Abdul R, Abdullah

Anand, Mohan

Andrew, Kiyu

Boon F, Lai

Jamail, Muhi

Mary Jane, Cardosa

Mohamad, T. Arif

Mong H, Ooi

Peng C, Pek

Phaik H, Tio

See C, Wong

See Y, Wong

Shekhar, Krishnan

Unimas Institutional Repository

Short communicationA decade of Japanese encephalitis surveillance in Sarawak,Malaysia: 1997–2006See C. Wong1, Mong H. Ooi1, Abdul R. Abdullah1, See Y. Wong1, Shekhar Krishnan1, Phaik H. Tio2, Peng C. Pek1,Boon F. Lai1, Anand Mohan1, Jamail Muhi3, Andrew Kiyu3, Mohamad T. Arif2 and Mary J. Cardosa21 Sibu Hospital, Sibu, Sarawak, Malaysia2 Universiti Malaysia Sarawak, Kota Samarahan, Sarawak, Malaysia3 Sarawak Health Department, Ministry of Health, MalaysiaSummary Japanese encephalitis virus (JEV) is an important encephalitis virus in Asia, but there are few data onMalaysia. A hospital-based surveillance system for Japanese encephalitis (JE) has been in operation inSarawak, Malaysia, for the last 10 years. JEV is endemic in Sarawak, with cases occurring throughout theyear and a seasonal peak in the last quarter (one-way anova, P < 0.0001). Ninety-two per cent of 133 caseswere children aged 12 years or younger; the introduction of JE vaccination in July 2001 reduced thenumber of JE cases (84 in the four seasons prior to vs. 49 in the six seasons after, McNemar’s test,P = 0.0001). After implementation of the programme, the mean age of infected children increased from 6.3to 8.0 years (Student’s t-test, P = 0.0037), suggesting the need for a catch-up programme.keywords Japanese encephalitis, surveillance, vaccineJapanese encephalitis virus (JEV), family Flaviviridae, is thetype species of the Japanese encephalitis serological groupof flaviviruses that includes West Nile virus. JEV istransmitted by Culex spp. mosquitoes and is maintained ina vertebrate host–mosquito cycle where pigs and waterbirds are the main amplifying hosts and humans merelyincidental hosts. JEV is considered the most importantcause of encephalitis in Asia with 30 000–50 000 casesreported annually. Most infected individuals are asymp-tomatic but of those who do present with encephalitis,25–30% of cases are fatal while half of the survivors havesevere neurological sequelae (Solomon et al. 2000;Mackenzie et al. 2004). The disease burden associatedwith JEV is not well appreciated and it has only been in thepast few years that the importance of JE has been broughtto general attention with the recognition of large outbreaksof JE in parts of India and Nepal. Even in countries whereit is assumed that JE does not occur, such as Indonesia, arecent hospital-based surveillance study in Bali has shownthat JE incidence and case-fatality rates are similar to thoseof other JE endemic countries (Kari et al. 2006).In Malaysia, there is a paucity of data on JE. Twooutbreaks have been recorded in the literature – PulauLangkawi in 1974 (Fang et al. 1980) and Penang in1988 (Cardosa et al. 1995). A series of studies from the1960s documented JEV isolation from mosquitoes inSarawak and showed that pigs play an important role asamplifying hosts (Bendell 1970; Simpson et al. 1970,1974, 1976; Bowen et al. 1975). Seroconversion to JEVin pigs suggested that transmission occurs throughout theyear with infection rates higher in the period fromNovember to January coinciding with the major seasonalpopulation increase of Culex tritaeniorynchus (Simpsonet al. 1976).In 1997, a pilot hospital-based surveillance study for JEwas set up in Sibu Hospital in Sarawak, followed in 1998by passive surveillance for all other hospitals in the state.Patients were suspected to have Japanese encephalitis ifthey had fever (or a history of fever), and at least one of thefollowing: reduced level of consciousness (lethargy,drowsiness