Evidence of hepatitis E virus in milk and feces from rural cattle farms in Mazandaran province, Iran

Document Type : Original Article

Authors

1 Department of Food Hygiene, Faculty of Veterinary Medicine, Amol University of Special Modern Technologies, Amol, Iran

2 Department of Pathobiology, Faculty of Veterinary Medicine, Amol University of Special Modern Technologies, Amol, Iran

3 Preventive Veterinary Medicine Graduate Group, School of Veterinary Medicine, University of California, Davis, USA

Abstract
Hepatitis E virus (HEV) is a zoonotic pathogen that can cause acute viral hepatitis in both humans and animals. Some animals, such as swine, rabbits, cattle, and sheep are recognized as primary reservoirs of HEV. Recently, HEV has emerged as a significant public health concern in both industrialized and developing countries. Up to now, there is no information about zoonotic sources and prevalence of HEV in wild and domestic animals in Iran. This cross-sectional study aims to determine the prevalence of HEV. Multi-stage cluster sampling approach was used to collect 400 fecal swabs and 400 milk samples between September and February 2022. These samples were collected from rural cattle dairy farms in northern Iran. The viral genome was extracted, and semi-nested reverse transcription polymerase chain reaction was used to detect the HEV RNA genome. The overall estimated herd-level prevalence of HEV was found to be 6.25% (5/80, 95.00% CI: 2.06 - 13.99%). Among the 400 fecal and 400 milk samples obtained from 80 farms, the prevalence of HEV was 3.75% (3/80, 95.00% CI: 0.78 -10.57%), and 2.50% (2/80, 95.00% CI: 0.80 - 30.74%), respectively. Positive fecal samples were detected in Abbas-abad and Amol cities, while positive milk samples were found in Tonekabon City. Based on our findings, Hepatitis E is present in the cattle population of Mazandaran province, Iran. Further, more in-depth investigations are recommended due to the zoonotic nature of this disease. It is crucial to consider control and preventive measures in order to mitigate the spread of HEV.

