Abstract
Japanese encephalitis is a mosquito borne disease and is the leading cause of viral encephalitis in the Asia-Pacific area. The causative agent, Japanese encephalitis virus (JEV) can be phylogenetically classified into five genotypes based on nucleotide sequence. In recent years, genotype I (GI) has displaced genotype III (GIII) as the dominant lineage, but the mechanisms behind this displacement event requires elucidation. In an earlier study, we compared host variation over time between the two genotypes and observed that GI appears to have evolved to achieve more efficient infection in hosts in the replication cycle, with the tradeoff of reduced infectivity in secondary hosts such as humans. To further investigate this phenomenon, we collected JEV surveillance data on human cases and, together with sequence data, and generated genotype/case profiles from seven Asia-Pacific countries and regions to characterize the GI/GIII displacement event. We found that, when comprehensive and consistent vaccination and surveillance data was available, and the GIII to GI shift occurred within a well-defined time period, there was a statistically significant drop in JEV human cases. Our findings provide further support for the argument that GI is less effective in infecting humans, who represent a dead end host. However, experimental investigation is necessary to confirm this hypothesis. The study highlights the value of alternative approaches to investigation of epidemics, as well as the importance of effective data collection for disease surveillance and control.
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Angami K, Chakravarty SK, Das MS, Chakraborty MS, Mukherjee KK. 1989. Seroepidemiological study of Japanese encephalitis in Dimapur, Nagaland. J Commun Dis, 21: 87–95.
Arai S, Matsunaga Y, Takasaki T, Tanaka-Taya K, Taniguchi K, Okabe N, Kurane I. 2008. Japanese encephalitis: surveillance and elimination effort in Japan from 1982 to 2004. Jpn J Infect Dis, 61: 333–338.
Burke DS, Leake CJ. 1988. Japanese encephalitis. In: The Arboviruses: epidemiology and ecology. T.P. Monath (ed.). Boca Raton: CRC Press, pp. 63–92.
Campbell GL, Hills SL, Fischer M, Jacobson JA, Hoke CH, Hombach JM, Marfin AA, Solomon T, Tsai TF, Tsu VD, Ginsburg AS. 2011. Estimated global incidence of Japanese encephalitis: a systematic review. Bull World Health Organ, 89: 766–774, 774A–774E.
Chakraborty AK, Chakravarti SK, Chakravarty MS. 1987. Outbreak of Japanese encephalitis in two districts of Assam during 1980: some epidemiological features. Indian J Public Health, 31: 5–11.
Chattopadhyay UK. 2001. A study on the status of Japanese encephalitis infection in Arunachal Pradesh. J Commun Dis, 33: 261–265.
Chen YY, Fan YC, Tu WC, Chang RY, Shih CC, Lu IH, Chien MS, Lee WC, Chen TH, Chang GJ, Chiou SS. 2011. Japanese encephalitis virus genotype replacement, Taiwan, 2009–2010. Emerg Infect Dis, 17: 2354–2356.
Dhillon GP, Raina VK. 2008. Epidemiology of Japanese encephalitis in context with Indian scenario. J Indian Med Assoc, 106: 660–663.
Dong D, Fu SH, Wang LH, Lv Z, Li TY, Liang GD. 2012. Simultaneous detection of three arboviruses using a triplex RT-PCR: enzyme hybridization assay. Virol Sin, 27: 179–186.
Fulmali PV, Sapkal GN, Athawale S, Gore MM, Mishra AC, Bondre VP. 2011. Introduction of Japanese encephalitis virus genotype I, India. Emerg Infect Dis, 17: 319–321.
George S, Yergolkar PN, Kamala H, Kamala CS. 1990. Outbreak of encephalitis in Bellary District of Karnataka & adjoining areas of Andhra Pradesh. Indian J Med Res, 91: 328–330.
Han N, Adams J, Chen P, Guo ZY, Zhong XF, Fang W, Li N, Wen L, Tao XY, Yuan ZM, Rayner S. 2014. Comparison of genotypes I and III in Japanese encephalitis virus reveals distinct differences in their genetic and host diversity. J Virol, 88: 11469–11479.
Henrich TJ, Hutchaleelaha S, Jiwariyavej V, Barbazan P, Nitatpattana N, Yoksan S, Gonzalez JP. 2003. Geographic dynamics of viral encephalitis in Thailand. Microbes Infect, 5: 603–611.
