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1、ReviewJapanese Encephalitis in China in the Period of 19502018:From Discovery to Control*Japaneseencephalitis(JE)wasfirstdiscoveredinJapanin1871;in1924,amajoroutbreakoccurred,with6,000JEcasesreportedandamortalityrateofapproximately60%1,2.LaterstudiesshowedthatJEis caused by the Japanese encephalitis

2、 virus(JEV),whichisspreadbymosquitoes.JEVcanbecarriedbya variety of mosquitoes(Culex,Anopheles,Aedes,andMansonia),andthereareseveralhosts,namelyaquaticwadingbirdsasreservoirhostsofJEV,pigs(including wild boar and domestic pigs)asamplification hosts,and humans and equids asterminalhosts.Culex tritaen

3、iorhynchus,amosquitospecies that mainly breeds in rice paddies,is themostimportantvectorofJEV1-3.SinceitsdiscoveryinJapan,JEhasgraduallyspreadtoSouthKoreainEastAsia,mainlandChina,thePhilippines,Indonesia,Thailand,andVietnaminSoutheastAsia,andthentoIndiaandSriLankainSouthAsia.JEhasalsospreadtoPapuaNe

4、wGuineainthePacificandtonorthernAustralia4-6.Although it is a vaccine-preventabledisease1,2,JEiscurrentlyprevalentin24countriesand regions in Asia and Oceania,with an annualincidence of approximately 69,000 cases and amortality rate of 30%;70%of survivors haveneurologicalsequelaeofvaryingseverity.Th

5、erefore,JEisavector-borneviralinfectiousdiseasewithahugeburden5-7.ThespreadofJEfromJapantoChinabeganinthe 1930s.In 1934,two cases of acute viralencephalitisinchildreninBeijingwereconfirmedtobeJEVinfectionbyneutralizationexperiments8,9,andthesecouldthereforebeconsideredthefirstlaboratory-confirmed JE

6、 cases in China.JE wassubsequentlyreportedinthesoutheasterncityofAmoy and the eastern city of Shanghai9,10,andthen in Shenyang and Tianjin in northern andeasternChina,respectively.In1939,theepidemiological data,clinical manifestations,andoutcomesofsixcasesofacuteviralencephalitisinBeijingwererecorde

7、d11,andneutralizingantibodies against JEV in the serum of thesepatientsweredetectedbyneutralizationtests,allofwhichwereconfirmedtobeJEVinfections12.Anepidemiological investigation of JE conducted inBeijingduringthe3-yearperiodfrom1948to1950identified a total of 729 cases and 330 deaths(fatalityrate,

8、45.3%):137casesand71deathsin1948,225casesand110deathsin1949,and367cases and 149 deaths in 195013.JE became aseriouspublichealthprobleminChinainthelate1940sandwasassociatedwithahugepublichealthburden.Astherewasnonationalinfectiousdiseasereporting system in China at that time,theepidemiological charac

9、teristics of JE were onlydetailed in scientific research papers,and theoverall prevalence of JE in China could not bedetermined.ThePeoplesRepublicofChinawasfoundedindoi:10.3967/bes2021.024*This work was supported by grants from the National Key Research and Development Program 2016YFD0500401(WH);the

10、 Development Grant of State Key Laboratory of Infectious Disease Prevention and Control2014SKLID103(LG)and 2015SKLID505(WH).The funders had no role in study design,data collection and analysis,decisiontopublish,orpreparationofthemanuscript.1.Department of Arbovirus,NHC Key Laboratory of Biosafety,Na

11、tional Institute for Viral Disease Control andPrevention,ChineseCenterforDiseaseControlandPrevention,Beijing102206,China;2.StateKeyLaboratoryforInfectiousDisease Prevention and Control,Chinese Center for Disease Control and Prevention,Beijing 102206,China;3.Department of Epidemiology,School of Medic

12、ine,Jinan University,Guangzhou 510632,Guangdong,China;4.DepartmentofEnvironmentalandGlobalHealth,CollegeofPublicHealthandHealthProfessions,UniversityofFlorida,Gainesville,USA;5.DepartmentofScienceandTechnology,BeijingTiantanHospital,CapitalMedicalUniversity,Beijing100070,China;6.Department of Microb

13、iology,University of Pennsylvania,Philadelphia,PA 19104,USA;7.NationalImmunizationProgram,ChineseCenterforDiseaseControlandPrevention,Beijing102206,ChinaBiomedEnvironSci,2021;34(3):175-1831751949.OnNovember25,1950,theInterimMeasuresfor the Prevention and Treatment of InfectiousDiseasesclassified13in

