Serological Investigation of Japanese Encephalitis Virus Infection in Commercially Reared Pigs, Southwestern Nigeria
DOI:
https://doi.org/10.12834/VetIt.3021.20221.2Keywords:
Pigs, Abortion, Japanese encephalitis virus, zoonosis, antibodies, surveillance, seropositivity, southwestern NigeriaAbstract
Japanese encephalitis virus (JEV) is a zoonotic arbovirus that causes abortion, stillbirth, and congenital defects in pigs, and epidemic encephalitis in humans. Currently, there is scarcity of information on JEV infection in pigs in Nigeria. Since the Culex tritaeniorhynchus vector of JEV is present in Nigeria and considering recent anecdotal reports of abortions and birth of weak piglets in some pig farms in southwestern Nigeria, there is a need for studies on the presence of the virus and its true burden among pig populations in the country. Serum samples (n=368) obtained from farm-reared pigs in four States of southwestern Nigeria were screened for JEV-specific IgG antibodies using a commercial ELISA kit. An overall JEV seropositivity of 35.1% (95% CI: 30.18 – 39.93%) was obtained, with detectable antibodies in pigs of all age groups, breeds, sex, and locations. Our results suggest natural exposure of these unvaccinated intensively reared pigs to JEV circulating silently in the swine population with significant association of the seropositivity with location (state/community in which the pig farms exist) and breed of the pigs studied. This first report of detection of anti-JEV antibodies in pigs in Nigeria indicates that JEV circulated among these pigs and underscores the need for active surveillance for JEV in humans, pigs, and mosquitoes to provide valuable epidemiological data for the design of effective control strategies against the virus, thus forestalling potential future outbreaks of the infection.
References
Aiki-Raji C.O., Adebiyi A.I., Adeyemo I.A., Fagbohun O.A., & Oluwayelu D.O. 2014. Seroprevalence of classical swine fever antibodies in slaughtered pigs at Bodija municipal abattoir, Ibadan, Southwest Nigeria. European Journal of Scientific Research, 126(4), 402–407.
Aiki-Raji C.O., Adebiyi A.I., Abiola J.O., & Oluwayelu D.O. 2018. Prevalence of porcine reproductive and respiratory syndrome virus and porcine parvovirus antibodies in commercial pigs, southwest Nigeria. Beni-Suef University Journal of Basic and Applied Sciences, 7(1), 80–83.
Calisher C.H., Karabatsos N., Dalrymple J.M., Shope R.E., Porterfield J.S., Westaway E.G., & Brandt W.E. 1989. Antigenic relationships between flaviviruses as determined by cross-neutralization tests with polyclonal antisera. Journal of General Virology, 70(1), 37-43.
Cappelle J., Duong, V., Pring, L., Kong, L., Yakovleff M., Praseyo D.B., Peng B., Choeung R., Duboz R., Ong S., Sorn S., Dussart P., Tarantola A., Buchy P., & Chevalier V. 2016. Intensive Circulation of Japanese Encephalitis Virus in Peri-urban Sentinel Pigs near Phnom Penh, Cambodia. PLoS Neglected Tropical Diseases, 10(12), e0005149.
Chong H.Y., Leow C.Y., Abdul Majeed A.B., & Leow C.H. 2019. Flavivirus infection-A review of immunopathogenesis, immunological response, and immunodiagnosis. Virus Res. 274, 197770.
Coker R.J., Hunter B.M., Rudge J.W., Liverani M., & Hanvoravongchai P. 2011. Emerging infectious diseases in southeast Asia: regional challenges to control. The Lancet 377, 599–609.
Conlan, J.V., Vongxay, K., Jarman, R. G., Gibbons, R. v., Lunt, R. A., Fenwick S., Thompson R.C.A., & Blacksell S.D. 2012. Serologic study of pig-associated viral zoonoses in Laos. American Journal of Tropical Medicine and Hygiene, 86(6), 1077–1084.
