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Reexamining El Niño and Cholera in Peru: A Climate Affairs Approach

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Title:
Reexamining El Niño and Cholera in Peru: A Climate Affairs Approach
Series Title:
Weather, Climate and Society
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Ramírez, Ivan J.
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American Meteorological Society
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In the 1990s Peru experienced the first cholera epidemic after almost a century. The source of emergence was initially attributed to a cargo ship, but later there was evidence of an El Niño association. It was hypothesized that marine ecosystem changes associated with El Niño led to the propagation of V. cholerae along the coast of Peru, which in turn initiated the onset of the epidemic in 1991. Earlier studies supported this explanation by demonstrating a relationship between elevated temperatures and increased cholera incidence in Peru; however, other aspects of El Niño–Southern Oscillation (ENSO) and their potential impacts on cholera were not investigated. Therefore, this study examines the relationship between El Niño and cholera in Peru from a holistic view of the ENSO cycle. A “climate affairs” approach is employed as a conceptual framework to incorporate ENSO’s multidimensional nature and to generate new hypotheses about the ENSO and cholera association in Peru. The findings reveal that ENSO may have been linked to the cholera epidemic through multiple pathways, including rainfall extremes, La Niña, and social vulnerability, with impacts depending on the geography of teleconnections within Peru. When the definition of an ENSO event is examined, cholera appears to have emerged either during ENSO neutral or La Niña conditions. Furthermore, the analysis herein suggests that the impact of El Niño arrived much later, possibly resulting in heightened transmission in the austral summer of 1992. In conclusion, a modified hypothesis with these new insights on cholera emergence and transmission in Peru is presented.
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Collected for Auraria Institutional Repository by the Self-Submittal tool. Submitted by Ivan J. Ramírez.
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Published
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This is a review paper challenging the hypothesis that claims El Nino triggered the epidemic in Peru in 1991.

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ReexaminingElNi ~ noandCholerainPeru:AClimateAffairsApproachIVA ´ NJ.RAMI ´ REZDivisionofSocialSciences,NewCollegeofFlorida,Sarasota,FloridaSUEC.GRADYDepartmentofGeography,MichiganStateUniversity,EastLansing,MichiganMICHAELH.GLANTZConsortiumforCapacityBuilding,UniversityofColorado,Boulder,Colorado (Manuscriptreceived18June2012,innalform21November2012) ABSTRACT Inthe1990sPeruexperiencedtherstcholeraepidemicafteralmostacentury.Thesourceofemergence wasinitiallyattributedtoacargoship,butlatertherewasevidenceofanElNi ~ noassociation.ItwashypothesizedthatmarineecosystemchangesassociatedwithElNi ~ noledtothepropagationof V.cholerae along thecoastofPeru,whichinturninitiatedtheonsetoftheepidemicin1991.Earlierstudiessupportedthis explanationbydemonstratingarelationshipbetweenelevatedtemperaturesandincreasedcholeraincidence inPeru;however,otheraspectsofElNi ~ no–SouthernOscillation(ENSO)andtheirpotentialimpactson cholerawerenotinvestigated.Therefore,thisstudyexaminestherelationshipbetweenElNi ~ noandcholerain PerufromaholisticviewoftheENSOcycle.A‘‘climateaffairs’’approachisemployedasaconceptual frameworktoincorporateENSO’smultidimensionalnatureandtogeneratenewhypothesesabouttheENSO andcholeraassociationinPeru.ThendingsrevealthatENSOmayhavebeenlinkedtothecholeraepidemic throughmultiplepathways,includingrainfallextremes,LaNi ~ na,andsocialvulnerability,withimpactsdependingonthegeographyofteleconnectionswithinPeru.WhenthedenitionofanENSOeventisexamined, choleraappearstohaveemergedeitherduringENSOneutralorLaNi ~ naconditions.Furthermore,the analysishereinsuggeststhattheimpactofElNi ~ noarrivedmuchlater,possiblyresultinginheightened transmissionintheaustralsummerof1992.Inconclusion,amodiedhypothesiswiththesenewinsightson choleraemergenceandtransmissioninPeruispresented.1.IntroductionIthasbeenalmost20yearssincePeruexperiencedthe rstcholeraepidemicafteralmostacentury.Theoutbreak,associatedwiththeElTorstrainof V.cholerae , beganinJanuary1991alongseveralcoastalcitiesin PeruandthenspreadrapidlytoneighboringSouthand CentralAmericancountries,infectingapproximately 400000peopleintherstyearoftheonset(PAHO 1991;MINSA1994,p.43).Overthenextdecade,an estimated1.2millioncasesofcholeraweredocumented intheregion.Approximately52.0%(703000)ofall choleracasesoccurredinPeru(PAHO2008). Whilepreviousstudieshaveshownthatthediffusion ofcholerainPeruwasduetopoorwaterandsanitation systemcapacities(PAHO1991;MINSA1994,p.44; Tauxeetal.1995;SeasandGotuzzo1996),thecauseof theinitialoutbreakisstillunknown.Thesourceof emergencewasinitiallyattributedtoinfectedpersonsor contaminatedwastewaterdispelledfromacargoship (GangarosaandTauxe1992,p.353).However,these explanationswerelaterchallengedbyanotherhypothesisthatlinkedthecholeraepidemictoElNi ~ no– SouthernOscillation(ENSO)(Epsteinetal.1993; Colwell1996;Mourino-Perez1998).ENSO,whichincludesElNi ~ no(warmphase)andLaNi ~ na(coldphase), isanimportantsourceofclimatevariabilityintheLatin Americanregion,wellknownforecosystemandsocietal Correspondingauthoraddress: Iva ´ nJ.Ram ´ rez,DivisionofSocialSciences,NewCollegeofFlorida,5800BayShoreRoad,Sarasota,FL34234. E-mail:iramirez@ncf.edu148WEATHER,CLIMATE,ANDSOCIETYVOLUME5 DOI:10.1175/WCAS-D-12-00032.1 2013AmericanMeteorologicalSociety 8QDXWKHQWLFDWHG_'RZQORDGHG$087&

