ/fnm/au/augsourceAm J Trop Med Hyg/sourcepubdate2006/pubdatevolume75/volumefpage1223/fpagelpage1231/lpagexrefbibpubid idtype="pmpid" link="fulltext"17172397/pubid/xrefbib/biblbibl id="B63"titlepImpact of urban agriculture on malaria vectors in Accra. Ghana/p/titleaugausnmKlinkenberg/snmfnmE/fnm/auausnmMcCall/snmfnmP/fnm/auausnmWilson/snmfnmM/fnm/auausnmAmerasinghe/snmfnmF/fnm/auausnmDonnelly/snmfnmM/fnm/au/augsourceMalar J/sourcepubdate2008/pubdatevolume7/volumefpage151/fpagexrefbibpubidlistpubid idtype="doi"10.11861475-2875-7-151/pubidpubid idtype="pmcid"2515328/pubidpubid idtype="pmpid" link="fulltext"18680565/pubid/pubidlist/xrefbib/biblbibl id="B64"titlepDistance threshold for the effect of urban agriculture on elevated self-reported malaria prevalence in Accra. Ghana/p/titleaugausnmStoler/snmfnmJ/fnm/auausnmWeeks/snmfnmJR/fnm/auausnmGetis/snmfnmA/fnm/auausnmHill/snmfnmAG/fnm/au/augsourceAm J Trop Med Hyg/sourcepubdate2009/pubdatevolume80/volumefpage547/fpagelpage554/lpagexrefbibpubidlistpubid idtype="pmcid"2714825/pubidpubid idtype="pmpid" link="fulltext"19346373/pubid/pubidlist/xrefbib/biblbibl id="B65"titlepRisk factors associated with malaria infection in an urban setting/p/titleaugausnmMendez/snmfnmF/fnm/auausnmCarrasquilla/snmfnmG/fnm/auausnmMuñoz/snmfnmA/fnm/au/augsourceTrans R Soc Trop Med Hyg/sourcepubdate2000/pubdatevolume94/volumefpage367/fpagelpage371/lpagexrefbibpubidlistpubid idtype="doi"10.1016S0035-9203(00)90106-8/pubidpubid idtype="pmpid"11127234/pubid/pubidlist/xrefbib/bibl/refgrp
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epdcx:valueString The effects of urbanization on global Plasmodium vivax malaria transmission
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Abstract
Background
Many recent studies have examined the impact of urbanization on Plasmodium falciparum malaria endemicity and found a general trend of reduced transmission in urban areas. However, none has examined the effect of urbanization on Plasmodium vivax malaria, which is the most widely distributed malaria species and can also cause severe clinical syndromes in humans. In this study, a set of 10,003 community-based P. vivax parasite rate (PvPR) surveys are used to explore the relationships between PvPR in urban and rural settings.
Methods
The PvPR surveys were overlaid onto a map of global urban extents to derive an urban/rural assignment. The differences in PvPR values between urban and rural areas were then examined. Groups of PvPR surveys inside individual city extents (urban) and surrounding areas (rural) were identified to examine the local variations in PvPR values. Finally, the relationships of PvPR between urban and rural areas within the ranges of 41 dominant Anopheles vectors were examined.
Results
Significantly higher PvPR values in rural areas were found globally. The relationship was consistent at continental scales when focusing on Africa and Asia only, but in the Americas, significantly lower values of PvPR in rural areas were found, though the numbers of surveys were small. Moreover, except for the countries in the Americas, the same trends were found at national scales in African and Asian countries, with significantly lower values of PvPR in urban areas. However, the patterns at city scales among 20 specific cities where sufficient data were available were less clear, with seven cities having significantly lower PvPR values in urban areas and two cities showing significantly lower PvPR in rural areas. The urban–rural PvPR differences within the ranges of the dominant Anopheles vectors were generally, in agreement with the regional patterns found.
Conclusions
Except for the Americas, the patterns of significantly lower P. vivax transmission in urban areas have been found globally, regionally, nationally and by dominant vector species here, following trends observed previously for P. falciparum. To further understand these patterns, more epidemiological, entomological and parasitological analyses of the disease at smaller spatial scales are needed.
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Qi, Qiuyin
Guerra, Carlos A
Moyes, Catherine L
Elyazar, Iqbal R F
Gething, Peter W
Hay, Simon I
Tatem, Andrew J
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BioMed Central Ltd
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Qiuyin Qi et al.; licensee BioMed Central Ltd.
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Malaria Journal. 2012 Dec 05;11(1):403
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Additional file 2 Table A2.1 : Results of Wilcoxon Signed Rank tests on Pv PR values between MODIS defined urban (U) and rural(R) survey pairs for continents, countries and the World Region No. pairs U>R U

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