Ho Dang Trung N, Le Thi Phuong T, Wolbers M, Nguyen Van Minh H, Nguyen Thanh V, Van MP, Thieu NT, Van TL, Song DT, Thi PL, Thi Phuong TN, Van CB, Tang V, Ngoc Anh TH, Nguyen D, Trung TP, Thi Nam LN, Kiem HT, Thi Thanh TN, Campbell J, Caws M, Day J, de Jong MD, Van Vinh CN, Van Doorn HR, Tinh HT, Farrar J, Schultsz C. 2012. Aetiologies of central nervous system infection in Viet Nam: a prospective provincial hospital-based descriptive surveillance study. PLoS One, 7: e37825.
Huang JH, Lin TH, Teng HJ, Su CL, Tsai KH, Lu LC, Lin C, Yang CF, Chang SF, Liao TL, Yu SK, Cheng CH, Chang MC, Hu HC, Shu PY. 2010. Molecular epidemiology of Japanese encephalitis virus, Taiwan. Emerg Infect Dis, 16: 876–878.
Jan LR, Yueh YY, Wu YC, Horng CB, Wang GR. 2000. Genetic variation of Japanese encephalitis virus in Taiwan. Am J Trop Med Hyg, 62: 446–452.
Johansson MA, Cummings DA, Glass GE. 2009. Multiyear climate variability and dengue—El Nino southern oscillation, weather, and dengue incidence in Puerto Rico, Mexico, and Thailand: a longitudinal data analysis. PLoS Med, 6: e1000168.
Kabilan L, Vrati S, Ramesh S, Srinivasan S, Appaiahgari MB, Arunachalam N, Thenmozhi V, Kumaravel SM, Samuel PP, Rajendran R. 2004. Japanese encephalitis virus (JEV) is an important cause of encephalitis among children in Cuddalore district, Tamil Nadu, India. J Clin Virol, 31: 153–159.
Kar NJ, Bora D, Sharma RC, Bhattacharjee J, Datta KK, Sharma RS. 1992. Epidemiological profile of Japanese encephalitis in Gorakhpur district, Uttar Pradesh, 1982–1988. J Commun Dis, 24: 145–149.
Kaur R, Agarwal CS, Das D. 2002. An investigation into the JE epidemic of 2000 in Upper Assam—a perspective study. J Commun Dis, 34: 135–145.
KCDCP. 2012. (Korean Centre for Disease Control & Prevention). Public Health Weekly Report, 5: 491.
Konishi E, Kitai Y, Nishimura K, Harada S. 2012. Follow-up survey of Japanese encephalitis virus infection in Kumamoto Prefecture, South-West Japan: status during 2009-2011. Jpn J Infect Dis, 65: 448–450.
Kuwayama M, Ito M, Takao S, Shimazu Y, Fukuda S, Miyazaki K, Kurane I, Takasaki T. 2005. Japanese encephalitis virus in meningitis patients, Japan. Emerg Infect Dis, 11: 471–473.
Le Flohic G, Porphyre V, Barbazan P, Gonzalez JP. 2013. Review of climate, landscape, and viral genetics as drivers of the Japanese encephalitis virus ecology. PLoS Negl Trop Dis, 7: e2208.
Le VT, Phan TQ, Do QH, Nguyen BH, Lam QB, Bach V, Truong H, Tran TH, Nguyen V, Tran T, Vo M, Tran VT, Schultsz C, Farrar J, van Doorn HR, de Jong MD. 2010. Viral etiology of encephalitis in children in southern Vietnam: results of a one-year prospective descriptive study. PLoS Negl Trop Dis, 4: e854.
Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gotzsche PC, Ioannidis JP, Clarke M, Devereaux PJ, Kleijnen J, Moher D. 2009. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLoS Med, 6: e1000100.
Liu W, Clemens JD, Yang JY, Xu ZY. 2006. Immunization against Japanese encephalitis in China: a policy analysis. Vaccine, 24: 5178–5182.
Ma SP, Yoshida Y, Makino Y, Tadano M, Ono T, Ogawa M. 2003. Short report: a major genotype of Japanese encephalitis virus currently circulating in Japan. Am J Trop Med Hyg, 69: 151–154.
MHLWJ. 2011. (Ministry of Health, Labour and Welfare. Japan.) Current status of Japanese encephalitis vaccination. (In Japanese)
Mudur G. 2005. Japanese encephalitis outbreak kills 1300 children in India. BMJ, 331: 1288.
