Serological markers for hepatitis a among captive and free-living wild mammals in the State of Pará, Brazil
DOI:
https://doi.org/10.5433/1679-0359.2021v42n3Supl1p1635Keywords:
Amazon, Viral hepatitis, Hepatovirus A., Mastofauna, Serology.Abstract
The hepatitis A virus (HAV, Hepatovirus A) in humans has a relevant impact on public health, especially in geographic regions with poor basic sanitation, such as the Brazilian Amazon. Isolates related to hepatoviruses have been described in non human primates, chiropterans, marsupials, rodents, marmots, shrews, and terrestrial hedgehogs. However, the circulation of these viruses in the Amazonian mammal fauna remains unexplored. This study aimed to evaluate the prevalence of antibodies against this hepatovirus in captive and free-living wild mammals belonging to the orders Didelphimorphia, Primates, Carnivora, and Artiodactyla. Serum samples from 71 animals, from three municipalities in the State of Pará (Belém, Santarém, and Capitão-Poço) were tested for total anti-HAV and anti-HAV IgM through enzyme-linked immunosorbent assay (ELISA). Total anti-HAV antibodies were detected in 29.5% (21/71) of non-human primates, 8.4% (6/71) of carnivores, and 5.6% (4/71) of didelphos. All tayassuidos 0% (0/2) were seronegative. Anti-HAV IgM antibodies were not detected in any of the samples tested. The highest total anti-HAV seropositivity in the municipalities studied was in Santarém with 54.24% (12/22), followed by Capitão Poço with 50% (15/30), and then Belém with 21.05% (4/19). Among the seropositive animals, animals kept in exposure cages showed 43.9% (18/41), quarantined animals with 60% (9/15), and free-living animals with 26.6% (4/15). The serological results indicated a profile of previous exposure to hepatovirus among these animals. Therefore, additional studies to characterize HAV-related viruses in captive and free living wild animals need to be conducted to better understand the impact of the circulation of this virus on human and animal health.Downloads
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References
Aggarwal, R., & Goel, A. (2015). Hepatitis A: epidemiology in resource-poor countries. Current Opinion Infection Diseases, 28(5), 488-496. doi: 10.1097/QCO.0000000000000188
Anthony, S. J., Leger, J. A. S. T., Liang, E., Hicks, A. L., Sanchez-Leon, M. D., Jain, K.,… Lipkin, W. I. (2015). Discovery of a novel hepatovirus (Phopivirus of Seals) related to human Hepatitis A virus. MBio, 6(4), 1-10. doi: 10.1128/mBio.01180-15
Bennett, A. J., Sibley, S. D., Lauck, M., Weny, G., Hyeroba, D., Tumukunde, A.,… Goldberg, T. L. (2016). Natturally circulating Hepatitis A Virus in Olive. Emerg Infection Disease, 22(7), 1308-1310. doi: 10. 3201/eid2207.151837
Bensabath, F., & Leão, R. N. Q. (2016). Epidemiologia na Amazônia brasileira. In R. Focaccia (Ed.), Tratado das Hepatites Virais (pp. 11-26) São Paulo: Atheneu.
Bensabath, G., Soares, M. C. P. & Maia, M. M. S. (1986). Hepatite por vírus. (p. 483-529) In Instituto Evandro Chagas: 50 anos de contribuição às Ciências Biológicas e à Medicina Tropical. Brasil, Belém: Fundação Serviços de Saúde Pública.
Carneiro, I. O., Sander, A. L., Silva, N., Moreira-Soto, A., Normann, A., Flehmig, B.,... Drexler, J. F. (2018). A novel marsupial hepatites A vírus corroborates complex evolutionary patterns shaping the genus Hepatovirus. Journal Virology, 92(13), 1-37. doi: 10.1128/JVI.00082-18
Center for Disease Control and Prevention (2009). Epidemiologic notes and reports hepatitis A among drug abusers. United States: MMWR Surveill.
Clemens, S. A. C., Fonseca, J. C., Azevedo, T., Calvalcanti, A., Silveira, T. R., Castilho, M. C., & Clemens, R. (2000). Soroprevalência para hepatite A e hepatite B em quatro centros no Brasil. Revista da Sociedade Brasileira de Medicina Tropical, 33(1), 1-10. doi: 10.1590/S0037-86822000000100001
Drexler, J. F., Corman, V. M., Lukashev, A. N., Brand, J. M. A., Gmyl, A. P., Brunink, S.,... Consortium, H. E. (2015). Evolutionary origins of hepatites Avirus in small mammals. PNAS, 112(49), 1-6. doi: 10.10 73/pnas.1516992112
Eichberg, J. W., & Kalter, S. S. (1980). Hepatitis A and B: serologic survey of human and nonhuman primate sera. Laboratory Animal Science, 30(3), 541-543. Retrived from https://europepmc.org/article/ med/6253744
Hollinger, F. B., & Emerson, S. U. (2001). Hepatitis A virus. In D. M. Knipe, & P. M. Howley (Eds.), Fields virology (pp. 799-840). New York: Lippincott Williams & Wilkins.
