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Decreasing incidence of Plasmodium vivax in the Republic of Korea during 2010–2012

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Title:
Decreasing incidence of Plasmodium vivax in the Republic of Korea during 2010–2012
Physical Description:
Mixed Material
Language:
English
Creator:
Kim, Tong-Soo
Kim, Jin Su
Na, Byoung-Kuk
Lee, Won-Ja
Lim, Heung-Chul
Youn, Seung-Ki
Gwack, Jin
Publisher:
Bio-Med Central (Malaria Journal)
Publication Date:

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Abstract:
Background: After the re-emergence of Plasmodium vivax in 1993, a total of 31,254 cases of vivax malaria were reported between 1993–2012 in the Republic of Korea (ROK). The purpose of this study was to review Korea Centers for Disease Control and Prevention records to investigate the transmission of malaria from 2010–2012. Methods: Reporting of microscopy-diagnosed cases of malaria is mandatory in the ROK. In this study, all available records of malaria cases and malaria vectors collected from 2010 – 2012 in Cheorwon County, Gangwon Province and Ganghwa County, Incheon Metropolitan City, were reviewed. Results: Although the number of cases of malaria peaked a third time in 2010 (1,772 cases) since the re-emergence of P. vivax, the incidence decreased two-fold to 838 in 2011 and three-fold to 555 in 2012. The number of cases decreased 52.7% in 2011 compared with that in 2010 and 33.8% in 2012 compared with that in 2011. However, the number of cases increased in Incheon Metropolitan City (15.3%) and Gyeongnam Province (23.1%) in 2012 compared with 2011. Of the 3,165 cases of vivax malaria in 2010–2012, 798 (25.2%) were in ROK military personnel, 519 (16.4%) in veterans, and 1,848 (58.4%) in civilians. In total, there were 2,666 male patients and 499 female patients, and the ratio of female to male patients increased from 1:7.9 in 2011 to 1:4.1 in 2012. Conclusions: A rapid decrease in the incidence of malaria was observed in most areas from 2010 to 2012, but the incidence increased again in the western part of the demilitarized zone. Therefore, more intensive surveillance is needed throughout high risk areas to identify factors responsible for increase/decrease in the incidence of malaria in the ROK
General Note:
Kim et al. Malaria Journal 2013, 12:309 http://www.malariajournal.com/content/12/1/309
General Note:
doi:10.1186/1475-2875-12-309 Cite this article as: Kim et al.: Decreasing incidence of Plasmodium vivax in the Republic of Korea during 2010–2012. Malaria Journal 2013 12:309. Submit your next manuscript to BioMed Central and take full advantage of: • Convenient online submission • Thorough peer review • No space constraints or color figure charges • Immediate publication on acceptance • Inclusion in PubMed, CAS, Scopus and Google Scholar • Research which is freely available for redistribution Submit your

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Material Information

Title:
Decreasing incidence of Plasmodium vivax in the Republic of Korea during 2010–2012
Physical Description:
Mixed Material
Language:
English
Creator:
Kim, Tong-Soo
Kim, Jin Su
Na, Byoung-Kuk
Lee, Won-Ja
Lim, Heung-Chul
Youn, Seung-Ki
Gwack, Jin
Publisher:
Bio-Med Central (Malaria Journal)
Publication Date:

Notes

Abstract:
Background: After the re-emergence of Plasmodium vivax in 1993, a total of 31,254 cases of vivax malaria were reported between 1993–2012 in the Republic of Korea (ROK). The purpose of this study was to review Korea Centers for Disease Control and Prevention records to investigate the transmission of malaria from 2010–2012. Methods: Reporting of microscopy-diagnosed cases of malaria is mandatory in the ROK. In this study, all available records of malaria cases and malaria vectors collected from 2010 – 2012 in Cheorwon County, Gangwon Province and Ganghwa County, Incheon Metropolitan City, were reviewed. Results: Although the number of cases of malaria peaked a third time in 2010 (1,772 cases) since the re-emergence of P. vivax, the incidence decreased two-fold to 838 in 2011 and three-fold to 555 in 2012. The number of cases decreased 52.7% in 2011 compared with that in 2010 and 33.8% in 2012 compared with that in 2011. However, the number of cases increased in Incheon Metropolitan City (15.3%) and Gyeongnam Province (23.1%) in 2012 compared with 2011. Of the 3,165 cases of vivax malaria in 2010–2012, 798 (25.2%) were in ROK military personnel, 519 (16.4%) in veterans, and 1,848 (58.4%) in civilians. In total, there were 2,666 male patients and 499 female patients, and the ratio of female to male patients increased from 1:7.9 in 2011 to 1:4.1 in 2012. Conclusions: A rapid decrease in the incidence of malaria was observed in most areas from 2010 to 2012, but the incidence increased again in the western part of the demilitarized zone. Therefore, more intensive surveillance is needed throughout high risk areas to identify factors responsible for increase/decrease in the incidence of malaria in the ROK
General Note:
Kim et al. Malaria Journal 2013, 12:309 http://www.malariajournal.com/content/12/1/309
General Note:
doi:10.1186/1475-2875-12-309 Cite this article as: Kim et al.: Decreasing incidence of Plasmodium vivax in the Republic of Korea during 2010–2012. Malaria Journal 2013 12:309. Submit your next manuscript to BioMed Central and take full advantage of: • Convenient online submission • Thorough peer review • No space constraints or color figure charges • Immediate publication on acceptance • Inclusion in PubMed, CAS, Scopus and Google Scholar • Research which is freely available for redistribution Submit your