Mukherjee KK, Chakravarti SK, Mukherjee MK, De PN, Chatterjee S, Chatterjee P, Chakraborty MS. 1991. Recurrent outbreaks of Japanese encephalitis in Nagaland (1985-1989)—a seroepidemiological study. J Commun Dis, 23: 11–17.
Nga PT, del Carmen Parquet M, Cuong VD, Ma SP, Hasebe F, Inoue S, Makino Y, Takagi M, Nam VS, Morita K. 2004. Shift in Japanese encephalitis virus (JEV) genotype circulating in northern Vietnam: implications for frequent introductions of JEV from Southeast Asia to East Asia. J Gen Virol, 85: 1625–1631.
Nishijima N, Marusawa H, Ueda Y, Takahashi K, Nasu A, Osaki Y, Kou T, Yazumi S, Fujiwara T, Tsuchiya S, Shimizu K, Uemoto S, Chiba T. 2012. Dynamics of hepatitis B virus quasispecies in association with nucleos(t)ide analogue treatment determined by ultra-deep sequencing. PLoS One, 7: e35052.
Nitatpattana N, Dubot-Peres A, Gouilh MA, Souris M, Barbazan P, Yoksan S, de Lamballerie X, Gonzalez JP. 2008. Change in Japanese Encephalitis Virus Distribution, Thailand. Emerg Infect Dis, 14: 1762–1765.
NVBDCP. 2012. (India Ministry of Health & Family Welfare). Japanese Encephalitis cases 2008-2010.
Obara M, Yamauchi T, Watanabe M, Hasegawa S, Ueda Y, Matsuno K, Iwai M, Horimoto E, Kurata T, Takizawa T, Kariwa H, Takashima I. 2011. Continuity and change of Japanese encephalitis virus in Toyama Prefecture, Japan. Am J Trop Med Hyg, 84: 695–708.
Olsen SJ, Supawat K, Campbell AP, Anantapreecha S, Liamsuwan S, Tunlayadechanont S, Visudtibhan A, Lupthikulthum S, Dhiravibulya K, Viriyavejakul A, Vasiknanonte P, Rajborirug K, Watanaveeradej V, Nabangchang C, Laven J, Kosoy O, Panella A, Ellis C, Henchaichon S, Khetsuriani N, Powers AM, Dowell SF, Fischer M. 2010. Japanese encephalitis virus remains an important cause of encephalitis in Thailand. Int J Infect Dis, 14: e888–892.
Pan XL, Liu H, Wang HY, Fu SH, Liu HZ, Zhang HL, Li MH, Gao XY, Wang JL, Sun XH. 2011. Emergence of Genotype I of Japanese Encephalitis Virus as the Dominant Genotype in Asia. J Virol, 85: 9847–9853.
Parida M, Dash PK, Tripathi NK, Ambuj, Sannarangaiah S, Saxena P, Agarwal S, Sahni AK, Singh SP, Rathi AK, Bhargava R, Abhyankar A, Verma SK, Rao PV, Sekhar K. 2006. Japanese Encephalitis Outbreak, India, 2005. Emerg Infect Dis, 12: 1427–1430.
Phukan AC, Borah PK, Mahanta J. 2004. Japanese encephalitis in Assam, northeast India. Southeast Asian J Trop Med Public Health, 35: 618–622.
Potula R, Badrinath S, Srinivasan S. 2003. Japanese encephalitis in and around Pondicherry, South India: a clinical appraisal and prognostic indicators for the outcome. J Trop Pediatr, 49: 48–53.
Prasad SR, Kumar V, Marwaha RK, Batra KL, Rath RK, Pal SR. 1993. An epidemic of encephalitis in Haryana: serological evidence of Japanese encephalitis in a few patients. Indian Pediatr, 30: 905–910.
Rao JS, Misra SP, Patanayak SK, Rao TV, Das Gupta RK, Thapar BR. 2000. Japanese Encephalitis epidemic in Anantapur district, Andhra Pradesh (October-November, 1999). J Commun Dis, 32: 306–312.
Saito M, Taira K, Itokazu K, Mori N. 2007. Recent change of the antigenicity and genotype of Japanese encephalitis viruses distributed on Okinawa Island, Japan. Am J Trop Med Hyg, 77: 737–746.
Sarkar A, Taraphdar D, Mukhopadhyay SK, Chakrabarti S, Chatterjee S. 2012. Serological and molecular diagnosis of Japanese encephalitis reveals an increasing public health problem in the state of West Bengal, India. Trans R Soc Trop Med Hyg, 106: 15–19.
