Prevalence of Hepatitis E Virus in Patients with Chronic Hepatopathy in a Reference Center of Bahia State, Brazil
Main Article Content
Abstract
Introduction: Hepatitis E virus infection can lead to severe liver disease and unregulated hepatitis in patients with a history of previous chronic liver disease of different etiologies.
Objective: To determine the seroprevalence of hepatitis E in untreated carriers of hepatitis C virus, hepatitis B virus, autoimmune hepatitis and in patients with drug-induced liver disease.
Materials and Methods: This is a cross-sectional study with a total sample of 301 outpatient hepatology volunteers. The detection of anti-HEV IgM and IgG antibodies was determined using the ELISA (RecomWell anti-HEV IgG and IgM, Mikrogen®, Germany), One-step real-time PCR was used for the detection of HEV-RNA (Taqman, Life Technologies TM, Foster City, CA, USA).
Results: The overall prevalence of anti-HEV IgG and IgM in the population studied was 12.95% and 2.3%, respectively. The prevalence by group were: anti-HEV IgG: hepatitis C virus with 13.2%, hepatitis B virus with 13%, autoimmune hepatitis with 8.1 and drug-induced liver disease with 21.1. Patients with HCV chronic hepatitis and positive HCV IgG serology showed an increase in transaminase levels in 66.7% (10/15) of the cases, while in the seronegative patients this increase was present in 42.4% (42/99) of the cases (p<0.05).
Conclusions: A high seroprevalence of HEV was observed. Among the patients with serology concomitantly positive for anti HEV IgG and IgM, 57.1% (4/7) had higher levels of TGO and TGP, suggesting acute HEV infection. A relationship between hepatitis C and E virus co-infection and elevated transaminase levels has been demonstrated. Future studies with evaluation of several clinical parameters are necessary.
Keywords:
Hepatitis E, Hepatitis B, Hepatitis C, Drug-induced liver disease, Autoimmune hepatitis
Article Details
How to Cite
MENEZES, Gisele B L et al.
Prevalence of Hepatitis E Virus in Patients with Chronic Hepatopathy in a Reference Center of Bahia State, Brazil.
Medical Research Archives, [S.l.], v. 11, n. 5, may 2023.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/3773>. Date accessed: 11 may 2024.
doi: https://doi.org/10.18103/mra.v11i5.3773.
Section
Research Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
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4 Hering T, Passos AM, Perez RM, et al. Past and current hepatitis E virus infection in renal transplant patients. J. Med. Virol. 2014; 86:948–953. https://doi.org/10.1002/jmv.23915
5 Passos-Castilho AM, de Sena A, Geraldo A, Spada C, Granato CF. High prevalence of hepatitis E virus antibodies among blood donors in Southern Brazil. J. Med. Virol. 2016; 88:361–364. https://doi.org/10.1002/jmv.24336.
6 Bricks G, Senise JF, Pott H Jr, et al. Seroprevalence of hepatitis E virus in chronic hepatitis C in Brazil. Braz J Infect Dis, 2018; 22:85-91. https://doi.org/10.1016/j.bjid.2018.02.001
7 Bricks G, Senise JF, Pott-Jr H, et al. Previous hepatitis E virus infection, cirrhosis and insulin resistance in patients with chronic hepatitis C. Braz. J. Infect. Dis. 2019; 23:45–52. https://doi.org/10.1016/j.bjid.2019.02.002
8 Castro VOL, Tejada-Strop A, Weis SMS, et al. Evidence of hepatitis E virus infections among persons who use crack cocaine from the Midwest region of Brazil. J. Med. Virol. 2019; 91:151–154. https://doi.org/10.1002/jmv.25288
9 Kumar AS, Kumar SP, Singh R, et al. Hepatitis E virus (HEV) infection in patients with cirrhosis is associated with rapid decompensation and death. J Hepatol, 2007; 46:387-394. https://doi.org/10.1016/j.jhep.2006.09.016
10 Vento S. Fulminant hepatitis associated with hepatitis A virus superinfection in patients with chronic hepatitis C. J Viral Hepat.2000; 7:7-8. https://doi.org/10.1046/j.1365-2893.2000.00019.x
11 Sagnelli NE e Coppola V M, et al. HBV superinfection in hepatitis C virus chronic carriers, viral interaction, and clinical course. Hepatology, 2002; 36:1285-1291. https://doi.org/10.1053/jhep.2002.36509