Record Information

Source Institution:
University of Florida
Holding Location:
University of Florida
Rights Management:
All rights reserved by the source institution.
System ID:
AA00017970:00001


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RESEARCHOpenAccessDecreasingincidenceof Plasmodiumvivax inthe RepublicofKoreaduring2010 – 2012Tong-SooKim1,JinSuKim1,Byoung-KukNa2,Won-JaLee3,Heung-ChulKim4,Seung-KiYoun5,JinGwack5, HeeSungKim5,PyoYunCho1,SeongKyuAhn1,SeokHoCha6,Yun-KyuPark1,SungKeunLee7,Yoon-JoongKang8, YoungjooSohn9,YeongseonHong10andHyeong-WooLee11*AbstractBackground: Afterthere-emergenceof Plasmodiumvivax in1993,atotalof31,254casesofvivaxmalariawere reportedbetween1993 – 2012intheRepublicofKorea(ROK).ThepurposeofthisstudywastoreviewKorea CentersforDiseaseControlandPreventionrecordstoinvestigatethetransmissionofmalariafrom2010 – 2012. Methods: Reportingofmicroscopy-diagnosedcasesofmalariaismandatoryintheROK.Inthisstudy,allavailable recordsofmalariacasesandmalariavectorscollectedfrom2010 – 2012inCheorwonCounty,GangwonProvince andGanghwaCounty,IncheonMetropolitanCity,werereviewed. Results: Althoughthenumberofcasesofmalariapeakedathirdtimein2010(1,772cases)sincethere-emergence of P.vivax ,theincidencedecreasedtwo-foldto838in2011andthree-foldto555in2012.Thenumberofcases decreased52.7%in2011comparedwiththatin2010and33.8%in2012comparedwiththatin2011.However,the numberofcasesincreasedinIncheonMetropolitanCity(15.3%)andGyeongnamProvince(23.1%)in2012 comparedwith2011.Ofthe3,165casesofvivaxmalariain2010 – 2012,798(25.2%)wereinROKmilitarypersonnel, 519(16.4%)inveterans,and1,848(58.4%)incivilians.Intotal,therewere2,666malepatientsand499female patients,andtheratiooffemaletomalepatientsincreasedfrom1:7.9in2011to1:4.1in2012. Conclusions: Arapiddecreaseintheincidenceofmalariawasobservedinmostareasfrom2010to2012,butthe incidenceincreasedagaininthewesternpartofthedemilitarizedzone.Therefore,moreintensivesurveillanceis neededthroughouthighriskareastoidentifyfactorsresponsibleforincrease/decreaseintheincidenceofmalaria intheROK.BackgroundPlasmodiumvivax isthecausativeagentofrelapsingbenigntertianhumanmalaria,thesecondmostcommon typeofmalariainhumans,thatafflictsseveralhundred millionpeopleannuallyintheworld.Vivaxmalariaisa majorpublichealthprobleminmanytropicalandsemitropicalregionsandtemperatecountries,includingthe DemocraticPeople ’ sRepublicofKorea(DPRK)andthe RepublicofKorea(ROK)[1]. Thefirstscientificdocumentationofmalariawaspublishedin1913,althoughithadbeenprevalentthroughout theKoreanpeninsulaforseveralcenturies[2].Asaresult ofanationalmalariaeradicationprogrammeconductedin cooperationwiththeWorldHealthOrganization(WHO), theincidenceofvivaxmalariaintheROKrapidlydecreaseduntilin1979whenWHOdeclaredtheROKtobe malariafree[3-5].Inthe1980 ’ stwosporadiccaseswere detected[6]andin1993,aROKsoldierservingin northernGyeonggiProvince [7],andtwocivilianswere diagnosedwithvivaxmalaria[8].Thereafter,anumber ofmalariacaseswerereportednearthedemilitarized zone(DMZ),whichcentersonPaju-si,Yeoncheon-gun, Cheorwon-gun,Gimpo-si,Ganghwa-gun,Goyang-si,and Dongducheon-si. Duringthefirstfewyearsofre-emergenceofvivax malariaintheROK,mostcasesoccurredinROKmilitary personneldeployedneartheDMZ.Butsomecivilians wholiveinDaeseongdongwherelocatedinsideofDMZ andTongilchonsurroundedbyROKmilitaryinstallations *Correspondence: rainlee67@naver.com11DepartmentofPathology,Immunology,andLaboratoryMedicine,College ofMedicine,UniversityofFlorida,J-566,1275CenterDrive,Gainesville,FL 32610,USA Fulllistofauthorinformationisavailableattheendofthearticle 2013Kimetal.;licenseeBioMedCentralLtd.ThisisanOpenAccessarticledistributedunderthetermsoftheCreative CommonsAttributionLicense(http://creativecommons.org/licenses/by/2.0),whichpermitsunrestricteduse,distribution,and reproductioninanymedium,providedtheoriginalworkisproperlycited.Kim etal.MalariaJournal 2013, 12 :309 http://www.malariajournal.com/content/12/1/309