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impacts,particularlyinPeru(LagosandBuizer1992; Glantz2001a;Caviedes2001).Therefore,itwasproposedthatmarineecosystemchangesassociatedwithEl Ni ~ noledtothepropagationof V.cholerae alongthe coastofPeru,whichinturninitiatedtheonsetofthe epidemicin1991(Colwell1996). Inearlierstudies,someevidenceinPerusuggested thatairandwatertemperaturechangescontributedto choleraincidenceviaitsecologicalimpactsonvibrios. Forexample,itwasshownthatelevatedtemperatures werepositivelycorrelatedwithdiarrhealdisease(SalazarLindoetal.1997;Checkleyetal.2000;Lamaetal.2004) andthepresenceof V.cholerae inwatersourcesinPeru (Francoetal.1997;Speelmonetal.2000;Lippetal. 2003).Itwasalsoreportedthatcholeraincidencewas stronglyassociatedwithairandseawatertemperatures duringthe1997/98ElNi ~ no(Speelmonetal.2000;Gil etal.2004).Morerecently,researchersdemonstrated howocean–atmosphereinteractionsinuencedthe transportofvibriosalongthecoastofPeru(MartinezUrtazaetal.2008). Still,despitetheseadvancesinpotentialevidence,El Ni ~ no’slinkwithcholerainPeruremainsunclear.Thisis largelyduetopreviousstudies,whichwerelimitedin theirexaminationoftheENSOcycle.Forexample,the empiricalevidencesofarismainlybasedontemporal investigationsincoastalLima.Giventhevariabilityof ENSO’sinuencewithinPeru,thetemperature–cholera associationmayhavedifferedbygeography(e.g.,coast versusjungle).Moreover,thestrongestevidenceis basedononeElNi ~ noeventin1997/98.ElNi ~ no’simpact ontheinitialoutbreakhasyettobeexamined(SalazarLindoetal.2008).Furthermore,theElNi ~ no–cholera hypothesisisbasedonaperiodwhentherewasdisagreementaboutthetimingofElNi ~ no(WMO1999; Glantz2001a,p.21).Conceivably,thisraisesquestions aboutthedenitionofanENSOevent(Trenberth 1997),andthecoincidencebetweenthephysicalimpacts ofENSOandtheemergenceofcholerainPeru.Inaddition,thepotentialimpactsofrainfallextremesandLa Ni ~ nahavenotbeenexploredinrelationtocholera,even thoughtheformerisanimportantteleconnection,and thelatterisalsoassociatedwithhealtheffectsinPeru (MINSA1999a).Finally,howsocialfactorsofvulnerability,especiallyatthetimeofemergence,mayhave contributedtotheimpactofENSOoncholeraisnotyet known. Therefore,thepurposeofthisstudyistoexplorethese gapsofknowledgeintheliteraturebyexaminingthe relationshipbetweenElNi ~ noandcholerainPerufrom aholisticviewofENSO.Ourgoalistobetterunderstandthisassociationbyconsideringthemanywaysin whichENSOmayhavebeenlinkedtocholera emergenceandtransmissioninPeru.Anothergoalisto providenewinsightsonthehypothesisinordertostimulatenewavenuesforpotentialresearch.Asaconceptual framework,weemploya‘‘climateaffairs’’approachto widenthescopeofanalysisinrelationtoprevious studies.Climateaffairsisamultidisciplinaryconcept usedtounderstandclimate–societyinteractionsworldwide(GlantzandAdeel2000;Glantz2003;CCB2011) and,inparticular,societalimpactsassociatedwith ENSO(Glantz2001a,b).Fromaclimateaffairsorientation,weincorporateENSO’smultidimensionalnature togeneratenewhypothesesabouttheENSOandcholeraassociationinPeru.Inadditiontoaliteraturereview wealsodescribedataabouttheepidemicandENSO collectedduringeldworkinPeruin2008and2009. Thesedatawereobtainedfromdocumentsincluding healthdataandbulletins,newspaperarchives,andreportsfromPeruviannongovernmentalandgovernmental institutions. Followingthisintroductionisadescriptionofthe climateaffairsapproachanditsapplicationinthisstudy. ThesecondsectionisareviewoftheElNi ~ no–cholera hypothesisinPeru.Thethirdsectionrecountsthecurrentevidenceinsupportofthehypothesisandalink. Here,ourfocusistheliteratureinPeru.Thefourth sectionreexaminestherelationshipbetweenElNi ~ no andcholerainPeruusingaclimateaffairsapproach.We beginbyrevisitingthetemperatureassociationandthen explorethedenitionofanENSOevent,whichincludes anassessmentofElNi ~ no’stimingandimpactsinPeru; rainfallextremes;theLaNi ~ nafactor;andsocialvulnerability.Inthenalsection,wesummarizeourndingsandconcludebypresentingamodiedhypothesis withnewinsightsoncholeraemergenceandtransmissioninPeru.2.AclimateaffairsapproachClimateaffairsisaholisticapproachtounderstanding themanyfacetsofclimate(e.g.,averages,extremes, variability,andchange)andhowsocietiesinteractwith climatephenomena(GlantzandAdeel2000;Glantz 2003;CCB2011).Itsbasiccomponentsencompass,but arenotlimitedto,(a)climatescience,(b)climateimpacts,(c)climateeconomics,(d)climatepoliticsand policy,and(e)climateethics.Thus,itemphasizesthe importanceofmultidisciplinaryeffortsacrossphysical andsocialsciencesandhumanities.Italsorecognizes localandregionalknowledgetounderstandingclimate– societyinteractions(Glantz2003).Theconceptevolved fromthecollaborativeresearchandprogramactivities ofDr.MichaelH.Glantz,beginningin1974attheEnvironmentalandSocietalImpactsGroupattheNationalAPRIL2013RAMI ´ REZETAL.149 8QDXWKHQWLFDWHG_'RZQORDGHG$087&

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CenterforAtmosphericResearch(NCAR).Itlater cametofruitionasaresearch,training,andeducation initiativein2003.Currently,itcontinuestobeimplementedthroughtheConsortiumforCapacity BuildinganditspartnersattheUniversityofColorado atBoulder. Untilnow,theapplicationofclimateaffairshas generallyfocusedoncapacitybuildingeffortswith universities,researchinstitutes,multilateralorganizations,andgovernmentsaroundtheworld.Among theseactivities,thetransferofknowledgeaboutENSO, includingforecasting,sectoralimpacts,andsocietalresponses,hasbeenacentraltheme(Glantz1997,2001b, 2002).Inthisstudy,theconceptofclimateaffairsis utilizedasaresearchlenstohighlightandintegrate variousaspectsofENSOthatmayhavebeenimportant forcholeraemergenceandtransmissioninPeru.Specically,wedrawuponthefollowingelementsofENSO knowledge:ENSOscience,impacts,economics,politics, andethics.a.ENSOscienceENSOisaquasi-periodicphenomenon,composed ofwarm(ElNi ~ no),cold(LaNi ~ na),andneutralphases andocean–atmosphereinteractionsthatarebasinwide (i.e.,equatorialPacicOcean)andlocal(e.g.,Peru). ENSOneutralrefersto‘‘average’’seasurfacetemperature(SST)conditionsintheequatorialPacicthat donotqualifyaswarmorcoldphases(NOAA2011). ENSOismonitoredacrosstheequatorialPacicOcean basininfourdelimitedNi ~ noregionsknownasNi ~ no1 1 2,Ni ~ no-3,Ni ~ no-3.4,andNi ~ no-4(Fig.1).Interpreting thecharacteristicsofphasescanvarydependingonthe denitionofanevent,thevariableschosentomeasure ENSO,andtheNi ~ noregionofanalysis(Trenberth 1997;IRI2008).Therefore,carefulattentionshould bepaidtohoweventsarecharacterizedbecausethey mayaffecttheinterpretationofquantitativeassociationsbetweenENSOandhealthoutcomes(Kovatsetal. 