Hollinger, F. B., & Martin, A. (2013). Hepatitis a virus. In W. Kluwer (Ed.), Field’s virology (pp. 550-581). Philadelphia: Lippincott Williams & Wilkins.
Horney, B., Kammerer, R., Moubayed, P., Frings, W., Gauss-muller, V., & Dotzauer, A. (2001). Experimental hepatitis A virus infections in Guinea Pigs. Journal of Medical Virology, 64(4), 402-409. doi: 10.1002/jmv.1065
International Committee on Taxonomy of Viruses (2018). Taxonomy of viruses. Retrieved from https://talk. ictvonline.org/
Jacobsen, K. H., & Wiersma, S. T. (2010). Hepatitis A virus seroprevalence by age and world region, 1990 and 2005. Vaccine, 28(41), 6653-6657. doi: 10.1016/j.vaccine.2010.08.037
Jones, K. E., Patel, N. G., Levy, M. A., Storeygard, A., Balk, D., Gittleman, J. L., & Daszak, P. (2008). Global trends in emerging infectious diseases. Nature, 451(21), 990-993. doi: 10.1038/nature06536
Koff, R. D. (1992). Clinical manifestations and diagnosis of hepatitis A vírus infection. Vaccine, 10(1), 15-17. doi: 10.1016/0264-410X(92)90533-P
Koff, R. S. (1998). Hepatitis A. Lancet, 351(1), 1643-1649. doi: 10.1016/S0140-6736(98)01304-X
Lanford, R. E., Walker, C. M., & Lemon, S. M. (2019). Nonhuman primate models of Hepatitis A virus and Hepatitis E virus infections. Cold Spring Harb Perspect Medicine, 9(2), 1-29. doi: 10.1101/cshperspect. a031815 .
Leão, R. N. Q., Bichara, C. N. C., Fraiha, N., Neto, & Vasconcelos, P. F. C. (2013). Medicina Tropical e infectologia na Amazônia (pp. 685-740). Brasil: Samauma.
Leduc, J. W., Lemon, S. M., Keenan, C. M., Graham, R. R., Marchwicki, R. H., & Binn, L. H. (1983). Experimental infection of the new world owl monkey (Aotus trivirgatus) with hepatitis A virus. Infection and Immunity, 40(2), 766-772. doi: 10.1128/IAI.40.2.766-772.1983
Lemon, S. M., Leduc, J. W., Binn, L. N., Escajadillo, A., & Ishak, K. G. (1982). Transmission of hepatitis A vírus among recently captured Panamian owl monkeys. Journal of Medical Virology, 10, 25-36. doi: 10. 1002/jmv.1890100105
Lewisohn, T. M., & Prado, P. I. (2002). Biodiversity of Brazil: a synthesis of the current state of knowledge. São Paulo: Contexto Acadêmica.
Nath, B. G., Chakraborty, A., Sarma, D. K., Rahman, T., & Boro, P. K. (2013). Seroprevalence of Hepatitis A virus infection in non-human primates in Assam, Indian. Journal of Threatened, 5(12), 4722-4724. doi: 10.11609/JoTT.o3121.4722-4
Paula, V. S. de. (2012). Laboratory diagnosis of hepatitis A. Future Virology, 7(5), 461-472. doi: 10.2217/ fvl.1235
Pereira, W. L. A., Galo, K. R., Silva, K. S. M. D., Soares, M. D. C. P., & Alves, M. M. (2010). Viral hepatitis, helminthiasis and protozoan disease in neotropical primates reaised in captivity: potentially zoonotic affections with fecal-oral transmission. Revista Pan Amazônica Saúde, 1(3), 57-60. doi: 10.51 23/S2176-62232010000300008
Reis, N. R., Peracchi, A. L., Fregonezi, M. N., & Rossaneis, B. K. (2010). Mamíferos do Brasil: guia de identificação. São Paulo: Technical Books.
