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First Seroepidemiological Investigation of Hepatitis E Virus Infection in Backyard Pigs from Northeastern India: Prevalence and Associated Risk Factors

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Abstract

Hepatitis E virus (HEV) is the leading cause of acute viral hepatitis globally, with zoonotic potential, and pigs are considered the major reservoir. To determine the seroprevalence of HEV infection in pigs reared in backyard conditions in the northeastern region of India, blood samples were collected from 400 pigs from five northeastern states (80 samples from each state) and tested for IgG antibodies against HEV using an ELISA assay. Questionnaires on farm characteristics and management practices were completed, and risk factors associated with HEV were studied using univariate and multivariate analysis. The apparent seroprevalence of HEV infection was 51% (46.1–55.9, 95% CI), with a true prevalence of 52.98% (47.22–58.75, 95% CI). The risk factors significantly associated with higher HEV seropositivity were as follows: lack of disinfection (OR 4.65), feeding swill (restaurant and bakery waste) (OR 2.55), failure to follow the all-in-all-out production system (OR 3.47), and medium holding size (OR 9.83), which refers to mixed rearing of younger and older age groups. This study demonstrates that HEV is widespread among pigs reared in northeastern India. The risk factor analysis conducted in this study provides valuable insights into the prevalence of HEV in the region.

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References

  • Alkali, B. R., Bello, M. B., Hussaini, S., & Onwuliri, C. O. (2015). Serological evidence and public health implication of Hepatitis E virus infection in pigs found in Zaria, Kaduna State. African Journal of Microbiology Research, 9, 2270–2274.

    Article  Google Scholar 

  • Arankalle, V. A., Joshi, M. V., Kulkarni, A. M., Gandhe, S. S., Chobe, L. P., Rautmare, S. S., Mishra, A. C., & Padbidri, V. S. (2001). Prevalence of anti-hepatitis E virus antibodies in different Indian animal species. Journal of Viral Hepatitis, 8, 223–227.

    Article  CAS  PubMed  Google Scholar 

  • Bansal, M., Kaur, S., Deka, D., Singh, R., & Gill, J. P. S. (2017). Seroepidemiology and molecular characterization of hepatitis E virus infection in swine and occupationally exposed workers in Punjab, India. Zoonoses and Public Health, 64(8), 662–672.

    Article  CAS  PubMed  Google Scholar 

  • Bouwknegt, M., Rutjes, S. A., Reusken, C. B., StockhofeZurwieden, N., Frankena, K., de Jong, M. C., de Roda Husman, A. M., & Poel, W. H. (2009). The course of hepatitis E virus infection in pigs after contact-infection and intravenous inoculation. BMC Veterinary Research, 4, 5–7.

    Google Scholar 

  • Chen, Y., Gong, Q. L., Wang, Q., Wang, W., Wei, X. Y., Jiang, J., & Ni, H. B. (2021). Prevalence of hepatitis E virus among swine in China from 2010 to 2019: A systematic review and meta-analysis. Microbial Pathogenesis, 150, 104687.

    Article  CAS  PubMed  Google Scholar 

  • Daniel, W. W. (1999). Biostatistics: A foundation for analysis in the health sciences (7th ed.). Wiley.

    Google Scholar 

  • Ivanova, A., Tefanova, V., Reshetnjak, I., Kuznetsova, T., Geller, J., Lundkvist, Å., Janson, M., Neare, K., Velström, K., Jokelainen, P., Lassen, B., Hütt, P., Saar, T., Viltrop, A., & Golovljova, I. (2015). Hepatitis E virus in domestic pigs, wild boars, pig farm workers, and hunters in Estonia. Food and Environmental Virology, 7(4), 403–412.

    Article  PubMed  Google Scholar 

  • Jinshan, J., Manglai, D., Takahashi, M., Nagashima, S., & Okamoto, H. (2010). Molecular and serological survey of hepatitis E virus infection among domestic pigs in Inner Mongolia, China. Archives of Virology, 155(8), 1217–1226.

    Article  CAS  PubMed  Google Scholar 

  • Krumbholz, A., Joel, S., Neubert, A., Dremsek, P., Dürrwald, R., Johne, R., Hlinak, A., Walther, M., Lange, J., Wutzler, P., Sauerbrei, A., Ulrich, R. G., & Zell, R. (2013). Age-related and regional differences in the prevalence of hepatitis E virus-specific antibodies in pigs in Germany. Veterinary Microbiology, 167(3–4), 394–402.