or coma); severe headache; neck stiffness; tenseanterior fontanelle; focal neurological signs and prolongedseizures.Paired sera and paired CSF for each patient wereconsidered to be the ideal specimen set. However, in realitythe complete specimen set was not obtained from manycases. Specimens were tested for JEV specific IgM by MACELISA (Venture Technologies Sdn Bhd, Malaysia), whichdistinguishes IgM elicited by JEV from that elicited bydengue viruses (Solomon et al. 1998; Cardosa et al. 2002).Tropical Medicine and International Health doi:10.1111/j.1365-3156.2007.01967.xvolume 13 no 1 pp 52–55 january 200852 ª 2008 Blackwell Publishing LtdThe sensitivity, specificity, positive predictive value andnegative predictive value of the test used were 83%, 99%,0.98 and 0.92, respectively for CSF and 91%, 95%, 0.92and 0.94, respectively for serum.All cases of encephalitis with specific IgM to JEV inserum and ⁄ or CSF were considered to have been infectedrecently with JEV. It should be noted that patients withsingle IgM-negative sera or CSF cannot be consideredconclusively negative because an IgM seroconversion canoccur in a second specimen. With only single specimens, welose this information. Here we report data obtained over a10-year period from 1997 to 2006. Four seasons into thestudy period, in July 2001 the Sarawak Health Departmentimplemented a JE vaccination programme. JE vaccine(Biken, Japan) was included in the Expanded Programmeof Immunization (EPI), covering children aged 1–2 years.All individuals aged 1–15 years in the household of everyidentified JE case were also vaccinated. There are somecultural factors that are notable in our practice ofvaccination of case contacts. Many rural communities inSarawak live in longhouses. These are single structures thathouse many individual family units with a commonconnecting veranda called ruai. Thus there is very closecontact and frequent movement of people among differentfamilies in our longhouse villages. In our control pro-gramme we have treated each longhouse as a singlehousehold.A total of 133 patients with serologically confirmedrecent JEV infection were admitted into Sibu Hospitalduring the study period. One hundred and twenty-two(92%) were children aged 12 years and younger, 11 (8%)patients were older children and adults. After the intro-duction of JE vaccination in Sarawak, we recorded areduction in JE admissions (Figure 1) in Sibu Hospital: 84(63%, 79 children aged £12 years, five adults) of 133patients between the months of February 1997 and June2001 (Table 1), compared with 49 (37%, 43 children£12 years, six adults) of 133 patients were hospitalizedbetween the months of July 2001 and December 2006(McNemar’s test, P = 0.0001). We also observed anincrease in the age of affected patients. The mean age(range) of all affected patients shifted from 7.0 (0.3–28) to9.2 (1.3–27.4) years (Student’s t-test, P = 0.0066). Furthersubgroup analysis for children £12 years showed that themean age of affected under-twelves increased from 6.3(0.3–12) to 8.0 (1.3–12) years (Student’s t-test,P = 0.0037). This shift in age distribution has alsooccurred in other countries where JE vaccine was intro-duced, namely in Japan, Korea, China and Taiwan (Tsaiet al. 1999).Our data show that JE is seasonal in Sibu with asignificantly higher number of cases in the last quarter ofeach year, and sporadic cases throughout the year. Itconfirms the conclusion of the pig seroconversion study inthe early 1960s suggesting that there is higher rate oftransmission of JEV during the period of November toJanuary (Simpson et al. 1976).Our focus on a single hospital in the state allowed usto be more certain of the true numbers of cases beingseen at