Robertson, B. H. (2001). Viral hepatitis and primates: historical and molecular analysis of human and nonhuman primate hepatitis A, B and GB-related viruses. Journal of Viral Hepatitis, 8(4), 233-242. doi: 10.1046/j.1365-2893.2001.00295.x
San-nguanmoo, P., Thawornsuk, N., Rianthavorn, P., Sommanustweechai, A., Ratanakorn, P., & Poovorawan, Y. (2010). High prevalence of antibodies against hepatitis A virus among captive nonhuman primates. Primates, 51(2), 167-170. doi: 10.1007/s10329-009-0172-z
Setzer, A. P., Gaspar, A. M. C., Sidoni, M., Bueno, M. G., & Catão-Dias, J. L. (2014). Serosurvey for hetatitis A in neotropical primates in southeast Brazil. Journal Medical Primatology, 43(3), 202-205. doi: 10.1111/jmp.12106.
Seymor, I. J., Appletton, H. (2001). Foodborne viruses and fresh produce. Journal of Applied Microbiology, 91(5), 759-773. doi: 10.1111/jmp.12106
Soares, M. C. P., Bensabath, G., & Travassos Da Rosa, A. P. A. (1987). Presença de anticorpos para vírus da hepatite A em Didelphis marsupialis (Vertebrata, Marsupialia) da Amazônia. Revista do Instituto de Medicina Tropical, 29(2), 110-111. doi: 10.1590/S0036-46651987000200008
Svoboda, W. K., Soares, M. C. P., Alves, M. M., Rocha, T. C., Gomes, E. C., Menonci, F.,... Navarro, I. T. (2016). Serological detection of hepatitis A virus in free-ranging neotropical primates (Sapajus spp., Aluatta caraya) from the Paraná river basin, Brasil. Revista do Instistituto de Medicina Tropical, 58(9), 1-6. doi: 10.1590/S1678-994658009
Vaughan, G., Rossi, L. M. G., Forbi, J. C., Paula, V. S. de, Purdy, M. A., Xia, G., & Khudyakov, Y. E. (2014). Hepatitis A virus: host interactions, molecular epidemiology and evolution. Infection, Genetics and Evolution, 21(4), 227-243. doi: 10.1016/j.meegid.2013.10.023
Wang, W. L., Li, B., Zhang, W., Zhu, Y., Shi, Z. L., & Yang, X. L. (2018). Genomic characterization of novel hepatovirus from great roundleaf bats in China. Virologica Sinica, 33(1), 108-110. doi: 10.1007/s 12250-018-0013-6
Wang, X., Ren, J., Gao, Q., Hu, Z., Sun, Y., Li, X.,… Fry, E. E. (2015). Hepatitis A virus and the origins of picornaviruses. Nature, 517(1), 85-88. doi: 10.1038/nature13806
Yahner, R. H. (1992). Dynamics of small mammal community in a fragment forest. American Midland Naturalist, 127(2), 381-391. doi: 10.2307/2426545
Yu, J., Li, L., Zhang, C., Lu, S., Ao, Y., Gao, H.,… Duan, Z. J. (2016). A novel hepatovirus identified in wild woodchuck Marmota himalayana. Scientific reports. Nature, 6(1), 1-11. doi: 10.1038/srep22361
Anthony, S. J., Leger, J. A. S. T., Liang, E., Hicks, A. L., Sanchez-Leon, M. D., Jain, K.,… Lipkin, W. I. (2015). Discovery of a novel hepatovirus (Phopivirus of Seals) related to human Hepatitis A virus. MBio, 6(4), 1-10. doi: 10.1128/mBio.01180-15
Bennett, A. J., Sibley, S. D., Lauck, M., Weny, G., Hyeroba, D., Tumukunde, A.,… Goldberg, T. L. (2016). Natturally circulating Hepatitis A Virus in Olive. Emerg Infection Disease, 22(7), 1308-1310. doi: 10. 3201/eid2207.151837
Bensabath, F., & Leão, R. N. Q. (2016). Epidemiologia na Amazônia brasileira. In R. Focaccia (Ed.), Tratado das Hepatites Virais (pp. 11-26) São Paulo: Atheneu.
Bensabath, G., Soares, M. C. P. & Maia, M. M. S. (1986). Hepatite por vírus. (p. 483-529) In Instituto Evandro Chagas: 50 anos de contribuição às Ciências Biológicas e à Medicina Tropical. Brasil, Belém: Fundação Serviços de Saúde Pública.