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1.     Hon KLE, Leung AKC, Wong AHC, et al. Hepatitis E virus and zoonosis: recent advances and therapeutic implications. Recent Adv Inflamm Allergy Drug Discov 2023; 17(1): 54-63.
2.     Yin X, Kan F. Hepatitis E virus infection and risk of hepatocellular carcinoma: a systematic review and meta-analysis. Cancer Epidemiol 2023; 87: 102457. doi: 10.1016/j.canep.2023.102457.
3.     Maphumulo SS, Goedhals D, van Rooyen C, et al. High seroprevalence of hepatitis E virus in the Free State province of South Africa. S Afr J Infect Dis 2024; 39(1): 577. doi: 10.4102/sajid.v39i1.577.
4.     Geng J, Wang L, Wang X, et al. Study on prevalence and genotype of hepatitis E virus isolated from Rex Rabbits in Beijing, China. J Viral Hepat 2011; 18(9): 661-667
5.     Santos-Silva S, da Silva Dias Moraes DF, López-López P, et al. Hepatitis E virus in the Iberian Peninsula: a systematic review. Food Environ Virol 2023; 15(3): 193-211.
6.     Krawczynski K. Hepatitis E vaccine- -ready for prime time? N Engl J Med 2007; 356(9): 949-951.
7.     Santos-Silva S, López-López P, Gonçalves HMR, et al. A systematic review and meta-analysis on hepatitis E virus detection in farmed ruminants. Pathogens 2023; 12(4): 550. doi: 10.3390/pathogens12040550.
8.     Dalton HR, Fellows HJ, Stableforth W, et al. The role of hepatitis E virus testing in drug‐induced liver injury. Aliment Pharmacol Ther 2007; 26(10):1429-1435.
9.     Meng XJ. Hepatitis E virus: animal reservoirs and zoonotic risk. Vet Microbiol 2010; 140(3-4): 256-265.
10. Takahashi M, Nishizawa T, Sato H, et al. Analysis of the full-length genome of a hepatitis E virus isolate obtained from a wild boar in Japan that is classifiable into a novel genotype. J Gen Virol 2011; 92(Pt 4): 902-908.
11. Emerson SU, Purcell RH. Hepatitis E virus. Rev Med Virol 2003; 13(3): 145-154.
12. Khuroo MS, Kamili S, Yattoo GN. Hepatitis E virus infection may be transmitted through blood transfusions in an endemic area. J Gastroenterol Hepatol 2004; 19(7): 778-784.
13. Turlewicz-Podbielska H, Augustyniak A, Wojciechowski J, et al. Hepatitis E virus in livestock—update on its epidemiology and risk of infection to humans. Animals (Basel) 2023; 13(20): 3239. doi: 10.3390/ani13203239.
14. Sadeghi F, Golchob Z, Javadian M, et al. Seroprevalence of hepatitis A and hepatitis E viruses among pregnant women in Northern Iran. Infect Dis Obstet Gynecol 2021; 2021: 5130586. doi: 10.1155/2021/5130586.
15. Saade MC, Haddad G, El Hayek M, et al. The burden of hepatitis E virus in the Middle East and North Africa region: a systematic review. J Infect Dev Ctries 2022; 16(5): 737-744.
16. Cancela F, Cravino A, Icasuriaga R, et al. Co-circulation of hepatitis E virus (HEV) genotype 3 and Moose-HEV-like strains in free-ranging-spotted deer (Axis axis) in Uruguay. Food Environ Virol 2023; 15(4): 281-291.
17. Tsachev I, Gospodinova K, Pepovich R, et al. First insight into the seroepidemiology of hepatitis E virus (HEV) in dogs, cats, horses, cattle, sheep, and goats from Bulgaria. Viruses 2023; 15(7): 1594. doi: 10.3390/v15071594.
18. Obaidat MM, Roess AA. Individual animal and herd level seroprevalence and risk factors of hepatitis E in ruminants in Jordan. Infect Genet Evol 2020; 81: 104276. doi: 10.1016/j.meegid.2020.104276.
19. Alighadri M, Musazadeh V, Gholinia B, et al. Effective factors on the amount and type of consumption milk in Ardabil city of Iran: a descriptive study. JNFS 2020; 5(3): 259-265.
20. Shariatifar M, Salavati-Hamedani M, Rezaeian-Doloei R, et al. Antibiotic resistance and enterotoxin gene profiles of Staphylococcus aureus isolated from raw milk in Iran. J Hellenic Vet Med Soc 2023; 74(1): 5433-5440.
21. Sarani A, Ravanbakhsh A, Kamaladini H. First detection of hepatitis E virus in dromedary camels from Iran. Vet Med Sci2023; 9(4): 1812-1817.
22. Go HJ, Park BJ, Ahn HS, et al. Identification of hepatitis E virus in bovine and porcine raw livers. J Microbiol Biotechnol 2019; 29(12): 2022-2025.
23. Salman SK, Teo ALJ. Windmill modeling consideration and factors influencing the stability of a grid-connected wind power based embedded generator. IEEE Trans Power Syst 2003; 18(2): 793-802.
24. Thrusfield MCR, Brown H, Diggle PJ, et al. Veterinary epidemiology. 4th ed. New Jersey, USA: Wiley-Blackwell 2018; 272-280.
25. Geng Y, Zhao C, Huang W, et al. Hepatitis E virus was not detected in feces and milk of cows in Hebei province of China: no evidence for HEV prevalence in cows. Int J Food Microbiol 2019; 291: 5-9.
26. Johne R, Plenge- Bönig A, Hess M, et al. Detection of a novel hepatitis E-like virus in faeces of wild rats using a nested broad-spectrum RT-PCR. J Gen Virol 2010; 91(Pt 3):750-758.
27. Amiri Dehnoyi M, Mokhtari A. Genomic investigation of hepatitis E virus in Persian Gazelle. Jentashapir J Cell Mol Biol 2020; 11(4): e111737. doi: 10.5812/ jjcmb.111737.
28. Kant A, Koch G, Van Roozelaar DJ, et al. Differentiation of virulent and non-virulent strains of Newcastle disease virus within 24 hours by polymerase chain reaction. Avian Pathol 1997; 26(4): 837-849.
29. Demirci M, Yiğin A, Ünlü Ö, et al. Detection of HEV RNA amounts and genotypes in raw milks obtained from different animals [Turkish]. Mikrobiyol Bul 2019; 53(1): 43-52.
30. Sayed IM, Elkhawaga AA, El-Mokhtar MA. Circulation of hepatitis E virus (HEV) and/or HEV-like agent in non-mixed dairy farms could represent a potential source of infection for Egyptian people. Int J Food Microbiol 2020; 317: 108479. doi: 10.1016/ j.ijfoodmicro. 2019.108479.
31. Santos-Silva S, Gonçalves HMR, Rivero-Juarez A, et al. Detection of hepatitis E virus in milk: current evidence for viral excretion in a wide range of mammalian hosts. Transbound Emerg Dis 2022; 69(6): 3173-3180.
32. Huang F, Li Y, Yu W, et al. Excretion of infectious hepatitis E virus into milk in cows imposes high risks of zoonosis. Hepatology 2016; 64(2): 350-359.
33. Bastos C, Eisen AKA, Demoliner M, et al. Hepatitis E virus genotype 3 in bovine livers slaughtered in the state of Rio Grande do Sul, Brazil. Braz J Microbiol 2022; 53(3): 1115-1120.
34. Pavio N, Kooh P, Cadavez V, et al. Risk factors for sporadic hepatitis E infection: a systematic review and meta-analysis. Microb Risk Anal 2021; 17: 100129. doi: 10.1016/j.mran.2020.100129.
35. Movafagh F, Zeinali T, Jamshidi A. Contamination rate of bovine raw milk with Yersinia enterocolitica biotypes in Mashhad, Iran. JHEHP 2021; 7(1): 30-34.
36. Ferri G, Vergara A. Hepatitis E virus in the food of animal origin: a review. Foodborne Pathog Dis. 2021; 18(6):368-77.
37. Tonbak F, Atasever M. Determination of hepatitis E virus in sheep and cattle by serological and molecular methods DNA sequences analysis. Acta Vet Eurasia 2022; 48(2): 94-100.
38. Zahmanova G, Takova K, Tonova V, et al. The re-emergence of hepatitis E virus in Europe and vaccine development. Viruses 2023; 15(7): 1558. doi: 10.3390/v15071558.
39. Al-Shimari FH, Rencken CA, Kirkwood CD, et al. Systematic review of global hepatitis E outbreaks to inform response and coordination initiatives. BMC Public Health 2023; 23: 1120. doi: 10.1186/s12889-023-15792-8.
40. Caballero-Gómez J, García-Bocanegra I, Jiménez-Martín D, et al. Epidemiological survey and risk factors associated with hepatitis E virus in small ruminants in southern Spain. Zoonoses Public Health 2022; 69(4): 387-393.
Volume 16, Issue 9
September 2025
Pages 523-528

  • Receive Date 13 July 2024
  • Revise Date 25 December 2024
  • Accept Date 28 December 2024