    Article  CAS  PubMed  Google Scholar 

  • Kumaresan, A., Bujarbaruah, K. M., Pathak, K. A., Das, A., & Bardoloi, R. K. (2009). Integrated resource-driven pig production systems in a mountainous area of Northeast India: Production practices and pig performance. Tropical Animal Health and Production, 41(7), 1187–1196.

    Article  CAS  PubMed  Google Scholar 

  • Li, P., Ji, Y., Li, Y., Ma, Z., & Pan, Q. (2022). Estimating the global prevalence of hepatitis E virus in swine and pork products. One Health, 14, 100362.

    Article  CAS  PubMed  Google Scholar 

  • Li, P., Liu, J., Li, Y., Su, J., Ma, Z., Bramer, W. M., Cao, W., de Man, R. A., Peppelenbosch, M. P., & Pan, Q. (2020). The global epidemiology of hepatitis E virus infection: A systematic review and meta-analysis. Liver International, 40(7), 1516–1528.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lopez-Lopez, P., Risalde, M. L. A., Frias, M., García-Bocanegra, I., Brieva, T., Caballero-Gomez, J., Camacho, A., Fernández-Molera, V., Machuca, I., Gomez-Villamandos, J. C., Rivero, A., & Rivero-Juarez, A. (2018). Risk factors associated with hepatitis E virus in pigs from different production systems. Veterinary Microbiology, 224, 88–92.

    Article  PubMed  Google Scholar 

  • Matsuda, H., Okada, K., Takahashi, K., & Mishiro, S. (2003). Severe hepatitis E virus infection after ingestion of uncooked liver from a wild boar. The Journal of Infectious Diseases, 188(6), 944.

    Article  PubMed  Google Scholar 

  • Milojević, L., Velebit, B., Teodorović, V., Kirbiš, A., Petrović, T., Karabasil, N., & Dimitrijević, M. (2019). Screening and molecular characterization of hepatitis E virus in slaughter pigs in Serbia. Food and Environmental Virology, 11(4), 410–419.

    Article  PubMed  Google Scholar 

  • Naing, L., Winn, T., & Rusli, B. N. (2006). Practical issues in calculating the sample size for prevalence studies. Archives of Orofacial Sciences, 1, 9–14.

    Google Scholar 

  • Pavio, N., Meng, X. J., & Renou, C. (2010). Zoonotic hepatitis E: Animal reservoirs and emerging risks. Veterinary Research, 41, 1–20.

    Article  Google Scholar 

  • Raji, Y. E., Toung, O. P., Taib, N. M., & Sekawi, Z. B. (2022). Hepatitis E Virus: An emerging enigmatic and underestimated pathogen. Saudi Journal of Biological Sciences, 29(1), 499–512.

    Article  CAS  PubMed  Google Scholar 

  • Rogan, W. J., & Gladen, B. (1978). Estimating prevalence from results of a screening-test. American Journal of Epidemiology, 107, 71–76.

    Article  CAS  PubMed  Google Scholar 

  • Rose, N., Lunazzi, A., Dorenlor, V., Merbah, T., Eono, F., Eloit, M., Madec, F., & Pavio, N. (2011). High prevalence of hepatitis E virus in French domestic pigs. Comparative Immunology, Microbiology & Infectious Diseases, 34, 419–427.

    Article  Google Scholar 

  • Rutjes, S. A., Bouwknegt, M., van der Giessen, J. W., de Roda Husman, A. M., & Reusken, C. B. (2014). Seroprevalence of hepatitis E virus in pigs from different farming systems in The Netherlands. Journal of Food Protection, 77, 640–642.

    Article  CAS  PubMed  Google Scholar 

  • Salines, M., Andraud, M., & Rose, N. (2017). From the epidemiology of hepatitis E virus (HEV) within the swine reservoir to public health risk mitigation strategies: A comprehensive review. Veterinary Research, 48(1), 31.

    Article  PubMed  PubMed Central  Google Scholar 

  • Salines, M., Barnaud, E., Andraud, M., Eono, F., Renson, P., Bourry, O., Pavio, N., & Rose, N. (2015). Hepatitis E virus chronic infection of swine co-infected with porcine reproductive and respiratory syndrome virus. Veterinary Research, 46, 55.