Carneiro, I. O., Sander, A. L., Silva, N., Moreira-Soto, A., Normann, A., Flehmig, B.,... Drexler, J. F. (2018). A novel marsupial hepatites A vírus corroborates complex evolutionary patterns shaping the genus Hepatovirus. Journal Virology, 92(13), 1-37. doi: 10.1128/JVI.00082-18
Center for Disease Control and Prevention (2009). Epidemiologic notes and reports hepatitis A among drug abusers. United States: MMWR Surveill.
Clemens, S. A. C., Fonseca, J. C., Azevedo, T., Calvalcanti, A., Silveira, T. R., Castilho, M. C., & Clemens, R. (2000). Soroprevalência para hepatite A e hepatite B em quatro centros no Brasil. Revista da Sociedade Brasileira de Medicina Tropical, 33(1), 1-10. doi: 10.1590/S0037-86822000000100001
Drexler, J. F., Corman, V. M., Lukashev, A. N., Brand, J. M. A., Gmyl, A. P., Brunink, S.,... Consortium, H. E. (2015). Evolutionary origins of hepatites Avirus in small mammals. PNAS, 112(49), 1-6. doi: 10.10 73/pnas.1516992112
Eichberg, J. W., & Kalter, S. S. (1980). Hepatitis A and B: serologic survey of human and nonhuman primate sera. Laboratory Animal Science, 30(3), 541-543. Retrived from https://europepmc.org/article/ med/6253744
Hollinger, F. B., & Emerson, S. U. (2001). Hepatitis A virus. In D. M. Knipe, & P. M. Howley (Eds.), Fields virology (pp. 799-840). New York: Lippincott Williams & Wilkins.
Hollinger, F. B., & Martin, A. (2013). Hepatitis a virus. In W. Kluwer (Ed.), Field’s virology (pp. 550-581). Philadelphia: Lippincott Williams & Wilkins.
Horney, B., Kammerer, R., Moubayed, P., Frings, W., Gauss-muller, V., & Dotzauer, A. (2001). Experimental hepatitis A virus infections in Guinea Pigs. Journal of Medical Virology, 64(4), 402-409. doi: 10.1002/jmv.1065
International Committee on Taxonomy of Viruses (2018). Taxonomy of viruses. Retrieved from https://talk. ictvonline.org/
Jacobsen, K. H., & Wiersma, S. T. (2010). Hepatitis A virus seroprevalence by age and world region, 1990 and 2005. Vaccine, 28(41), 6653-6657. doi: 10.1016/j.vaccine.2010.08.037
Jones, K. E., Patel, N. G., Levy, M. A., Storeygard, A., Balk, D., Gittleman, J. L., & Daszak, P. (2008). Global trends in emerging infectious diseases. Nature, 451(21), 990-993. doi: 10.1038/nature06536
Koff, R. D. (1992). Clinical manifestations and diagnosis of hepatitis A vírus infection. Vaccine, 10(1), 15-17. doi: 10.1016/0264-410X(92)90533-P
Koff, R. S. (1998). Hepatitis A. Lancet, 351(1), 1643-1649. doi: 10.1016/S0140-6736(98)01304-X
Lanford, R. E., Walker, C. M., & Lemon, S. M. (2019). Nonhuman primate models of Hepatitis A virus and Hepatitis E virus infections. Cold Spring Harb Perspect Medicine, 9(2), 1-29. doi: 10.1101/cshperspect. a031815 .
Leão, R. N. Q., Bichara, C. N. C., Fraiha, N., Neto, & Vasconcelos, P. F. C. (2013). Medicina Tropical e infectologia na Amazônia (pp. 685-740). Brasil: Samauma.
Leduc, J. W., Lemon, S. M., Keenan, C. M., Graham, R. R., Marchwicki, R. H., & Binn, L. H. (1983). Experimental infection of the new world owl monkey (Aotus trivirgatus) with hepatitis A virus. Infection and Immunity, 40(2), 766-772. doi: 10.1128/IAI.40.2.766-772.1983
Lemon, S. M., Leduc, J. W., Binn, L. N., Escajadillo, A., & Ishak, K. G. (1982). Transmission of hepatitis A vírus among recently captured Panamian owl monkeys. Journal of Medical Virology, 10, 25-36. doi: 10. 1002/jmv.1890100105
Lewisohn, T. M., & Prado, P. I. (2002). Biodiversity of Brazil: a synthesis of the current state of knowledge. São Paulo: Contexto Acadêmica.