this hospital and has given us a clear picture of thetrends in JEV infection in Sarawak. We believe thatdespitehe fact that the numbers of cases notified through-out the state are likely to be an underestimate of the trueincidence of JE in Sarawak, obtaining accurate data from amajor hospital in the state will allow some measure ofconfidence in providing an evidence base from which tomake decisions about public health interventions.We had an opportunity to obtain a better estimate of thenumbers of JE cases in Sarawak during the season of1998 ⁄ 1999 when there was a large outbreak of fatal viralencephalitis in Peninsular Malaysia (Chua et al. 1999;Farrar 1999). This outbreak, of the newly discovered02468101214161820Q1-97Q3-97Q1-98Q3-98Q1-99Q3-99Q1-00Q3-00Q1-01Q3-01Q1-02Q3-02Q1-03Q3-03Q1-04Q3-04Q1-05Q3-05Q1-06Q3-06Number of JEV IgM positive casesIntroduction of JE vaccination Figure 1 Japanese encephalitis (JE) admissions in Sibu Hospitalbetween 1997 and 2006. The bars represent the number of JEadmissions in Sibu Hospital by quarter of the year over the 10-yearstudy period, 1997–2006 (Q1 = January–March, Q2 = April–June, Q3 = July–September, Q4 = October–December).Table 1 Cumulative distribution of JE cases presenting to SibuHospital by quarter of the years 1997–2006Quarter MeanStandarddeviationStandarderror RangeCumulativetotalQ1 3.6 5.8 1.8 0–20 20Q2 4.4 6.6 2.0 1–24 24Q3 4.0 6.3 1.9 0–22 22Q4 12.2 18.9 5.7 1–67 67Tropical Medicine and International Health volume 13 no 1 pp 52–55 january 2008S. C. Wong et al. Japanese encephalitis in Sarawakª 2008 Blackwell Publishing Ltd 53Nipah virus (Lam & Chua 2002), was originally misdiag-nosed as being due to JEV. Doctors in all hospitals inMalaysia were reminded to notify encephalitis cases to thepublic health authorities and we thus had an unusuallyhigh number of cases of encephalitis with specimenssubmitted to the laboratory. Figure 2 shows that duringthis season of 1998 ⁄ 1999, there was a large increase ofcases reported in the state suggesting that JE is probablyunder reported most years.In conclusion, we report that the introduction of theBiken JE vaccine in Sarawak has reduced the incidence ofthe disease. The total population of Sibu is 600 000 with180 000 under 12 years of age. The data we have obtainedover this last decade of surveillance show that the averageannual incidence of JEV was 9.8 per 100 000 populationunder 12 years, dropping to 4.3 per 100 000 populationunder 12 years after the introduction of JE vaccination.The policy of vaccinating 1 to 15-year-old householdcontacts of JE cases immediately probably contributed tothe remarkable reduction in the JE caseload after theintroduction of the vaccine. We introduced this practicebecause of specific cultural factors, especially because ofthe longhouse mode of living common among our ruralcommunities, with animals reared under or near thelonghouse. However, because we did not have a pro-gramme of ‘catch-up’ vaccination for the general paediatricpopulation, we have seen a shift in the age of JE cases toolder children and teenagers.Another point to note is that JEV is a zoonotic virus andhumans are incidental and dead end hosts. Thus anyvaccination programme would have to target all suscepti-ble individuals without expecting herd immunity to con-tribute to a reduction in incidence. For these reasons, theimplementation of JE vaccination into any JE endemic areashould take into consideration the need for a ‘catch-up’immunization programme at the time of introduction ofvaccine into the routine EPI.ReferencesBendell PJ (1970) Japanese encephalitis in Sarawak: studies onmosquito behaviour in a Land Dayak village. Transactions ofthe Royal Society of Tropical Medicine and