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neartheDMZshowedhighinfectionrateasmuchas ROKmilitarypersonnel.Inaddition,asthenumberof malariacasesincreased,theratioofciviliancaseswere increased[9]. Thus,itwasofconsiderableconcernthatvivaxmalaria mightbecomere-establishedthroughouttheROKas veteransoldiersreturnedtotheirhometownsthroughout allofKorea[10-12]. Theaimofthisstudywastodeterminetheannualnumberofpatientswithmalariaamongmilitarypersonnel,veterans,andciviliansintheROK;themeandailyincidence forweeklyintervals;thegeographicdistributionofcases amongmilitarypersonnelandcivilians;andthenumberof Anopheles mosquitoescapturedbyblacklighttrapinthe malariariskfrom2010 – 2012toanalysethecurrentstatus ofmalariaintheROK.MethodsEthicsstatementAllparticipantswereinformedaboutthestudymethodologyandprovidedwritteninformedconsentaccordingto ethicalstandards.Thestudyprocedures,potentialrisks, andbenefitswereexplainedtoallparticipants.Alladult participantsandparents/guardiansinthehouseholdof participantsunder18yearsofageprovidedinformedconsent.Parentswhowereunwillingtohavetheirchildren participateinthestudywereidentifiedandtheirchildren subsequentlyexcludedwithoutprejudicefromstudysurveys.Allpatientdatawereanonymous.TheHumanEthics CommitteeofInhaUniversityprovidedethicalapproval, andthisstudywasconductedaccordingtotheprinciples expressedintheDeclarationofHelsinki.DatacollectionfrompatientswithmalariaMalariaisclassifiedasoneoftheGroupIIIcommunicable diseasesthatshouldbecontrolledbytheKoreangovernment.Fortheconvenienceofdataanalysis,patientswith malariawerecategorizedascivilians,veterans,andmilitarypersonnel.Forciviliansandveterans(whowerediagnosedwithvivaxmalariawithin24monthsofdischarge frommilitaryserviceinmalariaepidemicareas),casesof malariadetectedinprivatehospitalsorclinicsarereported tothelocalPublicHealthCenter(PHC).ThedatacollectedbythePHCsisprovidedperiodicallytotheDivision ofInfectiousDiseaseSurveillance,KoreaCentersfor DiseaseControlandPrevention.Formilitarypersonnel, casesofmalariaarereportedtotheOfficeoftheSurgeon General,ArmyHeadquarters,andtheMinistryofHealth andWelfare[13].Thereportusuallycontainsthepatient ’ s name,age,sex,address,dateofonsetofillness,dateof diagnosisofmalaria,andestimatedareaswherepossibly infected.Mostcasesofmalariadiagnosedincivilian hospitalorhealthclinicsincludeveterans,butmight alsoincludeROKsoldierswhowerediagnosedwhile leave.However,thesecasesamongROKsoldiersare excludedfromthecivilian/veteranpopulationsbythe DivisionofInfectiousDiseaseSurveillance,sincethepatientsarecontacteddirectlyaspartoftheverification process[14,15].DefinitionofmalariaThickandthinbloodfilmsobtainedfromsuspected malariapatientswerefixedwithmethanolandstained withGiemsadilutedwithbufferedwateratpH7.2in accordancewithstandardprocedure[16].Toestimate thedensitiesofblood-stageparasites,thenumbersof parasiteswerecountedrelativeto200whitebloodcells (WBCs)andthentheparasite/WBCratiowasmultiplied by8,000(estimatednumberofWBCspermicrolitreof blood)[17].GeographicdistributionofpatientswithmalariaTheannualgeographicdistributionof P.vivax malaria incivilians,veterans,andROKmilitarypersonnelwas determinedbythepatientsresidenceandtravelhistory duringdiagnosis.Theseasonalincidencewasanalysed bygroupingcasesatweeklyormonthlyintervals.CalculationoftheannualparasiteincidenceTheannualparasiteincidence(API)wascalculatedasthe numberofmalaria-positivepatientsper1,000inhabitants foreachofthestudysites:API=(numberofmicroscopicallyprovenmalariacases/1,000population/year).Densityof Anopheles mosquitoesThenumberof Anopheles mosquitoeswasmonitored usingablacklighttrapsinGyodong-myeon(Figure1A,I) andSamsan-myeon(Figure1A,II),GanghwaCountyof IncheonMetropolitanCityandCheorwon-eup(Figure1B, III)andGimhwa-eup(Figure1B,IV),CheorwonCounty ofGangwonProvinceintheROKduringthemalaria transmissionseasonfrom2010 – 2012.Mosquitocollectionswereconductedtwiceaweekbetween8PMand 7AMfromApril-October,atthesamecollectionsites forcomparativeanalysis.Femalemosquitoeswereidentifiedusingmorphologicaldifferencesandcountedregardlessoftheblood-fedstatusormalariaparasiteinfectivity. Theaverageofthenumberofcollectedmosquitoesover twodayswasconsideredarepresentativevalueforthe week[14].ResultsOverviewofmalariainthepasttwodecadesAtotalof31,254casesofvivaxmalariawerereported from1993 – 2012(Figure2).Intotal,9,501cases(30.4%) werereportedinROKmilitarysoldiers,7,658cases (24.5%)inveteranswhoservedinmalariariskareas,and 14,095cases(45.1%)inciviliansduringthe20yearsafterKim etal.MalariaJournal 2013, 12 :309 Page2of9 http://www.malariajournal.com/content/12/1/309

