enzyme-linked immunosorbent assay, Japanese encephalitis virus, Macaca fascicularis, seroprevalence
Abstract :
[en] Background and Aim: Japanese encephalitis (JE) is a zoonotic infectious inflammatory brain disease caused by the JE virus (JEV). Considerable research into the seroprevalence of JE in domestic animals has been conducted, but there have been no reports of its occurrence in wild animals, including long-tailed macaques (Macaca fascicularis). This study aimed to estimate the seroprevalence of JEV infection and its determinants in long-tailed macaques in Bali and the prevalence of mosquito vectors.
Materials and Methods: Blood samples (3 mL) were collected from a population of M. fascicularis (92 heads) inhabiting a small forest with irrigated rice field nearby (wetland area) in Ubud, Gianyar, and from two populations in dryland areas with no wet rice field (Uluwatu, Badung, and Nusa Penida, Bali Province, Indonesia). The collected sera were tested for antibodies against JEV using a commercially available enzyme-linked immunosorbent assay kit (qualitative monkey JE Immunoglobulin G antibody kit). The seropositivity of the antibodies was then compared based on different variables, namely, habitat type, age, and sex.
Results: The seroprevalence of the JEV antibodies in all the samples tested was found to be 41.3%. The seropositivity of the monkey serum samples collected from the wetland area was 46.4%, which was higher than the seropositivity of the sera samples collected from the dried field areas (1.25%). Monkey sera collected from the wetland areas were 6.1 times (odds ratio [OR]: 6.1; 95% confidence interval [CI]: 0.71-51.5, p>0.05) more likely to be seropositive compared to the monkey sera collected from the dried field areas. Meanwhile, female monkeys were 1.79 times (OR: 1.79; 95% CI: 0.76-4.21; p>0.05) more likely to be seropositive to JEV than males. Similarly, juvenile monkeys were 2.38 times (OR: 2.38; 95% CI: 0.98-5.79); p>0.05) more likely to be seropositive against the JEV than adult monkeys. However, none of these differences achieved statistical significance. Regarding the JEV mosquito vector collection, more Culex mosquitoes were found in the
samples from the wetland areas than from the dried field areas.
Conclusion: The study confirms the existence of JEV infection in long-tailed macaques in Bali. There were patterned seropositivity differences based on habitat, age, and sex of the monkeys, but these were not significant. The possibility of monkeys as a JEV reservoir and the presence of the mosquitoes as the JEV vector are suggested but require more study to
confirm.
Disciplines :
Veterinary medicine & animal health
Author, co-author :
Putra, Gusti Agung Arta
Adi, Anak Agung Ayu Mirah
Astawa, Nyoman Mantik
Kardena, Made
Wandia, Nengah
Soma, Gede
Brotcorne, Fany ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Biologie du comportement - Ethologie et psychologie animale ; Université de Liège - ULiège > Sphères
Fuentes, Agustin
Language :
English
Title :
First survey on seroprevalence of Japanese encephalitis in long-tailed macaques (Macaca fascicularis) in Bali, Indonesia
Patabendige, A., Michael, B.D., Craig, A.G. and Solomon, T. (2018) Brain microvascular endothelial-astrocyte cell responses following Japanese encephalitis virus infection in an in vitro human blood-brain barrier model. Mol. Cell. Neurosci., 89: 60-70.
Yun, S.I. and Lee, Y.M. (2018) Early events in Japanese encephalitis virus infection: Viral entry. Pathogens (Basel, Switzerland), 7(3): 68.
Lian, W.C., Liau, M. and Mao, C.L. (2002) Diagnosis and genetic analysis of Japanese encephalitis virus in infected horses. J. Vet. Med. Series B, 49(8): 361-365.
Sendow, I., Bahri, S. and Sarosa, A. (2000) Prevalensi Japanese-B-enchepalitis pada berbagai spesies ternak di Indonesia. Indonesian J. Anim. Vet. Sci., 5(1): 46-53.
Adi, A.A.A., Astawa, N.M., Damayanti, P.A.A., Kardena, I.M., Erawan, I.G.M., Suardana, I.W., Putra I G.A. and Matsumoto, Y. (2016) Seroepidemiological evidence for the presence of Japanese encephalitis virus infection in ducks, chickens, and pigs, Bali-Indonesia. Bali Med. J., 5(3): 189-193.