    Article  PubMed  PubMed Central  Google Scholar 

  • Shukla, P., Chauhan, U. K., Naik, S., Anderson, D., & Aggarwal, R. (2007). Hepatitis E virus infection among animals in northern India: An unlikely source of human disease. Journal of Viral Hepatitis, 14, 310–317.

    Article  CAS  PubMed  Google Scholar 

  • Smith, D. B., Purdy, M. A., & Simmonds, P. (2013). Genetic variability and the classification of hepatitis E virus. Journal of Virology, 87(8), 4161–4169.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takova, K., Koynarski, T., Minkov, I., Ivanova, Z., Toneva, V., & Zahmanova, G. (2020). Increasing hepatitis E virus seroprevalence in domestic pigs and wild boar in Bulgaria. Animals (Basel), 10(9), 1521.

    Article  PubMed  Google Scholar 

  • Teixeira, J., Mesquita, J. R., Pereira, S. S., Oliveira, R. M., Abreu-Silva, J., Rodrigues, A., Myrmel, M., Stene-Johansen, K., Øverbø, J., Gonçalves, G., & Nascimento, M. S. (2017). Prevalence of hepatitis E virus antibodies in workers occupationally exposed to swine in Portugal. Medical Microbiology and Immunology, 206(1), 77–81.

    Article  CAS  PubMed  Google Scholar 

  • Veronesi, F., Ranucci, D., Branciari, R., Miraglia, D., Mammoli, R., & Fioretti, D. P. (2011). Seroprevalence and risk factors for Toxoplasma gondii infection on finishing swine reared in the Umbria region, central Italy. Zoonoses and Public Health, 58(3), 178–184.

    Article  CAS  PubMed  Google Scholar 

  • Villalobos, N. V. F., Kessel, B., Rodiah, I., Ott, J. J., Lange, B., & Krause, G. (2022). Seroprevalence of hepatitis E virus infection in the Americas: Estimates from a systematic review and meta-analysis. PLoS ONE, 17(6), e0269253.

    Article  Google Scholar 

  • Wacheck, S., Sarno, E., Martlbauer, E., Zweifel, C., & Stephan, R. (2012). Seroprevalence of anti-hepatitis E virus and anti-Salmonella antibodies in pigs at slaughter in Switzerland. Journal of Food Protection, 75, 1483–1485.

    Article  CAS  PubMed  Google Scholar 

  • Xiao, P., Li, R., She, R., Yin, J., Li, W., Mao, J., & Sun, Q. (2012). Prevalence of hepatitis E virus in swine fed on kitchen residue. PLoS ONE, 7, e33480.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The project received funding from the institute (Project Code: IXX18528). We sincerely thank the Director of the institute for providing funding support and necessary facilities.

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Authors and Affiliations

  1. ICAR Research Complex for NEH Region, Umiam, Meghalaya, India

    A. A. P. Milton, Samir Das, S. Ghatak, K. Srinivas, M. Angappan, M. C. B. Prasad, L. Wahlang, Sabia Khan, Blessa Sailo,  Lalhruaipuii, Mahak Singh & A. Sen

  2. College of Agriculture, Central Agricultural University (Imphal), Kyrdemkulai, Meghalaya, India

    G. Bhuvana Priya

  3. Department of Animal Husbandry, Veterinary & Dairy Development, Nirjuli, Arunachal Pradesh, India

    G. B. Garam

Authors
  1. A. A. P. Milton
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  2. Samir Das
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  3. S. Ghatak
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  4. K. Srinivas
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  5. M. Angappan
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  9. Sabia Khan
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  11. Lalhruaipuii
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  14. A. Sen
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Contributions

AAPM: Conceptualization, methodology, investigation, formal analysis, writing—original draft; SD: investigation, writing—review and editing; SG: formal analysis, writing—review and editing; KS: formal analysis; MA: investigation; MCB: investigation; LW: investigation; GBP: formal analysis, writing—original draft; SK: investigation; BS: sample and data collection; L: sample and data collection; MS: sample and data collection; GBG: sample and data collection; AS: writing—review and editing.

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Correspondence to A. A. P. Milton.

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Milton, A.A.P., Das, S., Ghatak, S. et al. First Seroepidemiological Investigation of Hepatitis E Virus Infection in Backyard Pigs from Northeastern India: Prevalence and Associated Risk Factors. Food Environ Virol 15, 307–317 (2023). https://doi.org/10.1007/s12560-023-09564-1

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