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A B Figure1 Locationswherecollectedmosquitoesbyblacklighttraps.A ,GanghwaCounty; B ,CheorwonCounty.Mosquitocollectionarea: I ,Gyodong-myeon; II ,Samsan-myeon; III ,Cheorwon-eup;IV,Gimhwa-eup. 1 21 107 358 1723 3930 3622 4141 2538 1761 1164 864 1311 2019 2203 1009 1317 1772 838 5550 500 1000 1500 2000 2500 3000 3500 4000 45001 9 9 3 1 9 9 4 1 9 9 5 1 9 9 6 1 9 9 7 1 9 9 8 1 9 9 9 2 0 0 0 2 0 0 1 2 0 0 2 2 0 0 3 2 0 0 4 2 0 0 5 2 0 0 6 2 0 0 7 2 0 0 8 2 0 0 9 2 0 1 0 2 0 1 1 2 0 1 2YearNo. of Patients Figure2 Theannualnumberofvivaxmalariacasesfrom1993 – 2012. Kim etal.MalariaJournal 2013, 12 :309 Page3of9 http://www.malariajournal.com/content/12/1/309

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there-emergenceofmalariaintheROK.Therewere threepeaksintheincidenceofvivaxmalariaduringlast twodecades,with4,141cases,2,203cases,and1,772 casesin2000,2007,and2010,respectively.Patientswithmalariafrom2010 – 2012Atotalof3,165vivaxmalariacaseswerereportedfrom 2010 – 2012,including798(25.2%)insoldiers,519 (16.4%)inveterans(lessthan2yearsafteractiveduty service),and1,848(58.4%)incivilians(Table1).The proportionofannualnumberofciviliancasesincreased from48.6%in2011to71.0%in2012,whiletheproportion ofROKsoldiersandveteransdecreasedfrom264(31.5%) in2011to104(18.7%)in2012andfrom167(19.9%)in 2011to57(10.3%)in2012,respectively.Overall,the annualproportionofmalariacasesfor16administrative districtsdecreased52.7%in2011comparedto2010and by33.8%comparedto2011.However,thenumberof casesreportedfromtheIncheonMetropolitanCityand GyeongnamProvince(Figure3)increased15.3%and 23.1%,respectively,in2012(Table2).Inaddition,the USmilitaryreportedatotalofninemalariacasesduring 2010 – 2012.Sixcaseswerereportedwhiledeployedto Korea(4casesin2010,1casein2011,and1casein 2012),whilethreecaseswerereportedafterreturning totheUSA(duetothelong-incubationperiodofvivax malaria,onecasein2010,0casein2011,andtwocases in2012).ComparisonoftheAPIaccordingtoadministrativeareasOverall,APIdecreasedfrom0.036in2010to0.017in 2011and0.011in2012(Table3).In2010,Gangwon ProvincehadthehighestAPIat0.123,followedbyIncheon MetropolitanCity(0.093),G yeonggiProvince(0.069), andSeoulMetropolitanCity(0.029).In2011,Gangwon ProvincehadthehighestAPIat0.063,followedby Table1Annualnumber(percentoftotal)of Plasmodium vivax casesamongROKmilitarypersonnel,veterans,and civilians201020112012Total Veteran295(16.6%)167(19.9%)57(10.3%)519(16.4%) Soldier430(24.3%)264(31.5%)104(18.7%)798(25.2%) Civilian1047(59.1%)407(48.6%)394(71.0%)1848(58.4%) Total1772(56.0%)838(26.5%)555(17.5%)3165 Incheon (523) Seoul(451) Gyeonggi(1470) Gangwon(291) Chungnam (33) Chungbuk(42) Daejeon(28) Gyeongbuk (39) Daegu(39) Ulsan(18) Busan(74) Gyeongnam (53) Jeonbuk (39) Jeonnam (36) Gwangju(16) Jeju island (13) Metropolitan Areas* * * * Figure3 ReportedvivaxmalariacasesintheRepublicofKorea(ROK)byProvinceandMetropolitanArea. DMZ,DemilitarizedZone. Kim etal.MalariaJournal 2013, 12 :309 Page4of9 http://www.malariajournal.com/content/12/1/309