Daniels P.W, Williams D.T, & Mackenzei J.S. Japanese encephalitis. In: Morilla A, Yoon K-J, Zimmerman JJ, editors. Trends in emerging viral infections of swine. Ames: Iowa State Press; 2002. P. 249-63.
Do Q.H., Vu T.Q.H., Huynh T.K.L., Dinh Q.T., & Deubel V.1994. Current situation of Japanese encephalitis in the south of Vietnam, 1976—1992. Trop Med 36: 202-214
Do L. P., Bui T. M., Hasebe F., Morita K., & Phan N. T. 2015. Molecular epidemiology of Japanese encephalitis in northern Vietnam, 1964-2011: genotype replacement. Virology Journal, 12, 51.
Dong-Kun Y., Chang-Hee K., Byoung-Han K., In-Jin H., Mun-II K., So B.J, & Cho K.O .2007. The seroprevalence of Japanese encephalitis virus in goats raised in Korea. Journal of Veterinary Science. J. Vet. Sci. (2007), 8(2), 197–199
Duong V., Sorn S., Holl D., Rani M., Deubel V., & Buchy P. 2011. Evidence of Japanese encephalitis virus infections in swine populations in 8 provinces of Cambodia: Implications for national Japanese encephalitis vaccination policy. Acta Tropica, 120(1–2), 146–150.
Faizah A. N., Kobayashi D., Amoa-Bosompem M., Higa Y., Tsuda Y., Itokawa K., Miura K., Hirayama K., Sawabe K., & Isawa H. 2020. Evaluating the competence of the primary vector, Culex tritaeniorhynchus, and the invasive mosquito species, Aedes japonicus japonicus, in transmitting three Japanese encephalitis virus genotypes. PLoS Neglected Tropical Diseases, 14(12), 1–18.
Jan L.R., Yueh Y.Y., Wu Y.C., Horng C.B.,& Wang G.R. 2000. Genetic variation of Japanese encephalitis virus in Taiwan. Am J Trop Med Hyg. 62(4), 446-452.
Kumar K., Arshad S. S., Selvarajah G. T., Abu J., Toung O. P., Abba Y., Bande F., Yasmin A.R., Sharma R., Ong B.L., Rasid A.A., Hashim N., Peli A., Heshini E.P., & Shah A.K.M.K. 2018. Prevalence and risk factors of Japanese encephalitis virus (JEV) in livestock and companion animal in high-risk areas in Malaysia. Tropical Animal Health and Production, 50(4), 741–752.
Kumar H.B.C., Dhanze H., Bhilegaonkar K.N., Chakurkar E.B., Kumar A., & Yathish H.M. 2020. Serological evidence of Japanese Encephalitis virus infection in pigs in a low human incidence state, Goa, India. Preventive Veterinary Medicine 175:104882.
Kumar, R. 2014. Prevention, diagnosis, and management of Japanese encephalitis in children. Pediatric Health, Medicine, and Therapeutics, 2014(5), 99-110.
Le Flohic G., Porphyre V., Barbazan P., & Gonzalez, J. P. 2013. Review of Climate, Landscape, and Viral Genetics as Drivers of the Japanese Encephalitis Virus Ecology. PLoS Neglected Tropical Diseases, 7(9), e2208.
Lee H. S., Thanh T. L., Ly N. K., Nguyen-Viet H., Thakur K.K., & Grace D. 2019. Seroprevalence of leptospirosis and Japanese encephalitis in swine in ten provinces of Vietnam. PLoS ONE, 14(8), e0214701.
Lindahl J., Chirico J., Boqvist S., Thu H. T. V., & Magnusson U. 2012. Occurrence of Japanese encephalitis virus mosquito vectors in relation to urban pig holdings. American Journal of Tropical Medicine and Hygiene, 87(6), 1076–1082.
Lindahl J. F., Ståhl K., Chirico, J., Boqvist S., Thu H. T. V., & Magnusson U.2013. Circulation of Japanese Encephalitis Virus in Pigs and Mosquito Vectors within Can Tho City, Vietnam. PLoS Neglected Tropical Diseases, 7(4), e2153.