14、fectiousdiseases,includingJE.Therefore,since1950,JEhasbeenanationallynotifiable disease,and the national annual JEincidenceandmortalityrateshavebeenrecorded14.WecollectedJEannualincidenceandmortalitydatafor China from 1950 to 2018,including itsspatiotemporal distribution,to characterize theprocess b

15、eginning when JE first entered China,followed by the nationwide JE pandemic,anddecadesofeffortstoeffectivelycontrolJEinChinabyvaccination.ThisstudysummarizesJEpreventionandcontroleffortsinChinaandservesasavaluablereference for the prevention and control of JE inotherareasaroundtheworld.Overall Trend

16、s of JE in China During 19502018In China(excluding regions of Taiwan,HongKong,andMacao),atotalof2,364,177JEcasesand275,792 deaths were reported between 1950 and2018,with an average annual incidence of 34,263andanaverageannualmortalityof3,997(Table1).ThehistoryofJEinChinacanbedividedintofourperiods(T

17、able1andFigure1).Theperiodfrom1950 to 1962 was the invasion period,with thecases therein accounting for 8.1%of the total(191,413/2,364,177),with an average annualincidence of 2.59/100,000.The cases in thepandemicperiod(19631975)accountfor60.0%ofthetotal(1,407,865/2,364,177)andthisperiodhasthe highes

18、t annual incidence of 13.65/100,000.Duringthe30-yearperiodfrom1976to2007,theincidenceandmortalityratesdecreasedannually;thisperiodaccountsfor31.5%(744,238/2,364,177)of all cases,with an average annual incidence of2.23/100,000.Duringthe10-yearperiodfrom2008to2018,duringwhichtheJEvaccinewasincludedin

19、Chinas Expanded Program on Immunization(EPI),the average annual incidence fell to0.14/100,000.EpidemiologicalinformationonJEinChinafrom1950to2018isshowninTable1andFigures1and2.JEisanaturalfocaldisease,anditsprevalenceisrelatedtothelocalnaturalenvironment.ChinaislocatedintheeasternregionofAsia,withal

20、andareaof9.6millionkm2,includinghighmountainsand plains,and can be roughly divided intosoutheastern and northwestern regions based ongeoclimaticconditionsandresidentialpopulations(Figure3A).ThesoutheasternregionincludestheYunnan-GuizhouPlateau(Yunnan,Guizhou,Sichuan,Guangxi,andChongqing),theNorthChi

21、naPlain(Hebei,Beijing,Tianjin,Shanxi,Shandong,andHenan),the Yangtze River Plain(Hunan,Hubei,Anhui,Jiangsu,Zhejiang,Jiangxi,Shanghai,andFujian),andthePearlRiverDeltaPlain(Guangdongand Hainan),while the northwestern regionincludes the Loess Plateau(Shaanxi,Gansu,andNingxia),the Northeast China Plain(H

22、eilongjiang,Jilin,and Liaoning),the Inner Mongolian Plateau(InnerMongolianAutonomousRegion),theQinghai-Tibet Plateau(Qinghai and Tibet),andXinjiangProvince15-17.Table1showstheendemicityofJEbyregionandperiodinChina.Between1950and2018,southeasternChinaaccountedfor92.7%(2,192,685/2,364,177)of all JE ca

23、ses,while thenorthwestern region accounted for only 7.3%(171,492/2,364,177).DuringtheJEpandemicperiod(19631975),cases in the southeastern regionaccounted for 93.2%(1,312,412/1,407,865)of allcasesinthisperiod.CasesofJEintheYangtzeRiverPlainaccountedfor44.6%(627,706/1,407,865)ofallcasesinthisperiod,an

24、d47.8%(627,706/1,312,412)of those in the southeastern region.The YangtzeRiver Plain has historically been a highly endemicareaforJEinChina.ThecasesofJEintheYunnan-GuizhouPlateauareaofthesoutheasternregionofChina accounted for 12.3%(173,635/1,407,865)ofall cases nationwide during the pandemic period(

25、19631975),and 43.8%(9,058/20,661)of thoseduring the period of routine JE vaccination(20082018).The Yunnan-Guizhou Plateau has thehighestJErateinChina.TheproportionofJEcasesinthe Loess Plateau(northwestern China)increasedfrom 2.4%in 19501962 to 12.2%in 20082018(Table1).Invasion of China by JE(1950196

26、2)JE has been a nationally notifiable disease inChina since 1950.JE was mainly reported in 10provinces,typically in eastern China,with Beijing(25.39/100,000),Tianjin(21.16/100,000),Liaoning(3.80/100,000),Jiangsu(1.35/100,000),andShandong(0.86/100,000)accounting for 90.2%(2,725/3,021)ofallcasesin1951