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IncheonMetropolitanCity(0.045),GyeonggiProvince (0.033),andSeoulMetropolitanCity(0.009).In2012, IncheonMetropolitanCityhadthehighestAPIat 0.052,followedbyGyeonggiProvince(0.022),Gangwon Province(0.009),andSeoulMetropolitanCity(0.007). MostcasesofmalariawerereportedfromJune throughSeptemberin2010 – 2012withthehighestpeaks observedfromthe29thweekof2010(July10 – 17)with 113patients,inthe28thweekof2011(July2 – 9)with 63patients,andinthe31stweekof2012(July28to August4)with42patients(Figure4).Interestingly,the lastapparentpeaksofannualincidenceduringthesethree yearswereapproximatelythreeweeksafterChuseok (KoreanThanksgivingDay,whichwasonSeptember22in 2010,September12in2011,andSeptember30in2012), thatis,the42ndweekof2010(October10 – 16)with32 patients,the40thweekof2011(October2 – 8)with32 patients,andthe43rdweekof2012(October21 – 27)with 13patients(Figure4).SexratioandoccupationofvivaxmalariapatientTherewere2,666maleand499femalepatientswith vivaxmalariafrom2010 – 2012.Theratiooffemaleto malepatientsincreasedfrom1:7.9in2011to1:4.1in2012 (Figure5).Themostcommonoccupationwassoldier (18.74 – 31.50%),followedbystudents(9.73 – 13.25%),and farmersandfishermen(4.23 – 6.85%)(Figure6).Densityof Anopheles mosquitoesAtotalof67,566 An.sinensis sensulatowerecollectedin 2010,5,022in2011,and38,207in2010inGanghwaCounty fromApril-October(Figure7A).InCheorwonCounty, 1,308 An.sinensis s.l.werecollectedin2010,228in2011, and2,427in2010(Figure7B). An.sinensis s.l.wasfirst detectedduringthe17thweekinCheorwonCountyinall threeyears;however,inGanghwaCounty, An.sinensis s.l. wasfirstdetectedduringthe17thweekof2010,18thweek of2011,and15thweekof2012(Figure7). Thehighestdensityof An.sinensis s.l.wasrecorded duringthe33rdweek(236)of2010,the34thweek(42) of2011,andthe33rdweek(696)of2012inCheorwon County.InGanghwaCounty,thehighestdensityof An. sinensis s.l.wasreportedduringthe34thweek(14,848) of2010,the36thweek(1,027)of2011,andthe33rdweek (9,909)of2012.Thenumberof An.sinensis s.l.waslowest attheendofthesurveillanceperiod(Figure7). Table2Annualnumberandpercentdifferenceof Plasmodiumvivax casesbyMetropolitanCityand Province,2010-2012No. cases 2010 No. cases 2011 Percent difference 2011 No. cases 2012 Percent difference 2012 Metropolitan areas Seoul29094-67.667-28.7 Busan4324-44.27-70.8 Daegu1916-15.84-75.0 Incheon256124-51.6143+15.3 Gwangju96-33.31-83.3 Daejeon159-40.04-55.6 Ulsan87-12.53-57.1 Provinces Gyeonggi818389-52.4263-32.4 Gangwon18494-48.913-86.2 Chungbuk2311-52.28-27.3 Chungnam1412-14.37-41.7 Jeonbuk2212-45.55-58.3 Jeonnam2111-47.64-63.6 Gyeongbuk1912-36.88-33.3 Gyeongnam2413-45.816+23.1 Jeju74-42.92-50.0 Total1772838-52.7555-33.8 Table3Thenumberof Plasmodiumvivax malaria patientsandannualparasiteincidencefrom2010-21012 byMetropolitanCityandProvince201020112012 No.of population No.of patient (API) No.of patient (API) No.of patient (API) Metropolitan areas Seoul10,026,000290(0.029)94(0.009)67(0.007) Busan3,464,00043(0.012)24(0.007)7(0.002) Daegu2,477,00019(0.008)16(0.006)4(0.002) Incheon2,750,000256(0.093)124(0.045)143(0.052) Gwangju1,506,0009(0.006)6(0.004)1(0.001) Daejeon1,527,00015(0.010)9(0.006)4(0.003) Ulsan1,105,0008(0.007)7(0.006)3(0.003) Provinces Gyeonggi11,788,000818(0.069)389(0.033)263(0.022) Gangwon1,496,000184(0.123)94(0.063)13(0.009) Chungbuk1,539,00023(0.015)11(0.007)8(0.005) Chungnam2,104,00014(0.007)12(0.006)7(0.003) Jeonbuk1,802,00022(0.012)12(0.007)5(0.003) Jeonnam1,772,00021(0.012)11(0.006)4(0.002) Gyeongbuk2,638,00019(0.007)12(0.005)8(0.003) Gyeongnam3,232,00024(0.007)13(0.004)16(0.005) Jeju552,0007(0.013)4(0.007)2(0.004) Total49,778,0001,772(0.036)838(0.017)555(0.011) Kim etal.MalariaJournal 2013, 12 :309 Page5of9 http://www.malariajournal.com/content/12/1/309