Litzba N., Klade C. S., Lederer S., & Niedrig M. 2010. Evaluation of serological diagnostic test systems assessing the immune response to Japanese encephalitis vaccination. PLoS Neglected Tropical Diseases, 4(11), e883.
Mackenzie J.S., Chua K.B., Daniels P.W., Eaton B.T., Field H.E., Hall R.A., Halpin K., Johansen C.A., Kirkland P.D., Lam S.K., McMinn P., Nisbet D.J., Pyke A.T., Ritchie S.A., Siba P., Smith D.W., Smith G.A., Van den Hurk A.F., Wang L.F., & Williams D.T. 2001. Emerging viral diseases of Southeast Asia and the Western Pacific. Emerg Infect Dis 7, 497-504.
Mackenzie J. S., Johansen C. A., Ritchie S. A., Van den Hurk A. F., & Hall R. A. 2002. Japanese encephalitis as an emerging virus: The emergence and spread of Japanese encephalitis virus in Australasia. Current Topics in Microbiology and Immunology, 267, 49–73.
Mackenzie J. S., Williams D. T., & Smith D. W. 2006. Japanese Encephalitis Virus: The Geographic Distribution, Incidence, and Spread of a Virus with a Propensity to Emerge in New Areas. Perspectives in Medical Virology, 16, 201–268.
MacLachlan N.J., & Dubovi E.J. 2017. Flaviviridae. In: Fenner’s Veterinary Virology 5th Edition, Elsevier Inc., London, pp 525–545.
Maeki T., Tajima S., Ikeda M., Kato F., Taniguchi S., Nakayama E., Takasaki T., Lim C.K., & Saijo M. 2019. Analysis of cross-reactivity between flaviviruses with sera of patients with Japanese encephalitis showed the importance of neutralization tests for the diagnosis of Japanese encephalitis. Journal of Infection and Chemotherapy, 25(10), 786–790.
Mansfield K. L., Hernández-Triana L. M., Banyard A. C., Fooks A. R., & Johnson N. 2017. Japanese encephalitis virus infection, diagnosis, and control in domestic animals. Veterinary Microbiology, 201, 85–92.
Mulvey P., Duong V., Boyer S., Burgess G., Williams D. T., Dussart P., & Horwood P.F. 2021. The ecology and evolution of Japanese encephalitis virus. Pathogens, 10(12), 1534.
Nitatpattana N., le Flohic G., Thongchai P., Nakgoi K., Palaboodeewat S., Khin M., Barbazan P., Yoksan S., & Gonzalez J.P.2011. Elevated Japanese encephalitis virus activity monitored by domestic sentinel piglets in Thailand. Vector-Borne and Zoonotic Diseases, 11(4), 391–394.
Omodele T., Okere I.A., Oladele-Bukola M.O., Omole A.J., Oyegbami A. 2019. Application of GIS in pig production system in Nigeria. African Journal of Agricultural Research, 14(25), 1042–1050.
Pant G. R. 2006. A serological survey of pigs, horses, and ducks in Nepal for evidence of infection with Japanese encephalitis virus. Annals of the New York Academy of Sciences, 1081, 124–129.
Park S. L., Huang Y. J. S., & Vanlandingham, D. L. 2022. Re-Examining the Importance of Pigs in the Transmission of Japanese Encephalitis Virus. Pathogens, 11, 575.
Pearce J. C., Learoyd T. P., Langendorf B. J., & Logan J. G. 2018. Japanese encephalitis: the vectors, ecology, and potential for expansion. 25, 16–26.
Ricklin M. E., Garcìa-Nicolàs O., Brechbühl D., Python S., Zumkehr B., Posthaus H., Oevermann A., & Summerfield A. 2016. Japanese encephalitis virus tropism in experimentally infected pigs. Veterinary Research, 47, 34.
Sasaki O., Karoji Y., Kuroda A., Karaki T., Takenokuma K., & Maeda O. 1982. Protection of pigs against mosquito-borne Japanese encephalitis virus by immunization with a live attenuated vaccine. Antiviral Research 2(6), 355-360.