2003).b.ENSOimpactsENSO’sinuenceonlocalclimate(e.g.,temperatureand rainfallteleconnections)canvarywithindifferentregions ofPeruandbyseason.Geographically,themostnotable effectsarestormsandrainsalongthenortherncoast,an areathatistypicallyarid,orbelowaveragerainsinthe southernandcentralAndes(Lagosetal.2008;SENAMHI 2009).Althoughprobable,teleconnectionsarenotdeterministicbecauseeacheventisuniqueandcanvaryinhow itdevelopsfromoneperiodtoanother(Wyrtki1975). However,itispossibletoforeseesomepotentialeffects onecosystemsandsocietiesbasedondirectandindirect observationsoftheenvironment,statisticalassessments, computermodeling,andhistoricalreportsofpastevents (Glantz2001a,163–173;McPhadenetal.2006).InPeru, theymayincludemarineecosystemchangesduetothe disruptionofupwellingprocesses,terrestrialecosystem changes(e.g.,vegetation,insects,andanimals),impactson sheriesandagriculture,anddamagedbuiltenvironment duetoooding(e.g.,energy,water,andsanitationsystems)(Glantz2001a).Whenecosystemchangeco-occurs withcollapseofinfrastructure,humanexposuretoinfectiousdiseasescanincreaseduringENSOevents(Gueri 1984;Valverde1998;PAHO1998a;Kovatsetal.2003).c.ENSOeconomics,politics,andethicsENSOimpactsonsocietyarecontingentnotonlyonthe geographiclocationofteleconnections,butalsoonsocial, economic,andpoliticalfactorsofvulnerabilitythatcontributetoclimate-relateddisasters(Glantz2003,p.253; Cutteretal.2009).InPeru,thegovernmentandits populationfacedanumberofchallengeswhencholera emergedthatincludedhumanitarianemergencies (UNDRO1990a),economicrestructuring,andanenergy crisis(ElTiempo1991;Youngers2000),nottomention thehighratesofpopulationdeprivationthatexistedat thetime(PAHO1991).AssumingElNi ~ no’simpacts werefeltinPeruin1991,inadditiontotriggeringthe epidemicashasbeensuggested,climatemayalsohave exacerbatedtheseverityofcholeratransmission.Itis importanttohighlightthiscontextintheexplanationof theElNi ~ noandcholeraassociationbecauseitplacesthe choleraepidemicattheintersectionofENSOandsociety interactions,crossingdisciplinaryboundaries(McPhaden etal.2006).Tangentially,italsoalludestopotentialissues of‘‘climatejustice’’(e.g.,equityofimpactsanddifferentialvulnerabilities)thatmayarisefromtheseinterrelationships(GlantzandJamieson2000;Ram ´ rez2012).3.TheElNi ~ no–cholerahypothesisSincetheemergenceofcholerainPeru,ElNi ~ noand climatehavebeenassociatedwithcholeratransmission. FIG.1.MapofNi ~ noregions.Source:NOAA(http://www1.ncdc. noaa.gov/pub/data/cmb/enso/Ni ~ no-regions.gif).150WEATHER,CLIMATE,ANDSOCIETYVOLUME5 8QDXWKHQWLFDWHG_'RZQORDGHG$087&

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ThelinkwasrstproposedbyEpstein(1992)inaletter totheeditorat TheLancet .AccordingtoEpstein,once V.cholerae wasintroducedtothecoastalwatersofPeru, itharboredamongalgaeandplanktonbloomsand proliferatedbecauseof‘‘warming,’’possiblyduetoEl Ni ~ noorglobalclimatechange.Furthermore,itwas thoughtthathumanactivities(e.g.,eutrophicationdue tountreatedsewagewasteandagriculturalactivities) hadalsocontributedto‘‘enhanced’’blooms.Thus,itwas suggestedinitiallythatcholeraemergedasaresultof climateandhuman-relatedprocesses(Epstein1993; Epsteinetal.1993,1994).Asthemodeoftransmission, Epsteinproposedthathumanconsumptionofshellsh thatfeedonbloomswastheinitialpathway(Epstein 1992,1993).WhileElNi ~ noseemedalikelyreasonfor theepidemic,itwasalsothoughtthatfurtherinvestigationswereneededbeforecausationcouldbe deduced.1In1996ElNi ~ nowashypothesized,withgreatercondenceandexplanation,asthemostimportantdriving factorintheepidemic(Colwell1996).Motivatingthis postulationwerethreeideas.First,thepassingshiphypothesiswasdismissedonthegroundsthatasingleship couldnotexplainmultipleentrypointsalongthePeruviancoast.Second,therewasgrowingevidenceof positiverelationshipsamongplankton, V.cholerae ,and choleraoutbreaksinBangladesh(Colwell1996);furthermore, V.cholerae wasshowntosurvivefreelyin estuarineenvironments,lyingdormantwhenenvironmentalconditionsarelessfavorableandincreasingin concentrationswhenconditionsareoptimal(Colwell andSpira1992;Colwell1996).Third,therewerereports ofan‘‘extraordinary’’ElNi ~ no,whichlastedfrom1990 to1995(TrenberthandHoar1996),whichwasbelieved tocoincidewiththecholeraepidemic.Therefore,itwas proposedthatanElNi ~ noinuencedseasurfacetemperatureanomaliesintheequatorialPacicOcean, whichinturnpromotedtheabundanceofplankton blooms(harboringbacteria)thatledtocholeratransmissionatmultiplelocationsonthecoast(Epstein1992; Colwell1996;Seasetal.2000).Itwasalsosuggestedthat nutrientrunoff(duetoheavyrains)mayhavecontributedtotheriseinblooms.Themechanismbywhich bloomsinvadedtheinlandcoastwasintrusionofwarm waters(Colwell1996),eitherbyrisingsealevelsand/or stormsurgeswiththearrivalofElNi ~ no.Furthermore,it wassuggestedthattheoriginalsourceof V.cholerae was contaminatedplanktonfromAsia,whichmayhavebeen transportedviaeastward-owingoceancurrentsinducedbyElNi ~ no(Colwell1996;Mourino-Perez1998). In2000,thehypothesisofferedbyColwell(1996)was sustainedintwoimportantstudies.Therststudy(Seas etal.2000)identiedseveralclinicalcasesofcholera precedingtheonsetoftheepidemicinseveralcoastal cities.Thendingwasinstrumentalbecauseitsuggested thattheintroductionofcholeraoccurredpriortothe arrivalofthepassingship,dismissingthatexplanation andembracingtheElNi ~ nohypothesis(Epstein1992; Colwell1996;Mourino-Perez1998).Furthermore,there waslaboratoryconrmationof V.cholerae inwater sources,includingsewage,rivers,lagoons,andirrigation (GomezPandoandPineda1991;Madicoetal.1996) precedingcholeraoutbreaksinLima,Peru(Francoetal. 