Hygiene 64,497–502.Bowen ET, Simpson DI, Platt GS et al. (1975) Arbovirus infectionsin Sarawak, October 1968-February 1970: human serologicalstudies in a land Dyak village. Transactions of the Royal Societyof Tropical Medicine and Hygiene 69, 182–186.1Cardosa MJ, Tio PH & Kaur P (1995) Japanese encephalitis virusis an important cause of encephalitis among children in Penang.Southeast Asian Journal of Tropical Medicine and Public Health26, 272–275.Cardosa MJ, Wang SM, Sum MS et al. (2002) Antibodies againstprM protein distinguish between previous infection with dengueand Japanese encephalitis viruses. BMC Microbiology 2, 9.Chua KB, Goh KJ, Wong KT et al. (1999) Fatal encephalitis due toNipah virus among pig-farmers in Malaysia. Lancet 354,1257–1259.Fang R, Hsu DR & Lim TW (1980) Investigation of a suspectedoutbreak of Japanese encephalitis in Pulau Langkawi. MalaysianJournal of Pathology 3, 23–30.Farrar JJ (1999) Nipah-virus encephalitis – investigation of a newinfection. Lancet 354, 1222–1223.Kari K, Liu W, Gautama K et al. (2006) A hospital-basedsurveillance for Japanese encephalitis in Bali, Indonesia.BMC Medicine 4, 8.Lam SK & Chua KB (2002) Nipah virus encephalitis outbreakin Malaysia. Clinical Infectious Diseases 34 (Suppl. 2),S48–S51.Mackenzie JS, Gubler DJ & Petersen LR (2004) Emergingflaviviruses: the spread and resurgence of Japanese encephalitis,West Nile and dengue viruses. Nat Med 10 (Suppl. 12),S98–S109.Simpson DI, Bowen ET, Platt GS et al. (1970) Japanese encepha-litis in Sarawak: virus isolation and serology in a Land Dyakvillage. Transactions of the Royal Society of Tropical Medicineand Hygiene 64, 503–510.Simpson DI, Bowen ET, Way HJ et al. (1974) Arbovirus infectionsin Sarawak, October 1968–February 1970: Japanese encepha-litis virus isolations from mosquitoes. Annals of TropicalMedicine and Parasitology 68, 393–404.Simpson DI, Smith CE, Marshall TF et al. (1976) Arbovirusinfections in Sarawak: the role of the domestic pig. Transactions0Apr-97Jun-97Aug-97Oct-97Dec-97Jun-98Aug-98Oct-98Dec-98Feb-98Apr-98Jun-99Aug-99Oct-99Dec-99Feb-99Apr-99Jun-00Feb-00Apr-00Number of cases5101520253035SarawakSibu aloneFigure 2 Comparison of Japanese encephalitis (JE) cases fromSibu Hospital and the State of Sarawak. The solid line representsnumbers of JE cases from Sibu Hospital and the dotted line rep-resents numbers of cases from the whole state of Sarawak, inclu-sive of Sibu Hospital.Tropical Medicine and International Health volume 13 no 1 pp 52–55 january 2008S. C. Wong et al. Japanese encephalitis in Sarawak54 ª 2008 Blackwell Publishing Ltdof the Royal Society of Tropical Medicine and Hygiene 70,66–72.Solomon T, Thao LT & Kneen R (1998) Rapid diagnosis ofJapanese encephalitis by using an immunoglobulin M dotenzyme immunoassay. Journal of Clinical Microbiology 36,2030–2034.Solomon T, Thao LT, Dung NM et al. (2000) Japaneseencephalitis. Journal of Neurology, Neurosurgery andPsychiatry 68, 405–415.Tsai TF, Chang GJ & Yu YX (1999) Japanese encephalitisvaccines. In: Vaccines (eds SA Plotkin & WA Orenstein) WBSaunders Company, Philadelphia, pp. 672–710.Corresponding Author Mary Jane Cardosa, Institute of Health & Community Medicine, Universiti Malaysia Sarawak, Jalan DatukMusa, Kota Samarahan, Sarawak, Malaysia. E-mail: jane.cardosa@gmail.comTropical Medicine and International Health volume 13 no 1 pp 52–55 january 2008S. C. Wong et al. Japanese encephalitis in Sarawakª 2008 Blackwell Publishing Ltd 55

A decade of Japanese encephalitis surveillance in Sarawak, Malaysia-1997-2006

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A decade of Japanese encephalitis surveillance in Sarawak, Malaysia-1997-2006

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