Scherer W.F., Moyer J.T., & Izumi T. 1959. Immunologic studies of Japanese encepahliltis virus in Japan: Maternal anitbodies, antibody responses and viremia following infection of swine. The Journal of Immunology. Am Assoc Immunol. 83: 620-626.
Simon-Loriere E., Faye O., Prot M., Casademont I., Fall G., Fernandez-Garcia., Diagne M.M., Kipela J.M., Fall I.S., Holmes E.C., Sakuntabhai A., & Sall A.A. 2017. Autochthonous Japanese Encephalitis with Yellow Fever Coinfection in Africa. New England Journal of Medicine 376:1483-1485.
Soman R., Rodrigues F., Guttikar S., Guru P. 1977. Experimental viraemia and transmission of Japanese encephalitis virus by mosquitoes in ardeid birds. Indian Journal of Medical Research, 66, 709–718.
Takashima I., Watanabe T., Ouchi N., & Hashimoto, N. 1988. Ecological studies of Japanese encephalitis virus in Hokkaido: interepidemic outbreaks of swine abortion and evidence for the virus to overwinter locally. Am. I. Trop. Med. Hyg 38(2), 420-427.
Tarantola A., Goutard F., Newton P., de Lamballerie X., Lortholary O., Cappelle J., & Buchy P. 2014. Estimating the Burden of Japanese Encephalitis Virus and Other Encephalitides in Countries of the Mekong Region. PLoS Neglected Tropical Diseases, 8(1), e2533.
Thakur K. K., Pant G. R., Wang L., Hill C. A., Pogranichniy R. M., Manandhar S., & Johnson A.J. 2012. Seroprevalence of Japanese Encephalitis Virus and Risk Factors Associated with Seropositivity in Pigs in Four Mountain Districts in Nepal. Zoonoses and Public Health, 59(6), 393–400.
Udeze A. O., & Odebisi-Omokanye M. B. 2022. Sero-evidence of silent Japanese Encephalitis Virus infection among inhabitants of Ilorin, North-central Nigeria: a call for active surveillance. Journal of Immunoassay and Immunochemistry, 43(3), 250–258.
Unni S. K., Růžek D., Chhatbar C., Mishra R., Johri M. K., & Singh S.K. 2011. Japanese encephalitis virus: From genome to infectome. Microbes and Infection, 13(4), 312–321.
van den Hurk A. F., Ritchie S. A., & Mackenzie J. S. 2009. Ecology and geographical expansion of Japanese encephalitis virus. Annual Review of Entomology, 54, 17–35.
World Health Organization. 2019. Japanese encephalitis fact sheets. https://www.who.int/news-room/fact-sheets/detail/japanese-encephalitis (Accessed 12 August 2022).
Yamanaka A., Mulyatno K. C., Susilowati H., Hendrianto E., Utsumi T., Amin M., Lusida M.I., Soegijanto S., & Konishi E. 2010. Prevalence of Antibodies to Japanese Encephalitis Virus among Pigs in Bali and East Java, Indonesia, 2008. Jpn. J. Infect. Dis 63, 58-60.
Yang D.K., Kweon C.H., Kim B.W., Hwang I.J., Kang M.I., So B.J., Cho K.O. 2007. The seroprevalence of Japanese encephalitis virus in goats raised in Korea. Journal of Veterinary Science, 8, 197–199.
Yin Z., Wang H., Yang J., Luo H., Li Y.,Hadler S.C., Sandhu H.S., Fischer M., Jiang Y., Zhang Z., Liu G., Li L., Johnson B.W., & Liang X. 2010. Japanese encephalitis disease burden and clinical features of Japanese encephalitis in four cities in the People’s Republic of China. American Journal of Tropical Medicine and Hygiene, 83(4), 766–773.
Yun S. I., & Lee Y. M. 2014. Japanese encephalitis the virus and vaccines. Human Vaccines and Immunotherapeutics, 10(2), 263–279.