1997;Speelmonetal.2000).AccordingtoFrancoetal. (1997),elevatedtemperaturesprecipitatedarisein bacteria,whichthenampliedoncehumanfecalcontaminationbegantoincrease.Importantly,asecond studydemonstratedaquantitativerelationshipbetween ENSOandcholerafrom1980to1998inBangladesh. CholeratransmissionwasexplainedbyENSO’steleconnectedinuenceonlocalair–watertemperatures and,subsequently,theintrusionofplanktonblooms ontothecoastalshore(Pascualetal.2000).4.RecountingtheevidenceinPeru a.AirtemperatureFollowingtheinitialoutbreakin1991,severalstudies foundtemperature-relatedassociationsthatsupported anElNi ~ noandcholeralinkinPeru.Itwasshownthat diarrhealdiseasesincludingcholeracorrelatedwiththe warmestmonths(e.g.,australsummer,December–March) inthe1990s.Specicallywhentemperaturesincreased togreaterthan19.5 8 Ctherewasalsoanincreasein choleraincidence(Madicoetal.1996;Speelmonetal. 2000).Furthermore,itwasestimatedthatanincreaseof 1 8 Cinmeanairtemperatureledtoincreasedrisk( ; 8.0%) ofdiarrheainchildrenandadults(Checkleyetal.2000; Lamaetal.2004). ElNi ~ no–relatedriskwasnotobserveduntiltheonset ofthe1997/98ElNi ~ no,whichbeganrapidlydeveloping inApril1997(WMO1999,29–38).Subsequently,record airtemperatureswereobservedinPerufromMayto December,whichmeantthatPeruvianswouldnotexperiencewinter(BellandHalpert1998).Theimpactson diarrheaandcholerariskweresevere.InnorthLima, diarrhearoseby35.0%inchildrenand47.5%inadults duringthewinterof1997(Salazar-Lindoetal.1997; Lamaetal.2004).Intermsofcholera,afteradeclinein 1AttheEmergingDiseasesWorkshopin1993(WoodsHole,MA), Dr.RitaR.Colwell,whilesupportiveofthepotentialityofaclimate mechanism,expressedherconcern saboutassumingcausationwithoutfurtherquantitativestudies. APRIL2013RAMI ´ REZETAL.151 8QDXWKHQWLFDWHG_'RZQORDGHG$087&

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1996,casesbegantonoticeablyriseinJuly1997.The rstoutbreakswerereportedinsouthernPeru,wherea choleraemergencywasdeclaredbySeptember(MINSA 1998a). AccordingtotheMinisteriodeSalud(MINSA;the MinistryofHealth),thegreatestburdenofdiarrheal diseasewasobservedduringtheaustralsummerin1998 (MINSA1998d;Huanca2004).Speelmonetal.(2000) reportedthat88.0%ofcholeracasesinLimaoccurred fromJanuarytoMay.ItwasalsoestimatedthatElNi ~ no conditionscontributedtoanexcessof6225dailyadmissionsofchildrenwithdiarrhea(Checkleyetal. 2000).Overallin1998,thenumberofcholeracasesin Peruroseby112.0%fromthepreviousyear(MINSA 2008).MINSAattributedtheriseincholeraanddiarrhealdiseasetoElNi ~ no(MINSA1998a,c,2000).b.SeasurfaceconditionsOtherstudiesinPerufocusedontheeffectsofsea surfaceconditionson V.cholerae andcholeraincidence alongthecoastofPeru.Inonestudy,Lippetal.(2003) foundthat V.cholerae wassignicantlycorrelatedwith airtemperatureincreaseseveryJanuarytoMarchfrom November1998toMarch2000.Furthermore, V.cholerae wasdetectedinplanktonsamplesatthreecoastalsites: Trujillo(north),Lima(central) , andArequipa(south). Interestingly,coastalseawatertemperaturewasnotasignicantfactor.Inalaterstudy,Giletal.(2004)revisited thesamestudyareasasLippetal.(2003)butincludedone additionalsiteatCallao(consideredpartofgreaterLima). Theyalsomeasuredenvironmentalvariablesinrelationto choleraincidenceandextendedthetimeperiodtobegin inOctober1997.Inthisstudy,monthlycholeraincidence wasstronglyassociatedwithelevatedseawatertemperatureduringtheaustralsummerof1998.Asintheprevious study, V.cholerae wasdetectedintheseawater;thissupportedtheexistenceofacoastalenvironmentalreservoir linkedtoseawaterchanges(Giletal.2004). Morerecently,thehypothesishasgainedfurthersupport inastudythatmodeledequato rialwavesduringthe1997/98 ElNi ~ nowiththeoccurrenceofaproxyvibriostraincalled Vibrioparahaemolyticus (Martinez-Urtazaetal.2008). Usingseaheightanomalyandupperoceanheatcontentto representElNi ~ no,theauthorsshowedthatthedistribution ofindexcasesofcholerafollowedapatternalongthewest coastofSouthAmerica,similartotheoceanicparameters.Coincidently,thispatternalsoresembledlocations wherecholerawasrstidentiedin1990/91,according toSeasetal.(2000).Thiswastherststudytodemonstratehowvibriosandtheirreservoirsmayhavetraveled viaoceanwavesanduponarrival(i.e.,againstthecontinentalboundary)dispersedalongthecoastalenvironmentofPeru(Martinez-Urtazaetal.2008).c.SummaryInsum,descriptiveandstatisticalstudieshaveshown aclimatelink,bothdirectandindirect,withcholera, V.cholerae ,andenvironmentalreservoirsinPeru.The associationswerebasedoninlandandcoastalwater temperaturesduringtheaustralsummerandclimate thresholdswhichsuggestedthatelevatedtemperatures ledtoagreaternumberofdiarrhealdiseasesinthe 1990s.WithrespecttoElNi ~ no,therewasanapparent associationwiththe1997/98event.Whilethesestudies providedsomeevidenceforaclimate–choleraconnectioninPeru,therearestillmanyunansweredquestions. Inthefollowingsection,weexploreseveralfactorsthat wearguearecriticaltounderstandingElNi ~ no’slinkto choleraemergenceandtransmissioninPeru.5.ReexaminingElNi ~ noandcholerainPeruHere,weuseaclimateaffairsapproachtoreexamine theassociationbetweenElNi ~ noandcholerainPeru usingabroaderconceptionofENSO.Ourdiscussion beginsbyrevisitingthetemperature-relatedassociation followedbyanexploratoryinvestigationthathighlights thefollowingENSOcharacteristics:thedenitionofan ENSOevent,rainfallextremes,theLaNi ~ nafactor,and socialvulnerability.a.RevisitingthetemperatureassociationWhileatemperature-relatedassociationisplausible