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Atotalof110,795 An.sinensis s.l.werecollectedin GanghwaCountybutonly3,963werecollectedin CheorwonCounty(Figure7).Thehighvectordensity inGanghwaCountymayhaveresultedinthehighand increasedincidenceofvivaxmalariainthatarea.DiscussionInNorthKorea,thehigh-riskareasofvivaxmalariaare GaeseongCity,theSouthandNorthHwanghaeProvinces, andGangwonProvince,whichbordertheDMZ.The DMZisa4-km-wide,250-km-longcorridorthatextends acrossthemiddlepartoftheKoreanpeninsula.Ingeneral, nocivilianshavebeenallowedtoentertheDMZformore than60years,eventhoughoneexceptionalvillagecalled “ Daesungdong ” islocatedinsideofDMZ;therefore,naturalecosystemsandbiodiversityarehighlyconservedin theDMZ[18].Tocontrolmalaria,NorthKoreahas providedpresumptiveanti-relapsechemoprophylaxiswith primaquine(15mgfor14days)beforethemalariatransmissionseasonforcivilianslivingintheseareassince2002 [19].Asaresult,itwasbelievedthattransmissionofmalariaoccurredmainlyintheseareasinNorthKorea[20]. Therefore,theadjacenttomalariariskareasinNorth Korea,highriskareaswereobservedintheROK,e.g., IncheonMetropolitanCityandnorthernGyeonggiand Gangwonprovinces.Thereisnoobjectiveopinionthat masschemoprophylaxismightlargelydecreasethenumberofmalariacasesamongmilitarypersonnel,whichmay alternativelydecreasenumbersofcasesamongcivilian populations.Chemoprophylaxisstartedwithapproximately16,000militarypersonnelin1997andexpanded tomorethan200,000militarypersonnelwhoarecurrentlyservinginmalariahighriskareas[13].Unfortunately,itwasfoundthatprophylacticfailureoccurred eveninthosewhohadsufficientplasmaconcentrations ofhydroxychloroquine.Itmeansthatachloroquineresistant P.vivax strainhasbeenreportedintheROK [21].Theappearanceofthisdrug-resistantstrainis troublesomeforthetreatmentofpatientsinthefuture. Therefore,anotherstandardregimenshouldbeconsidered toreplacethecurrentregimenofchloroquine-primaquine. However,itisnoteasytofindthenextdefensivelineof anti-malariadrugsbecauseithasbeenreportedthat Korean P.vivax isolatesarealreadyresistanttopyrimethamine,whichisrecommendedforuseinpatientswithmalariawhofailtorespondtochloroquinechemotheraphy [22].Itwasshownthattheexistenceofantifolate-resistant P.vivax intheROK.Furtherdetailedgeographicmapping ofcurrentandchangingpatternsofvivaxmalariadrugresistanceonanationalorregio nalscalewouldproveavaluableaidfordevelopingandupdatingnationalanti-malarial policyguidelinesintheR OK.Controlmeasuresand inter-governmentalco-operationarealsoneededto blockthespreadofdrug-resistantmalariaintheROK. 0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42 44 46 48 50 52 0 10 20 30 40 50 60 70 80 90 100 110 120 2010 2011 2012 WeekNo. of Patient113 63 42 Figure4 TheweeklyincidenceofvivaxmalariainROKpatientsfrom2010 – 2012. 2 0 10 20 1 1 2012 0 500 1000 1500 2000Male Female YearNo. of Patient 296 94 109 1476 744 446 Figure5 Thesexratioofpatientswithvivaxmalaria from2010 – 2012. Kim etal.MalariaJournal 2013, 12 :309 Page6of9 http://www.malariajournal.com/content/12/1/309