27、(Figure3A).Sincethen,thenumberofprovincesreportingJEcaseshasincreased each year,with the disease graduallyspreadingtocentralandeast-centralChinaandwasseenin25provincesnationwidein1956(Figure3B).By 1958,JE had been reported in all provinces ofChinaexceptXinjiang,Tibet,andQinghai,andwerethusclassified

28、asJE-freeareas(Figure3C).Withtheexpansion of endemic JE areas,the number of JEcasesinthisperiodalsoincreased(Table1).176BiomedEnvironSci,2021;34(3):175-183Table 1.EndemicityofJapaneseencephalitisinChinabyregionandperiodPeriodSoutheast ChinaNorthwest ChinaTotalNationwideYunnan-GuizhouPlateauNorthChin

29、aPlainYangtzeRiverPlainPearlRiverDeltaPlainSubtotalLoessPlateauNortheastChinaPlainInnerMongolianPlateauOthers*SubtotalAverageannualincidence(per100,000population)Averageannualmortality(per100,000population)Averageannualfatality(%)Invasion(19501962)12,653/2,572(6.6)#70,202/18,117(36.7)75,603/13,794(3

30、9.5)9,659/2,731(5.0)168,117/37,214(87.8)4,615/1,242(2.4)18,627/5,525(9.7)50/6(0.03)4/0(0.002)23,296/6,773(12.2)191,413/43,9872.590.622.98Pandemic(19631975)173,635/25,890(12.3)391,367/46,701(27.8)627,706/66,450(44.6)119,704/16,673(8.5)1,312,412/155,714(93.2)31,066/4,416(2.2)64,205/9,541(4.6)177/43(0.

31、01)5/0(0.003)95,453/14,000(6.8)1,407,865/169,71413.651.6512.06Decline(19762007)195,265/17,057(26.2)154,883/11,762(20.8)322,781/23,904(43.4)21,185/2,626(2.8)694,114/55,349(93.2)35,371/3,049(4.8)13,092/2,495(1.8)1,616/296(0.2)45/1(0.006)50,124/5,841(6.8)744,238/61,1902.230.178.22Subtotal381,553/45,519

32、(16.3)616,452/76,580(26.3)1,026,090/104,148(43.8)150,548/22,030(6.4)2,174,643/248,277(92.8)71,052/8,707(3.0)95,924/17,561(4.1)1,843/345(0.08)54/1(0.002)168,873/26,614(7.2)2,343,516/274,8914.910.6111.46Control(20082018)9,058/360(43.8)4,744/208(23.0)3,636/1,30(17.5)604/21(2.9)18,042/719(87.3)2,515/165

33、(12.2)77/14(0.4)15/2(0.07)12/1(0.06)2,619/182(12.7)20,661/9010.140.014.36Total390,611/45,879(16.5)621,196/76,788(26.3)1,029,726/104,278(43.6)151,152/22,051(6.4)2,192,685/248,996(92.7)73,567/8,872(3.1)96,001/17,575(4.1)18,583/347(0.08)66/2(0.003)171,492/26,796(7.3)2,364,177/275,7924.140.5110.31Note.#

34、Numberofcases/deaths(percentageoftotalcasesinthisperiod).*TibetanPlateau(QinghaiandTibetprovinces),andXinjiangProvince.NotincludingJapaneseencephalitisdatafor1950.Totalnumberofcases/totalnumberofdeaths.JapaneseencephalitisinChina:fromdiscoverytocontrol177Pandemic of JE in China(19631975)Twoepidemics

35、ofJEoccurredinChinaduringtheperiodof19631975:onein1966andtheotherin1971(Figures 1 and 4).During 1963 and 1964(beforethetwopeakyears),theaverageannualJEincidencerateinChina(exceptXinjiang,Tibet,andQinghai)varied between 0.01 and 20.00/100,000,1,800,0001,600,0001,400,0001,200,0001,000,000800,000600,00

36、0400,000200,0000No.of cases2520151050Incidence(per/100,000)No.of deathsNo.of cases19501952195419561958196019621964196619681970197219741976197819801982198419861988199019921994199619982000200220042006200820102012201420162018Inactjvated JE vaccineLive atuenuated JE vaccineIncluded in EPIFigure 1.Overal

37、l trends of Japanese encephalitis in China for the period of 19502018.The barsrepresenttheannualincidenceofJapaneseencephalitis(JE),whiletheorangeandblueblocksindicatethenumberofJEcasesandthenumberofJEdeathsinfourdistinctperiods.ThearrowsdenotetheintroductionoftheP3inactivatedJEvaccinein1968(stage2)

38、andtheliveattenuatedJEvaccinein1988(stage3),andtheinclusionoftheJEvaccineinChinasExpandedProgramonImmunization(EPI)in2008(stage4).ThefigurecoverstheinvasionofJEintoChinain19501962,thepandemicin19631975,thedeclinein19762007,andeffectivecontrolin20082018.ANBNCNDN0.000.015.005.0110.0010.0120.0020.0130.