Sarkari NB, Thacker AK, Barthwal SP, Mishra VK, Prapann S, Srivastava D, Sarkari M. 2012. Japanese encephalitis (JE). Part I: clinical profile of 1,282 adult acute cases of four epidemics. J Neurol, 259: 47–57.
Saxena SK, Mishra N, Saxena R, Singh M, Mathur A. 2009. Trend of Japanese encephalitis in North India: evidence from thirty-eight acute encephalitis cases and appraisal of niceties. J Infect Dev Ctries, 3: 517–530.
Schuh AJ, Ward MJ, Leigh Brown AJ, Barrett AD. 2014. Dynamics of the emergence and establishment of a newly dominant genotype of Japanese encephalitis virus throughout Asia. J Virol.
Seo HJ, Kim HC, Klein TA, Ramey AM, Lee JH, Kyung SG, Park JY, Cho YS, Cho IS, Yeh JY. 2013. Molecular Detection and Genotyping of Japanese Encephalitis Virus in Mosquitoes during a 2010 Outbreak in the Republic of Korea. PLoS One, 8: e55165.
Shrivastva A, Tripathi NK, Parida M, Dash PK, Jana AM, Lakshmana Rao PV. 2008. Comparison of a dipstick enzyme-linked immunosorbent assay with commercial assays for detection of Japanese encephalitis virus-specific IgM antibodies. J Postgrad Med, 54: 181–185.
Sohn YM. 2000. Japanese encephalitis immunization in South Korea: past, present, and future. Emerg Infect Dis, 6: 17–24.
Solomon T, Thao TT, Lewthwaite P, Ooi MH, Kneen R, Dung NM, White N. 2008. A cohort study to assess the new WHO Japanese encephalitis surveillance standards. Bull World Health Organ, 86: 178–186.
Takhampunya R, Kim HC, Tippayachai B, Kengluecha A, Klein TA, Lee WJ, Grieco J, Evans BP. 2011. Emergence of Japanese encephalitis virus genotype V in the Republic of Korea. Virol J, 8: 449.
Tang WF, Ogawa M, Eshita Y, Aono H, Makino Y. 2010. Molecular evolution of Japanese encephalitis virus isolates from swine in Oita, Japan during 1980-2009. Infect Genet Evol, 10: 329–336.
Thakare JP, Shenoy SR, Padbidri VS, Rajput CS, Karmarkar DP, Deo SS. 1999. Japanese encephalitis in Sangli district, Maharashtra. Indian J Med Res, 109: 165–166.
Tiwari S, Singh RK, Tiwari R, Dhole TN. 2012. Japanese encephalitis: a review of the Indian perspective. Braz J Infect Dis, 16: 564–573.
TMPH. 2012. (Thai Ministry of Public Health). Thailand Health Profile Report 2008-2010: 171.
Tsai TF. 2000. New initiatives for the control of Japanese encephalitis by vaccination: minutes of a WHO/CVI meeting, Bangkok, Thailand, 13-15 October 1998. Vaccine, 18 Suppl 2: 1–25.
Umenai T, Krzysko R, Bektimirov TA, Assaad FA. 1985. Japanese encephalitis: current worldwide status. Bull World Health Organ, 63: 625–631.
Vajpayee A, Dey PN, Chakraborty AK, Chakraborty MS. 1992. Study of the outbreak of Japanese encephalitis in Lakhimpur district of Assam in 1989. J Indian Med Assoc, 90: 114–115.
Vajpayee A, Mukherjee MK, Chakraborty AK, Chakraborty MS. 1991. Investigation of an outbreak of Japanese encephalitis in Rourkela City (Orissa) during 1989. J Commun Dis, 23: 18–21.
Yen NT, Duffy MR, Hong NM, Hien NT, Fischer M, Hills SL. 2010. Surveillance for Japanese encephalitis in Vietnam, 1998-2007. Am J Trop Med Hyg, 83: 816–819.
Yun SM, Cho JE, Ju YR, Kim SY, Ryou J, Han MG, Choi WY, Jeong YE. 2010. Molecular epidemiology of Japanese encephalitis virus circulating in South Korea, 1983-2005. Virol J, 7: 127.
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Han, N., Adams, J., Fang, W. et al. Investigation of the genotype III to genotype I shift in Japanese encephalitis virus and the impact on human cases. Virol. Sin. 30, 277–289 (2015). https://doi.org/10.1007/s12250-015-3621-4
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DOI: https://doi.org/10.1007/s12250-015-3621-4