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ItwasreportedthatsixAnophelesspeciesinthe ROK: Anophelessinensis sensustricto ,Anopheleslesteri, Anophelespullus,Anophelessineroides,Anopheleskleini and Anophelesbelenrae [23-26].Thesesixspeciescompriseaspeciescomplexcalled An.sinensis s.l.Becausethey occurinsympatryanditishardtodistinguishbymorphology.Thus,molecularmethodsareneededtoidentifythe species.Butitishardtoapplythenewlydeveloped methodsforclassificationsinthesurveillancesystemuntil developingmoreprecisemethodsforidentificationof Anopheles complexinrealtimemanners.Therefore, An. sinensis s.l.waspresentedinthisstudy.Analysisofthe mosquitodensityof An.sinensis s.l.instudyareas overthreeyearsshowedanextremelyhigherdensity 0 5 10 15 20 25 30 35 40 45Professionals E n g i n e e r s C l e r k s S e r v i c e w o r k e r s M a r k e t e r s F a r m e r s &F i s h e r m e n T e c h n i c i a n s M a k e r s L a b o r e r s S o l d i e r s H o u s e k e e p e r s St u d e n t s U n e m p l o y e e d O t h e r s 2010 2011 2012 Figure6 Occupationsofvivaxmalariapatientsfrom2010 – 2012. 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42 44 0 5000 10000 15000 20000 2010 2011 2012 A BNo. of Anopheles sinensis s.l. 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42 44 0 200 400 600 800 2010 2011 2012 Week WeekNo. of Anopheles sinensis s.l. Figure7 Theweeklynumberof Anophelessinensis s.l.inGanghwaCounty,IncheonMetropolitanCity(A)andCheorwonCounty, GangwonProvince(B)from2010 – 2012. Kim etal.MalariaJournal 2013, 12 :309 Page7of9 http://www.malariajournal.com/content/12/1/309