becauseofitspotentialimpactonthereproductionof vibrios,itsgeneralizationinPeruislimitedbyitsgeographicscope.Thisisduetothefactthatprevious ndingsinPeruweregenerallybasedontemporalobservationsinLima,whichislocatedonthecentralcoast. Giventhecountry’sdiversephysicalregions,which rangefromalow-lyingcoasttohighlandsandjunglein theeast(Fig.2),itispossiblethattheremayhavebeen regionalvariationsofthetemperatureassociationwithin Peru.Forinstance,inLoreto,ajungleregionlocatedin northeastPeru,seasonalpatternsofcholerawereindeed differentfromtheLimatimeseries(Fig.3a).InLima, peaksincholeracaseswereobservedfromFebruaryto Aprilfrom1993to1998.Incontrast,choleraincreased inLoretofrommidsummertoearlyautumn(Julyto October)in1993,1995,and1998;therewerealsopeaks inMayof1993and1998(Fig.3b).Ingeneral,thetemporalpatternofcholerainLoretowaslesswelldened andlaggedintimecomparedtoLima.Thesedifferences mayreect,particularlyinthecaseof1998,thegeographyofElNi ~ no–relatedteleconnections.Forexample, onthecentralcoastElNi ~ nomaycontributetowarmer andwetterthanaverageconditionsfromJunetoAugust152WEATHER,CLIMATE,ANDSOCIETYVOLUME5 8QDXWKHQWLFDWHG_'RZQORDGHG$087&

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(SENAMHI2004);intheAmazon,itmaycontributeto rainfalldecitinNovemberandDecember(Marengo 1999;Marengoetal.2008).Importantly,theseregional differencessuggestnotonlythatdifferenttemporalpathwaysmightexist,butalsothat differentclimatepathways mayhaveimpactedcholeratransmission. Thetemperature-relatedassociationisalsolimited becauseElNi ~ no’slinktocholeraisbasedononeevent in1997/98.Forexample,eventhoughLamaetal.(2004) foundastrongassociationbetweenElNi ~ noanddiarrhealdiseasein1998,itwasalsoshownthatpriorEl Ni ~ noswerenotstatisticallysignicant.2Onereasonfor thisoutcomemayhavebeentheshortlengthoftime series(i.e.,1991–98),whichseemstolimitstudiesin Perubecausetheyhavegenerallybeencross-sectional anddonotincludetheinitialoutbreaktimesegment.b.DeÞnitionofanENSOeventOneimportantassumptionoftheElNi ~ no–cholera hypothesisisthatElNi ~ noconditionswerepresentin ordertoimpactthetransportandreproductionofcontaminatedplanktonoffthecoastofPeru,potentially fromOctober1990toJanuary1991[i.e.,basedonSeas etal.(2000)].AlthoughanElNi ~ nowassuspectedduring thattime,therewerealsovaryingreportsaboutthe timingofElNi ~ no(s)intheearly1990s.Forexample,for someresearchersitwasthelongestElNi ~ noofthecentury,lastingveyearsfrom1990to1995(Trenberthand Hoar1996).Forothers,itlastedonlyfromSeptember 1991toJuly1993(McPhaden1994;Kesslerand McPhaden1995).Itwasalsoestimatedthatthreeevents tookplaceduring1)March1991toJune1992,2)1993 (February/MarchtoOctober),and3)1994(Juneto November)(GoddardandGraham1997).Importantly, PeruviansquestionedtheviewofanElNi ~ noin1991 FIG.2.PhysicalmapofPeruhighlightingthreedepartments: Lima(centralcoast),Loreto(northjungle)andPiura(northcoast, discussedinsection5c).MapproducedbyIva ´ nJ.Ram ´ rez.Source: UniversityofPiura(private). FIG.3.Choleracases(suspectedandconrmed)bymonthfor eachyearfrom1993to1998intheDepartmentsof(a)Limaand (b)Loreto.Source:GeneralOfceofEpidemiology,MINSA, Lima,Peru. 2ItisimportanttonotethatitisunclearhowLamaetal.(2004) identiedElNi ~ nos.Accordingtotheirstudy,whichciteddatafrom NOAA,theonsetdateswere1)September1991,2)April1993,and 3)September1994. APRIL2013RAMI ´ REZETAL.153 8QDXWKHQWLFDWHG_'RZQORDGHG$087&

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becausetheynoticedtheywerecatchingnear-recordsettinganchovylandings,highlyunlikelyduringawarm episode(Flores1998;Glantz2001a,p.21).Therefore,two fundamentalquestionsaboutthehypothesisareraised. TherstiswhetheranElNi ~ nowasindevelopmentat thetimeofemergence.ThesecondiswhetherElNi ~ no’s effectswereobservedinPeru.Thelatterquestionisimportantbecauseitmayexplainthetransportandcoastal intrusioncomponentofthehypothesis. ToaddressthequestionaboutElNi ~ no’stiming,we exploredthedenitionofanENSOevent,whichdeterminesthecharacteristicsofanepisodeincludingits beginningandenddates(Trenberth1997).ThedenitionisimportantbecauseitmayaffecthowonecharacterizestherelationshipbetweenElNi ~ noandcholera emergence,whichisdependentonwhetherthetwo eventscoincidedintime.Toillustratethispoint,we comparedseasurfacetemperatureanomalies(SSTAs) inthreeNi ~ noregionswithmonthlycholeracasesinPeru from1990to1992.Asadenition,wechosetheoperationaloneusedbytheNationalOceanicandAtmosphericAdministration(NOAA),whichiscommonly employedtoidentifyanevent(seeNOAA2012).Figure4 showstheSSTAandcholeratimeseriesandTable1 listsElNi ~ noandLaNi ~ naevents,respectively.AccordingtotheNi ~ no-4region,therstpossiblecasesof cholera[identiedbySeasetal.(2000)]andtheonsetof theepidemicoccurredinthemidstofaprolongedEl Ni ~ no(26months)thatdevelopedinJuly1990(eventa). ThetimingintheNi ~ no-4region,whichrepresentsthe westernequatorialPacic,sustainstheElNi ~ no–cholera hypothesisandsuggestsatimedelayofseveralmonths betweenElNi ~ noandcholeraemergence.Ontheother hand,regionsNi ~ no-3.4andNi ~ no-1 1 2,whichrepresent thecentralandeasternequatorialPacic,indicatethat ElNi ~ noconditionsfollowedtheinitiationoftheepidemic,beginninginMay(eventc)orNovember(eventd) of1991.UsingPearson’scorrelationanalysis,weexploredtheseassociationsfurtherandfoundthestrongest linkbetweencholeraandSSTAintheNi ~ no-1 1 2region ( r 5 0.42, p value 5 0.010).Thisndingisimportant becausetheNi ~ no-1 1 2regionincludescoastaland equatorialupwellingnearPeruandEcuador(Glantz 2001a,p.60),whichexhibitednon–ElNi ~ noconditions precedingandduringtheinitialoutbreakinJanuary 1991(seeFig.4andTable1d).Thus,itsuggeststhat ENSOneutralorLaNi ~ naconditionsratherthanEl Ni ~ nomayhavecontributedtocholeraemergencein Peru.ELNI ~ NO’SEFFECTSIN1991?ToexplorethetimingofElNi ~ nofurther,weexamined theliteraturetoidentifyElNi ~ no–relatedimpactson ecosystemsandclimateinPeru.Onepotentialeffectwe