Nath, B. G., Chakraborty, A., Sarma, D. K., Rahman, T., & Boro, P. K. (2013). Seroprevalence of Hepatitis A virus infection in non-human primates in Assam, Indian. Journal of Threatened, 5(12), 4722-4724. doi: 10.11609/JoTT.o3121.4722-4
Paula, V. S. de. (2012). Laboratory diagnosis of hepatitis A. Future Virology, 7(5), 461-472. doi: 10.2217/ fvl.1235
Pereira, W. L. A., Galo, K. R., Silva, K. S. M. D., Soares, M. D. C. P., & Alves, M. M. (2010). Viral hepatitis, helminthiasis and protozoan disease in neotropical primates reaised in captivity: potentially zoonotic affections with fecal-oral transmission. Revista Pan Amazônica Saúde, 1(3), 57-60. doi: 10.51 23/S2176-62232010000300008
Reis, N. R., Peracchi, A. L., Fregonezi, M. N., & Rossaneis, B. K. (2010). Mamíferos do Brasil: guia de identificação. São Paulo: Technical Books.
Robertson, B. H. (2001). Viral hepatitis and primates: historical and molecular analysis of human and nonhuman primate hepatitis A, B and GB-related viruses. Journal of Viral Hepatitis, 8(4), 233-242. doi: 10.1046/j.1365-2893.2001.00295.x
San-nguanmoo, P., Thawornsuk, N., Rianthavorn, P., Sommanustweechai, A., Ratanakorn, P., & Poovorawan, Y. (2010). High prevalence of antibodies against hepatitis A virus among captive nonhuman primates. Primates, 51(2), 167-170. doi: 10.1007/s10329-009-0172-z
Setzer, A. P., Gaspar, A. M. C., Sidoni, M., Bueno, M. G., & Catão-Dias, J. L. (2014). Serosurvey for hetatitis A in neotropical primates in southeast Brazil. Journal Medical Primatology, 43(3), 202-205. doi: 10.1111/jmp.12106.
Seymor, I. J., Appletton, H. (2001). Foodborne viruses and fresh produce. Journal of Applied Microbiology, 91(5), 759-773. doi: 10.1111/jmp.12106
Soares, M. C. P., Bensabath, G., & Travassos Da Rosa, A. P. A. (1987). Presença de anticorpos para vírus da hepatite A em Didelphis marsupialis (Vertebrata, Marsupialia) da Amazônia. Revista do Instituto de Medicina Tropical, 29(2), 110-111. doi: 10.1590/S0036-46651987000200008
Svoboda, W. K., Soares, M. C. P., Alves, M. M., Rocha, T. C., Gomes, E. C., Menonci, F.,... Navarro, I. T. (2016). Serological detection of hepatitis A virus in free-ranging neotropical primates (Sapajus spp., Aluatta caraya) from the Paraná river basin, Brasil. Revista do Instistituto de Medicina Tropical, 58(9), 1-6. doi: 10.1590/S1678-994658009
Vaughan, G., Rossi, L. M. G., Forbi, J. C., Paula, V. S. de, Purdy, M. A., Xia, G., & Khudyakov, Y. E. (2014). Hepatitis A virus: host interactions, molecular epidemiology and evolution. Infection, Genetics and Evolution, 21(4), 227-243. doi: 10.1016/j.meegid.2013.10.023
Wang, W. L., Li, B., Zhang, W., Zhu, Y., Shi, Z. L., & Yang, X. L. (2018). Genomic characterization of novel hepatovirus from great roundleaf bats in China. Virologica Sinica, 33(1), 108-110. doi: 10.1007/s 12250-018-0013-6
Wang, X., Ren, J., Gao, Q., Hu, Z., Sun, Y., Li, X.,… Fry, E. E. (2015). Hepatitis A virus and the origins of picornaviruses. Nature, 517(1), 85-88. doi: 10.1038/nature13806
Yahner, R. H. (1992). Dynamics of small mammal community in a fragment forest. American Midland Naturalist, 127(2), 381-391. doi: 10.2307/2426545
Yu, J., Li, L., Zhang, C., Lu, S., Ao, Y., Gao, H.,… Duan, Z. J. (2016). A novel hepatovirus identified in wild woodchuck Marmota himalayana. Scientific reports. Nature, 6(1), 1-11. doi: 10.1038/srep22361
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2021-04-22
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Bernal, M. K. M., Souza, A. J. S. de, Nunes, H. M., Malheiros, A. P., Chagas, A. A. C. das, Andrade, S. L. dos S., … Pereira, W. L. A. (2021). Serological markers for hepatitis a among captive and free-living wild mammals in the State of Pará, Brazil. Semina: Ciências Agrárias, 42(3Supl1), 1635–1646. https://doi.org/10.5433/1679-0359.2021v42n3Supl1p1635
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