39、0030.0160.00Average annualIncidence(1/100,000)0.000.015.005.0110.0010.0120.0020.0130.0030.0160.00Average annualIncidence(1/100,000)0.000.015.005.0110.0010.0120.0020.0130.0030.0160.00Average annualIncidence(1/100,000)0.0000.0010.1000.1010.2000.2010.3000.3010.4000.4010.500Average annualIncidence(1/100

40、,000)19501962196319751976200720082018Figure 2.Japaneseencephalitis(JE)inChinafortheperiodof19502018.(A)(D)showthegeographicchanges in JE endemic areas in China in the four periods,19501962,19631975,19762007,and20082018,respectively.ThecolorsindicatetheaverageannualJEincidenceratesbyprovince.ABC0.000

41、.015.005.0110.0010.0120.0020.0130.0030.0160.00Incidence(1/100,000)0.000.015.005.0110.0010.0120.0020.0130.0030.0160.00Incidence(1/100,000)0.000.015.005.0110.0010.0120.0020.0130.0030.0160.00Incidence(1/100,000)NNN195119561958Figure 3.Invasion of China by Japanese encephalitis(JE)(19501962).(A)(C)show

42、the geographicchangesintheJEendemicareasinChinain1951,1956,and1958,respectively.ThelineinFigure3ArepresentstheapproximateboundarybetweensoutheastandnorthwestChina.178BiomedEnvironSci,2021;34(3):175-183and the provinces with incidence rates between10.00and20.00/100,000weremainlyinsoutheastern China(F

43、igure 4A).The first JEpandemic in China occurred in 19661967,whichhad a significantly higher incidence than that in19631964.Theincidenceratesincreasedduringthisperiod:six provinces showed incidence rates of10.0120.00/100,000(Figure4B,orangearea),whileseven showed incidence rates of 20.0130.00/100,00

44、0(Figure4B,redarea)andfivehadincidencerates exceeding 30.00/100,000(Figure 4B,bluearea).Another JE pandemic occurred in China in19701971;onlysixprovinceshadincidenceratesof0.015.00/100,000(Figure4C,greenarea),withtheremainingprovinceshavingsignificantlyhigherrates.Only Fujian,Jiangsu,and Henan Provi

45、nces hadaverageannualincidenceratesexceeding30.00/100,000(Figure 4C,blue area),but theaverage annual incidence rate increased greatly ineast-centralChineseprovinces,includingShandong,Hubei,Hunan,Anhui,Jiangxi,Zhejiang,Guangxi,andGuangdong,to20.0030.00/100,000(Figure4C,redarea).AfterthetwopeaksinJEin

46、cidence,thenumberofcasesdecreasedannually,andthenationalannualincidence became 9.74/100,000 by 1975.TheincidenceofJErangedbetween0.0120.00/100,000in most provinces from 1974 to 1975;only JilinProvinceinnortheastChinahadanincidenceofover20.00/100,000(Figure4D).Decline of JE in China(19762007)From1976

47、to1977,theaverageannualincidencerates of JE were 20.0030.00/100,000 in AnhuiProvinceand10.0020.00/100,000inHenan,Jiangsu,and Jiangxi Provinces;the remainingprovinceshadincidenceratesbelow10.00/100,000(Figure5A).Inthe5-yearperiodfrom1980to1985,the average annual incidence rate of JE was0.015.00/100,0

48、00 in all provinces except Jiangsu,Anhui,Jiangxi,and Guizhou(Figure 5B,yellowregion).TheaverageannualincidencerateofJEinHenanProvince(Figure5C,yellowregion)remainedat5.0010.00/100,000between1990and1995,andtheincidenceratesintheotherprovinceswereallbetween0.01and5.00/100,000.From2000to2005,the annual

49、 average incidence rates of JE for allprovinces in China were less than 5.00/100,000(Figure5D).Effective Control of JE in China(20082018)The incidence of JE has sharply decreased inChinasince2008,whentheJEvaccinewasincludedinChinasEPI(Figure2D).Atotalof20,661JEcasesand901deathswerereportedduringthep

50、eriodof20082018,i.e.,anaverageof1,878casesand82deathsperyear.TheaverageannualincidenceratesofJEinthecentralandeasternprovincesofChina,ABCDNNNN0.000.015.005.0110.0010.0120.0020.0130.0030.0160.0019631964196619671970197119741975Average annualincidence(1/100,000)0.000.015.005.0110.0010.0120.0020.0130.00