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inGanghwaCountycomparedtoCheorwonCounty (Figure7).Therefore,thepotentialunknownthreatening factorsincludingmosquitodensitystillmayexistonthe westsideofmalariafocicomparedwiththeeastside;this explainswhytheAPIofGangwonProvince,whichisthe representativelocationoftheeastside,wasreduced dramaticallyfrom0.123in2010to0.063in2011andto 0.009in2012andtheAPIofIncheonMetropolitanCity changedfrom0.093in2010to0.045in2011butincreased to0.052in2012(Table3). PHCsareresponsibleforcontrollingthetransmissionof malariaineachofthevivaxmalariariskarea.Asaresult oftheanti-malariaeffortsofthePHCinCheorwon County,whichisahigh-riskareainGangwonProvince, thenumberofcasesofmalariadecreaseddramaticallyto lowlevel,27casesin2010,14casesin2011,andtwocases in2012.InCheorwonCounty,ninecaseswerefirst reportedin1997,whiletherewasapeakof166casesin 2000[27].Ittookanaverageof5.4averagedays(4.2 – 7.0) toconfirmacaseofmalariaafteronsetduring2010 – 2012 (unpublisheddata).Anti-mosquitoactivities,including foggingandresidualspray,tookplacefromApril8to October5in2010,May4toOctober4in2011,andMay 4toOctober9in2012.Intotal,748Lofinsecticideand 129Loflarvicidewereusedin2010,1,037Lofinsecticide and188Loflarvicidewereusedin2011,and807Lof insecticideand21Loflarvicidewereusedin2012to coveranareaof36,592m2.Toobtainthislevelofcoverage,activitieswererepeatedapproximately1,442timesin 2010,1,510timesin2011,and1,430timesin2012(data fromthePHCinCheorwonCounty,GangwonProvince). Theinterestingfindingisthatthelastpeakofeach yearwasshownthesimilarpatternsinthreeyears,that is,increasingthemalariacasesinthreeweeksafter Chuseok(Figure4, ).Thisdurationismatchedwith theincubationperiodofvivaxmalariaintheliver.It wasprobablyduetothemassiveinterregionalpopulationmovementthroughouttheROKduringChuseok fromhighriskareastomalariafreeareas,inaddition increasingtheactivitiesduringthenightwithoutself protectionfrommalariavectors.Itissuggestedthatsoldierswholeaveforvacationtotheirhometownsshouldbe eithercheckedortreatedformalariajustlikeretiringexsoldiersfromtheiractivemilitaryservice(primaquine/ 15mg/14days)[15,28,29]. Toevaluatetransmissionofmalariainagivengeographic region,manyfactors,includingtemperature,mosquito density,vectorcapacity,climate,rainfall,andhumidity, shouldbeconsidered[30].Patientincidencealonecannot provideacompleteunderstandingoftheprevalenceofmalariaintheROKbecausetherearemanyfactorsinvolved, includingthechangesinweeklypopulationdensityofmosquitoesduetoenvironmentalf actors,vectorialcapacity, long-andshort-incubationpa tientratios,symptomatic andasymptomaticpatientratios,anddifferencesin weeklyrainfallandtemperatures.Thisstudyanalysed onlytwofactors:incidenceand An.sinensis s.l.However, allfactorsindicatedthattransmissionofmalariawouldapparentlybereducedexceptinIncheonMetropolitan CityandGyeongnamProvince.Thereareopportunities fortheeradicationofmalariaintheROKduetoseveraleffortsoftheKoreaCDC,GovernmentPublic InstituteofHealthandEnvironment,PHCs,andrelatedinstitutes.ConclusionsThenumberofpatientswithvivaxmalariaintheROK peakedin2010forathirdtimeovertwodecadesand thendecreasedinthesubsequenttwoyears.Thiswas thethirdtimethenumberofcasesofmalariapeaked sinceatrendofdecreasingcaseswasobservedin2001. Itisexpectedthatthenumberofcasesofmalariawill continuetodecreaseinthefuture,althoughtheremay besomefluctuations.However,moreintensivemalaria surveillanceisneededinthewesternpartofthecountry wherefocihavere-emergedtoreducethepotentialfor futureincreasesinthenumberofmalariacasesinthe ROK.Competinginterests Theauthorsdeclarethattheyhavenocompetinginterests. Authors ’ contributions TSKandHWLconceivedanddesignedthestudyandcontributedtothe executionoftheresearch.TSKandHWLwrotethemanuscript.PYC,SKA, SKL,YJK,JSK,HSK,SHC,YKPandYSHcollectedthemosquitoes.HCK,WJL, SKY,JG,YS,BKN,andHSKcollectedtheinformationonpatientsand performedanalysisofthemosquitopopulation.Allauthorshavereadand approvedthefinalmanuscript. Acknowledgments Wearegratefultoallblooddonors;thestaffofthePublicHealthCentersin Cheorwon,Gimpo,Ganghwa,andYeoncheonCounty;andtheInstitutesof HealthandEnvironmentinIncheonMetropolitanCity,GangwonProvince, andGyeonggiProvince.Thisworkwassupportedbyaresearchgrantfrom InhaUniversity. Authordetails1DepartmentsofParasitology,InhaUniversitySchoolofMedicine,Incheon 400-712,RepublicofKorea.2DepartmentofParasitologyandInstituteof HealthSciences,GyeongsangNationalUniversitySchoolofMedicine,Jinju 660-751,RepublicofKorea.3DivisionofMalariaandParasiticDiseases, NationalInstituteofHealth,Osong363-951,RepublicofKorea.45thMedical Detachment,168thMultifunctionalMedicalBattalion,65thMedicalBrigade, Unit15247,APOAP96205-5247,USA.5DepartmentofEpidemiology, NationalInstituteofHealth,Osong363-951,RepublicofKorea.6Department ofBiomedicalTechnology,InhaUniversitySchoolofMedicine,Incheon 400-712,RepublicofKorea.7DepartmentofPharmacology,InhaUniversity SchoolofMedicine,Incheon400-712,RepublicofKorea.8Departmentof BiomedicalScience,JungwonUniversity,Goesan,Chungbuk367-805, RepublicofKorea.9DepartmentofAnatomy,CollegeofKoreanMedicine, InstituteofKoreanMedicine,KyungHeeUniversity,Seoul130-701,Republic ofKorea.10DepartmentofPublicHealth,SahmyookUniversity,Seoul 139-742,RepublicofKorea.11DepartmentofPathology,Immunology,and LaboratoryMedicine,CollegeofMedicine,UniversityofFlorida,J-566,1275 CenterDrive,Gainesville,FL32610,USA.Kim etal.MalariaJournal 2013, 12 :309 Page8of9 http://www.malariajournal.com/content/12/1/309

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