Damayanti, P.A.A., Adi, A.A.A., Astawa, I.N.M., Sudarmaja, I.M., Kardena, I.M. and Swastika, I.K. (2017) Incidence of Japanese encephalitis among children is associated with the presence of pigs in Bali, Indonesia. Biomed. Pharmacol. J., 10(3): 1237.
Inoue, S., Morita, K., Matias, R.R., Tuplano, J.V., Resuello, R.R.G., Candelario, J.R., Cruz, D.J.M., Mapua, C.A., Hasebe, F., Igarashi, A. and Natividad, F.F. (2003) Distribution of three arbovirus antibodies among monkeys (Macaca fascicularis) in the Philippines. J. Med. Primatol., 32(2): 89-94.
Nakgoi, K., Nitatpattana, N., Wajjwalku, W., Pongsopawijit, P., Kaewchot, S., Yoksan, S., Siripolwat, V., Souris, M. and Gonzalez, J. (2014) Dengue, Japanese encephalitis and chikungunya virus antibody prevalence among captive monkey (Macaca nemestrina) colonies of Northern Thailand. Am. J. Primatol., 76(1): 97-102.
Cappelle, J., Duong, V., Pring, L., Kong, L. Yakovleff, M., Prasetyo, D.B., Peng, B., Choeung, R., Duboz, R., Ong, S., Sorn, S., Dussart, P., Tarantola, A., Buchy, P. and Chevalier, V. (2016) Intensive circulation of Japanese encephalitis virus in peri-urban sentinel pigs near Phnom Penh, Cambodia. PLoS Negl. Trop. Dis., 10(12): e0005149.
Changbunjong, T., Weluwanarak, T., Taowan, N., Suksai, P., Chamsai, T. and Sedwisai, P. (2013) Seasonal abundance and potential of Japanese encephalitis virus infection in mosquitoes at the nesting colony of ardeid birds, Thailand. Asian Pac. J. Trop. Biomed., 3(3): 207-210.
Hurk, A.F.V., Ritchie, S.A., Johansen, C.A., Mackenzie, J.S. and Smith, G.A. (2008) Domestic pigs and Japanese encephalitis virus infection, Australia. Emerg. Infect. Dis., 14(11): 1736-1738.
Igarashi, A. (2002) Control of Japanese encephalitis in Japan: Immunization of humans and animals, and vector control. Curr. Top. Microbiol. Immunol., 267: 139-152.
Ravanini, P., Huhtamo, E., Ilaria, V., Crobu, M.G., Nicosia, A.M., Servino, L., Rivasi, F., Allegrini, S., Miglio, U., Magri, A., Minisini, R., Vapalahti, O. and Boldorini, R. (2012) Japanese encephalitis virus RNA detected in Culex pipiens mosquitoes in Italy. Euro. Surveill., 17(28): 20221.
Pearce, J., Learoyd, T.P., Langendorf, B.J. and Logan, J.G. (2018) Japanese encephalitis: The vectors, ecology and potential for expansion. J. Travel Med., 25(1): S16-S26.
Valentine, M.J., Murdock, C.C. and Kellu, P.J. (2019) Sylvatic cycles of arboviruses in non-human primates. Parasites Vectors, 12(1):463.
Giraud, G., Sosa, S., Hambuckers, A., Deleuze, S., Wandia, I.N., Huynen, M.C., Poncin, P. and Brotcorne, F. (2021) Effect of infant presence on social networks of sterilized and intact wild female Balinese macaques (Macaca fascicularis). Animals, 11(9): 2538.
Brotcorne, F., Holzner, A., Jorge-Sales L., Gunst, N., Hambuckers, A., Wandia, I.N. and Leca, J.B. (2020) Social influence on the expression of robbing and bartering behaviours in Balinese long-tailed macaques. Anim. Cogn., 23(2): 311-326.
Deleuze, S., Brotcorne, F., Polet, R., Soma, G., Rigaux, G., Giraud, G., Cloutier., Poncin, P., Wandia, N. and Huynen, M.C. (2021) Tubectomy of pregnant and non-pregnant female Balinese macaques (Macaca Fascicularis) with post-operative monitoring. Front. Vet. Sci., 8: 688656
DEPKES RI-Direktorat Jendral Pemberantasan Penyakit Menular dan Penyehatan Lingkungan. (2000) Kunci Bergambar Identifikasi Nyamuk Culex Dewasa di Jawa. DEPKES RI-Direktorat Jendral Pemberantasan Penyakit Menular dan Penyehatan Lingkungan, Indonesia.