lookedforistheimpactonanchovy,pelagicshwhose habitatandfoodsupplyarealteredwhenupwelling weakensduringElNi ~ nos(Chavezetal.2008).AccordingtothePeruvianMarineInstitute,1991wasdescribed asayearwithcoldcoastalwatersandgoodforanchovy catch(Pizarro1999),whichimpliedthataverageSST conditionswerepresentoffthecoastofPeruandthat upwellingandmarinebiologicalproductivitywasnormaltoo.Wealsolookedforecosystemimpactsinother areasoftheeasternPacicOcean.Forexample,biologicalimpacts(associatedwithElNi ~ no)werereportedoffthecoastofCostaRica(e.g.,coralbleaching andmortality)inMarchtoApril1992(Jime ´ nezand Corte ´ s2001),intheGalapagos(e.g.,penguinpopulationsdeclinedassociatedwithlowerfoodsupply) from1991to1993(HernanVargasetal.2006),andoff thecoastofChile(e.g.,changesinplankticfaunaspecies)fromNovember1991toMarch1992(Marchant etal.1998).Withregardtoimpactsonlocalclimate (teleconnections),NOAAreportedintenserainson thenorthcoastofPeruduringtheaustralsummerof FIG.4.MonthlySSTanomalies( 8 C)inthreeNi ~ noregions(1 1 2, 3.4,and4)areplottedinrelationtomonthlycholeracases(suspectedandconrmed)inPerufrom1990to1992.SSTanomalies arebasedontheperiod1971–2000.SeeTable1forENSOevents a–d.Sources:GeneralOfceofEpidemiology,MINSA,Lima, Peru,andNOAA(http://www.cpc.noaa.gov/data/indices/). TABLE1.ListingsofElNi ~ noandLaNi ~ naeventsfrom1990to 1992asdenedbySSTAexceeding 6 0.5 8 Cthreshold.EachqualifyingeventisgivenalongwiththeNi ~ noregion,phase,andstart andenddates. EventRegionPhaseBeginEndDuration ANi ~ no-4ElNi ~ noJul1990Aug199226 BNi ~ no-1 1 2LaNi ~ naJul1990Dec19906 CNi ~ no-3.4ElNi ~ noMay1991Jul199215 DNi ~ no-1 1 2ElNi ~ noNov1991Jun19928154WEATHER,CLIMATE,ANDSOCIETYVOLUME5 8QDXWKHQWLFDWHG_'RZQORDGHG$087&

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1992.Apparently,anElNi ~ nothatbegandevelopingin mid-1991wasinamaturephase(NOAA1992,1993). SupportingtheNOAAobservationswerelocalnewspaperaccountsthatdocumentedstorms,inundations anddisasters(ElTiempo1992a,b).Asmentionedpreviously,thenorthcoastofPeruisstronglyassociated withElNi ~ noandrains(Lagosetal.2008)andisthereforeagoodindicatorofawarmeventinPeru.Although speculative,biologicalchangesinmarineecosystems alongwithphysicalimpactsinmid-to-late1991/early 1992supporttheideathatElNi ~ nomayhavefollowed ratherthanledtheonsetofthecholeraepidemicin1991.c.RainfallextremesInadditiontotemperature,rainfallextremesareimportantElNi ~ noteleconnections.InPerutheymayhave beenapathwayforcholeratransmission.Rainfallextremescaninuencetheconcentrationandtransportof V.cholerae andenvironmentalhosts(Ruiz-Moreno etal.2007;Hashizumeetal.2008;Mendelsohnand Dawson2008;Akandaetal.2009;Reineretal.2011; Bertuzzoetal.2012;Rinaldoetal.2012).Inparticular, heavyrainscancontributetonutrientrunoff,whichin turnmaypositivelyaffectplanktonbloomsincoastal areas(ConstantindeMagnyetal.2008;Jutlaetal.2011); furthermore,wind-drivenraincandrivecoastalwaters withplanktoninland,therebyincreasinghumaninteractionswith V.cholerae (ConstantindeMagnyetal. 2008).Heavyrainscanalsoincreasecholerarisk throughoodingandoverowofriversandsubsequent contaminationofthewatersupply(Kovatsetal.2003; Ruiz-Morenoetal.2007;Akandaetal.2009;Reiner etal.2011).Forexample,duringtherecentcholera epidemicinHaiti,intenserainsincreasedincidencein 2010–11byenhancingsurfacerunoffandtransportof fecalmatterfromopenlatrinestoinlandwatersources (Rinaldoetal.2012).InPeru,choleramayhavespread viarainsinlow-lyingareasinthedepartmentofPiura (seeFig.2),whichreportedindexcasesin1991(Ries etal.1992).Figure5comparescholeracaseswithrainfall(inmm)inJanuarytoAprilfrom1991to2000in asubregionofPiura(located860kmnorthofLima). CholeraandrainfallincreasesinPiurawereclearlyevidentin1992and1998.Furthermore,duringtheonsetof choleraandtherstquarterof1991(i.e.,October1990 toApril1991),totalrainfallinPiurawas7mmcomparedto329mmin1992and1842mmin1998.Together,theseobservationsalongwithlocalreports suggestthatooding,possiblyviathebreakdownof waterandsanitationinfrastructures,ledtoenhanced choleratransmissioninPiura(ElTiempo1992a,b; PAHO1998b;MINSA1998b,d).Althoughelevated temperaturesmayhavecontributedtocholeraincidence inLima,heavyrainsmayhavebeenamoreimportant factorinnorthernPeru.Alternatively,rainfalldecit mayhavecontributedtocholeratransmissionaswell FIG.5.Choleracases(inhundreds)andrainfall(mminhundreds)forJanuarytoAprilfor 1991to2000attheMiraoresmeteorologicalstation(5.17 8 S,80.6 8 W;30ma.s.l.)inthesubregionofPiura,Peru.Sources:MINSA,PiuraandUniversityofPiura(private),Peru. APRIL2013RAMI ´ REZETAL.155 8QDXWKHQWLFDWHG_'RZQORDGHG$087&

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(Codeco2001;Pascualetal.2002;Hashizumeetal.2008; Akandaetal.2009).Forexample,inthejungleregionof Loreto,whichwediscussedearlier,lowriverlevelswere associatedwithcholerariskinplacesofpoorwaterand sanitationinfrastructures(MINSA1995,1998b).Adry seasonalongwithelevatedairtemperaturescanimpact bacteriaandincreasecholerariskduetolimitedavailabilityofpotablewater(Codeco2001;Huqetal.2005).d.TheLaNi ~ nafactorLaNi ~ na,thecoldphaseofENSO,isanotherpathway thatmayhaveimpactedcholeratransmissioninPeru.La Ni ~ naenhancesaverageSSTconditions(e.g.,cold)inthe easternequatorialPacicOcean.Therefore,viaits positiveinuenceonupwelling,whichbringsnutrients tothesurfacewaters,LaNi ~ namayhavecontributedto choleraemergence(wediscussthispathwaywithin abroadercontextoftheElNi ~ no–cholerahypothesisin thenalsection).Aswell,LaNi ~ namayhaveincreased cholerariskthroughitsownsetofteleconnections (RopelewskiandHalpert1987;Ordinola2002;NOAA 2011).DuringLaNi ~ na,climateinPeruisdrierthan averageonthenortherncoast(Ordinola2002)and wetterthanaverageinthesouthernandcentralAndes, particularlyintheAltiplano,whichbordersBoliviaand Chile(Sperlingetal.2008).Followingthe1997/98El Ni ~ no,rain-relateddisasterswerereportedinthehighlandsinFebruary1999.Subsequently,populationswere affectedbyoodsandmanywereinneedofassistance withfood,water,andsanitation(MINSA1999a).La Ni ~ naconditionsalongwiththoseinthetropicalAtlantic wereblamed(MINSA1999b).e.SocialvulnerabilityWhencholeraemergedin1990/91,thePeruvian governmentwasalreadyaddressingcomplexemergencies,whichbeganearlierthatyearinlatesummer/early winter.TherstwasanearthquakeinnortheastPeru, whichaffected70000andinjured1500peopleinMay 1990(UNDRO1990a).Thesecondwasanagricultural stateofemergencydeclaredacrosshighlandregionsin June1990.Itwasreportedthatover2millionsubsistencefarmersweregravelyaffectedbyanongoing droughtandcoldextremesexperiencedin1989,reportedlyaLaNi ~ nayear;consequently,foodandwater supplieswereindecline(UNDRO1990b).Thataustral winterwasalsothebeginningof‘‘Fujishock,’’asetof economicreformsimplementedbythethen-elected PresidentAlbertoFujimori(Brooke1990).Asaresult ofthesepolicies,publicinfrastructureandserviceswere reducedincludingthoseinthehealthsector,whereresourceswerealreadylimited(Cueto2001,107–137). Furthermore,thecountrywascontendingwithan energycrisis(ElTiempo1991;Nash1991;Youngers 2000).Poweroutagesaffectingwaterandsanitation plantsandresidentswerereported(ElTiempo1991). Ultimately,theseevents,whichincludedpublicpolicies, mayhaveaggravatedthepreexistinglivingconditionsof thepopulation,wholackedimmunitytocholeraand lackedadequatewaterandsanitationinfrastructure.3If ENSOanditsinuenceonclimateandsocietyhadan impactoncholerainPeru,itcouldnothaveoccurred apartfromsocialvulnerability.6.SummaryandconclusionsAlthoughcholerawaseradicatedinPeruin2002 (MINSA2005),it remainsapotentialthreattothe countryandregionbecauseoftherecentemergencein Haiti,whichwasalsoassociatedwithENSO(Enserink 2011).Therefore,thisresearchistimely,andsupports otherstudiesthatseektounderstandhowclimatevariabilityaffectscholeraepidemics(Pascualetal.2000; Koelleetal.2005;ConstantindeMagnyetal.2007; Reineretal.2011;Reyburnetal.2011).Insum,this studyexaminedtherelationshipbetweenElNi ~ noand cholerainPeruusingaclimateaffairsapproach.From thisholisticview,weexplainedcholeraincidencefrom abroaderconceptionofENSO,onewhichincludesnot onlytemperaturebutalsogeographicvariability,how wedeneENSO,theimpactsofrainfallandLaNi ~ na, andunderlyingsocialdimensions.Indoingso,welinked ENSOtocholerainPeruthroughmultiplepathways. Specically,ourstudyshowedthatatemperature– choleraassociationmayhavedifferedtemporallybetweenregionsbecauseofgeographyandthevariability ofElNi ~ noteleconnectionswithinPeru(e.g.,varying cholerapeaksbetweencoastandjungle).Itwasalso shownthatanotherpathwaymayhavebeenrainfall extremes(e.g.,torrentialrainsonthenorthcoast),which impactedinfrastructure,riverlevels,andwatersupply, leadingtoincreasedexposuretocholera.Heavyrains werelikelyacriticalfactorin1992and1998duringEl Ni ~ nos.Importantly,whenweexploredthedenitionof anENSOevent,ouranalysisrevealedthatcholeramay haveemergedinPeruduringENSOneutralorLaNi ~ na conditionsratherthanElNi ~ noconditions.Ourinterpretation,whichdisputesthepresenceofElNi ~ noin thepriorandonsetmonthsofthecholeraepidemic,is 3In1991approximately45.0%ofPeru’spopulationdidnothave accesstocleanwaterand59.0%werewithoutsanitationservices. Inruralareas,conditionsweremuchworse;there,lessthanonethirdofthepopulationhadaccesstocleanwaterandotherbasic services(PAHO1991).156WEATHER,CLIMATE,ANDSOCIETYVOLUME5 8QDXWKHQWLFDWHG_'RZQORDGHG$087&

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supportedbyasignicantcorrelationbetweencholera andseasurfacetemperaturesintheNi ~ no-1 1 2region,an areaproximatetothePeruviancoast.Ourstudyalso highlightsthatbiologicalandphysicalevidenceofEl Ni ~ nowasnotobserveduntiltheendof1991,whichsupportsfurtherthatElNi ~ nodidnotcoincidewiththeinitial epidemic.Inlightofthesendings,ourstudyoverall suggeststhatthecholeraepidemicinPeruwaslikelyalreadyunderwaybythetimeElNi ~ nodevelopedin1991. Therefore,thewarmphaseofENSOcouldnothave impactedtheonsetorinitiationofthecholeraoutbreak inPeru. However,ourndingsdonotprecludeanENSOor climatecontribution.Instead,ourstudysuggeststhat non–ElNi ~ noconditionsmayhaveplayedacontributive roleduringcholeraemergence.Non–ElNi ~ noconditions areindicativeofrichbiologicalproductivityduetoupwellingprocessesthatmayhavepositivelyinuenced planktonreservoirsinlate1990and/orearly1991.Concurrently,multiplicationofplanktonandvibriosinthe coastalzonemayhaveoccurredbecauseofeutrophicationduetohumanactivities(e.g.,agriculturerunoffand sewagedumping)(Epstein1992,1993).Vibriosmayhave alsoincreasedinpopulationduetoseasonalwarming ofSSTandairtemperaturesduetotheonsetofsummer inDecember.Thisassociationisplausiblegiven thatcholeraanddiarrhealdiseasewerecorrelated withwarmermonthsfollowingtheinitialoutbreakin January1991(Salazar-Lindoetal.1997;Checkleyetal. 2000;Speelmonetal.2000).Humantransmissionmay havetakenplacebyconsumptionofcontaminated seafood(e.g.,shellsh),whichwasaninitialvehicleof infectioninPeru(MINSA1994),andsuggestedoriginallybyEpstein(1993).Oncecholerawasintroducedto thecoastalinland,localtransmissionwasampliedby humanfecalcontamination(Francoetal.1997),andthen propagatedunderthesocialvulnerabilitycontext,which wedescribedearlierandwasreportedwidely(PAHO 1991;MINSA1994;Cueto2001,107–137). ItwasmorelikelythatElNi ~ no’simpactarrivedmuch laterthantheinitialoutbreakin1991,contributingto choleratransmissionintheaustralsummerof1992via themechanismproposedbyColwell(1996).Morespecically,thismultiplepathwayoccursasfollows:with thearrivalofKelvinwaves,whichcarrywarmwaters fromthewesternPacic,SSTincreasedandsealevelrose alongthecoastofPeru.Thepoolofanomalouswarm waterspositivelyaffectedthereproductionofvibrios livinginthecoastalzone.Withrespecttoplankton reservoirs,theirproliferationwaspotentiallyinuenced bythreefactorsassociatedwithnutrientenrichment. Therstfactorisrelatedtohumanactivities(Epstein 1993;Epsteinetal.1993),whichwementionedpreviously. Thesecondfactorisnutrientenrichmentbyrunoffdue tohighriverdischarge(Jutlaetal.2011),whichmayoccur duringstrongElNi ~ nos(LavadoCasimiroetal.2012). Jutlaetal.