Kardena, I.M., Adi, A.A.A. and Astawa, N.M. (2021) Comparison of a commercial and a manual antigen-coated ELISA tests used in detecting antibodies against Japanese encephalitis virus in pig serums collected from the Province of Bali. Int. J. Vet. Sci. Anim. Husb., 6(4): 34-39.
Kardena, I.M., Adi, A.A.A., Astawa, N.M., O'Dea M., Laurence, M., Sahibzada, S. and Bruce, M. (2021) Japanese encephalitis in Bali, Indonesia: Ecological and socio-cultural perspectives. Int J Vet. Sci. Med., 9(1): 31-43.
Kari, K., Liu, W., Gautama, K., Mammen, M.P. Jr., Clemens, J.D., Nisalak, A., Subrata, K., Kim, H.K. and Xu, Z.Y. (2006) A hospital-based surveillance for Japanese encephalitis in Bali, Indonesia. BMC Med., 4(8 ): 1-7.
Bhattacharya, S., and Basu, P. (2014) Japanese encephalitis virus (JEV) infection in different vertebrates and its epidemiological significance: A Review. Int. j. fauna biol. Stud. 1(6): 32-14.21.
Cleton, N., Bosco-Lauth, A., Page, M.J., and Bowen, R. A. (2014) Age-related susceptibility to Japanese encephalitis virus in domestic ducklings and chicks. Am. J. Trop. Med. Hyg., 90(2), 242-246.
Lord, J.S., Gurley, E.S., and Pulliam J.R.C. (2015) Rethinking Japanese encephalitis virus transmission: A Framework for implicating host and vector species. PLoS Negl. Trop. Dis., 9(12): e0004074.
Kardena, I.M., Adi, A.A.A., Astawa, N.M., Oka I.B.M. and Dwinata, I.M. (2022) Mosquito diversity and abundance collected from paddy fields and animal farms in Bali province, Indonesia. Int. J. Mosq. Res., 9(1): 18-23.
Hurk, A.F.V., Ritchie, S.A. and Mackenzie, J.S. (2009) Ecology and geographical expansion of Japanese encephalitis virus. Ann. Rev. Entomol., 54: 17-35.
Bae, W., Kim, J.H., Kim, J., Lee, J. and Hwang, E.S. (2018) Changes of epidemiological characteristics of Japanese encephalitis viral infection and birds as a potential viral transmitter in Korea. J. Korean Med. Sci., 33(9): e70.
Nitatpattana, N., Apiwathnasorn, C., Barbazan, P., Leemingsawat, S., Yoksan, S. and Gonzalez, J.P. (2005) First isolation of Japanese encephalitis from Culex quinquefasciatus in Thailand. Southeast Asian J. Trop. Med. Public Health, 36(4): 875-858.
Su, C.L., Yang, C.F., Teng, H.J., Lu, L.C., Lin, C., Tsai, K.H., Chen, Y.Y., Chen, L.Y., Chang, S.F. and Shu, P.Y. (2014) Molecular epidemiology of Japanese encephalitis virus in mosquitoes in Taiwan during 2005-2012. PLoS Negl. Trop. Dis., 8(10): e3122.
Hameed, M., Wahaab, A., Nawaz, M., Khan, S., Nazir, J., Liu, K., Wei, J. and Ma, Z. (2021) Potential role of birds in Japanese encephalitis virus zoonotic transmission and genotype shift. Viruses, 13(3): 357.
Zhang, S., Hu, W., Qi, X. and Zhuang, G.G. (2018) How socio-environmental factors are associated with Japanese encephalitis in Shaanxi, China-a bayesian spatial analysis. Int. J. Environ. Res. Public Health, 15(608): 1-13.
Solomon, T. (2006) Control of Japanese encephalitis-within our grasp? N. Engl. J. Med., 355(9): 869-871.
Rawal, D. (2019) A review on different strategies used for biological control of mosquitoes. Int. J. Mosq. Res., 6(5): 41-3.