(2011)reportthatthisisthemaindriverof planktonbloomsratherthanrisingSSTincoastalBangladesh,andthereforethismayhavebeenanimportant pathwayin1992.Thethirdfactorisupwelling,which mayappearcounterintuitiveatrst.However,whileitis likelythatequatorialupwelling(nearEcuador)isnegativelyaffectedduringElNi ~ nos(NOAA2011),itisnot alwaystrueforcoastalupwellingnearPeru.There,upwellingdiminishesbygeographicextent(shiftingcloser tothecoast)butcontinuestopersistandevenintensify duringwarmepisodesaswindsblowingtowardthecoast increase(Eneld1981).Itexplainswhyplanktonspecies couldremainhighunderwarmanomalousSSTconditionsduringpastElNi ~ noevents(BarberandChavez 1983;Chavez1996).Oncevibriosandreservoirsmultipliedonthecoast,risingsealevelheightsandstorm surgesledtocoastalintrusiontransportingorganismsto theinland,whereteleconnections(e.g.,warmerairand watertemperaturesandheavyrains)affectedtheirreproductionanddistribution.Impactsoncholera,however,variedbygeographicregion,dependingonthe hydrology(Akandaetal.2009;Bertuzzoetal.2012; Rinaldoetal.2012),infrastructure,andimmunitylevels ofthepopulation(Koelleetal.2005;Marietal.2012; Rinaldoetal.2012).Withinapoorinfrastructurecontext,rainfallimpactsledtocollapseofwaterandsanitationsystemsalongthecoast,morelikelyinthenorth whereElNi ~ noimpactsarestrongest,resultingin heightenedtransmissioninthesummermonthsof1992. Althoughwecannotexplaintheinitialsourceof choleraemergenceinPeru,wecanassumethatifEl Ni ~ noconditionswerenotpresentintheeasternequatorialPacicduringtheinitialoutbreak,itisunlikely thatdistantvibrioswouldhavetraveledviaElNi ~ no– relatedoceanwavesin1990/91.TheanswertotheoriginsofcholerainPeruismorelikelytobefoundinan explanationthatcombinesinformationfromexisting hypotheses(bothhumanimportationandclimate)with currentadvancementsinthemicrobiologyandgenetics of V.cholerae .Mostrecently,thelatterhashelped conrmthesourceofcholeraemergenceinHaiti(Chin etal.2011),whichattributedtheintroductiontoforeign importationbyasymptomaticindividuals(Piarrouxetal. 2011;Craviotoetal.2011).InPeru,theideaofhuman importationremainsaviablepathwaytoinvestigate givenarecentgeneticstudythatsuggeststheLatin Americanstrainof V.cholerae camefromAfrica,possiblybyhumanmigration(duringsomeundenedtime period)followingthearrivaloftheseventhpandemicin thatcontinentinthe1970s(Lametal.2010).ItmayhelpAPRIL2013RAMI ´ REZETAL.157 8QDXWKHQWLFDWHG_'RZQORDGHG$087&

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explainhow V.cholerae mayhavebecomeindigenousto thecoastofPerupriortotheemergencein1990/91and then‘‘evolvedindependently’’throughgenetictransfer between V.cholerae strains(BlokeschandSchoolnik 2007;Nusrinetal.2009). Inconclusion,itishopedthatthisresearchwillstimulatenewpointsofinvestigationsinPeruandinother areaswherecholeraisemergentorreemerging.Tobegin,futureworkshouldconsidereachdimensionof ENSObecauseeachcanserveasapotentialpathway thatlinksENSOtodiseaseincidence.Moreover,quantitativestudiesarenecessarytoestimatetherelationship betweeneachpathway(describedinthisstudy)and cholera.Forexample,inordertobetterunderstandthe temporalpatternsofcholerabyregion,itmaybeuseful toutilizetimeseriesmethods,suchaswavelet,toidentifychangesintheclimate–cholerarelationshipacross time–frequencyspace(Cazellesetal.2007),includinglag effects.Suchataskwillrequireresearcherstoexamine theentirerecordduringwhichcholerawaspresentin Peru(1990/91to2002)inordertocaptureENSO’squasiperiodicity.Furthermore,thecharacteristicsofvarious ENSOeventsshouldbeexploredtounderstandhowan event’sevolutionandmagnitude(e.g.,degreeofimpact onSST),whichisuniquetoeachevent,canimpact transmission.Itmayexplainwhycholeradidnotemerge duringthesecondstrongesteventofthecentury,which occurredin1982/83,whenhealthimpactswerereported inPeru(Gueri1984).Equallyimportantisthenecessity toconsiderthemodifyingeffectsofnonclimaticfactors, whichmayalsoaddresscholeraemergenceandtransmissionquestionsinPeru.Thesefactorsincludesocial variables,suchassocioeconomicstatusandinfrastructure(Sasakietal.2009;Emchetal.2010;Mari etal.2012),immunity,whichinuencesbiological susceptibility(Koelleetal.2005;Rinaldoetal.2012), andhumanmigration,whichenablesconnectivitybetweeninfectedandsusceptiblepopulations(Koelleetal. 2005;Marietal.2012). Acknowledgments. Thisstudywassupportedthrough grantsatthefollowinginstitutionsatMichiganState University:DepartmentofGeography,Departmentof Philosophy(EthicsandDevelopmentSpecialization), CenterforLatinAmericanandCaribbeanStudies,and theGraduateSchool.Supportwasalsoprovidedby CCBinBoulder,Colorado.SpecialthankstoIng. NormaOrdinola,UniversityofPiura(Private),Ing. GroverOtero,ProyectoChira-Piura,Dr.ElsaGalarza, UniversityofPacico,JoannaNoeliaKamicheZegarra, UniversityofPac ´ co,andDr.LuisMiguelCastrovVfor facilitatingeldworkinLimaandPiura.Wealsothank alltheinstitutionsthatprovideddataanddocumentsin PeruincludingMINSAinLima andPiura,INEIinPiura, andDr.AnaI.Gil(NationalInstituteofNutrition Research).WealsothankNewCollegeofFloridafor providingthespacetocompletethisarticle.Finally,we acknowledgeDr.LinoNaranjoD ´ az(MeteoGalicia) andDr.KimKnowlton(NRDC)fortheircommentsand expertiseontherstdrafts.REFERENCES Akanda,A.S.,A.S.Jutla,andS.Islam,2009:Dualpeakcholera transmissioninBengalDelta:Ahydroclimatologicalexplanation. Geophys.Res.Lett., 36, L19401,doi:10.1029/ 2009GL039312. Barber,R.T.,andF.P.Chavez,1983:Biologicalconsequencesof ElNi ~ no. Science, 222, 1203–1210. Bell,G.D.,andM.S.Halpert,1998:Climateassessmentfor1997. Bull.Amer.Meteor.Soc., 79, S1–S50. 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