12 Costa MB, Gouvêa MSG, Chuffi S, et al. Seroprevalence of hepatitis E virus in risk populations and blood donors in a referral hospital in the south of Brazil. Sci Rep. 2021; 16:6011. https://doi.org/10.1038/s41598-021-85365-5
13 Hardtke S, Rocco R, Ogata J, et al. Risk factors and seroprevalence of hepatitis E evaluated in frozen-serum samples (2002–2003) of pregnant women compared with female blood donors in a Southern region of Brazil. J. Med. Virol. 2018; 90:1856–1862. https://doi.org/10.1002/jmv.25274
14 Kiesslich D, Rocha JE Jr e Crispim MA. Prevalence of hepatitis E virus antibodies among different groups in the Amazonian basin. Transactions of the Royal Society of Tropical Medicine and hygiene. 2002; 96:215 https://doi.org/10.1016/S0035-9203(02)90311-1
15 Purdy MA, Khudyakov YE. The molecular epidemiology of hepatitis E virus infection. Virus Res. 2011;161:319. https://doi.org/10.1016/j.virusres.2011.04.030
16 Pischke S, Behrendt P, Bock CT, Jilg W, Manns MP, Wedemeyer H. Hepatitis E in Germany--an under-reported infectious disease. Dtsch Arztebl Int. 2014; 111: 577-83. https://doi.org/10.3238/arztebl.2014.0577
17 Kaene F, Gompels M, Bendall R, et al. Hepatitis E virus coinfection in patients with HIV infection. HIV Med. 2012; 13:83-8. https://doi.org/10.1111/j.1468-1293.2011.00942.x
18 Junge N, Pischke S, Baumann U, Goldschmidt I, Manns M, Wedemeyer H, et al. Results of single-center screening for chronic hepatitis e in children after liver transplantation and report on successful treatment with ribavirin. Pediatr Transplant. 2013; 17:343–7. https://doi.org/10.1111/petr.12077
19 De Niet A, Zaaijer HL, Ten Berge I, Weegink CJ, Reesink HW, Beuers U. Chronic hepatitis E after solid organ transplantation. Neth J Med. 2012; 70:261–6. PMID: 22859417.
20 Calisti G, Irish D, Ijaz S, Tedder R, Moore K. Acute hepatitis E mimicking a flare of disease in a patient with chronic autoimmune hepatitis. Ann Hepatol. 2017; 16:160163. https://doi.org/10.5604/16652681.1226952
21 Jothikumar N, Cromeans TL, Robertson BH, Meng XJ, Hill VR. A broadly reactive one-step real-time RT-PCR assay for rapid and sensitive detection of hepatitis E virus. J Virol Methods. 2006; 131:65-71. https://doi.org/10.1016/j.jviromet.2005.07.004
22 de Moraes ACP, Gouvea MG, Ferreira AC, et al. The impact of hepatitis E infection on hepatic fibrosis in liver transplanted patients for hepatitis C infection. Braz J Infect Dis. 2021; 25(3):101587. https://doi.org/10.1016/j.bjid.2021.101587
23 Tengan FM, Figueiredo GM, Nunes AKS, et al. Seroprevalence of hepatitis E in adults in Brazil: a systematic review and meta-analysis. Infect Dis Poverty.2019; 8:3. https://doi.org/10.1186/s40249-018-0514-4
24 Trinta KS, Liberto MI, de Paula VS, Yoshida CF, Gaspar AM. Hepatitis E virus infection in selected Brazilian populations. Mem Inst Oswaldo Cruz. 2001; 96:25–9. https://doi.org/10.1590/s0074-02762001000100004
25 Parana R, Cotrim HP, Cortey-Boennec ML, Trepo C, Lyra L. Prevalence of hepatitis E virus IgG antibodies in patients from a referral unit of liver diseases in Salvador, Bahia, Brazil. Am J Trop Med Hyg. 1997; 57:60–1. https://doi.org/10.4269/ajtmh.1997.57.60
26 Ferreira AC, Gomes-Gouvea MS, Lisboa-Neto G, et al. Serological and molecular markers of hepatitis E virus infection in HIV-infected patients in Brazil. Arch Virol. 2018; 163:43–9. https://doi.org/10.1007/s00705-017-3562-3
27 de Oliveira J, Freitas NR, Teles SA, et al. Prevalence of hepatitis E virus RNA and antibodies in a cohort of kidney transplant recipients in Central Brazil. Int J Infect Dis. 2018; 69:41–3. https://doi.org/10.1016/j.ijid.2018.01.032
28 Bortoliero AL, Bonametti AM, Morimoto HK, Matsuo T, Reiche EM. Seroprevalence for hepatitis E virus (HEV) infection among volunteer blood donors of the Regional Blood Bank of Londrina, State of Paraná, Brazil. Rev Inst Med Trop Sao Paulo. 2006; 48:87-92. https://doi.org/10.1590/S0036-46652006000200006.
29 Passos-Castilho, A M, Reinaldo, M R, Sena, A G, Celso F.H. High prevalence of hepatitis E virus antibodies in Sao Paulo, Southeastern Brazil: analysis of a group of blood donors representative of the general population. The Brazilian Journal of Infectious Diseases. 2017; 21:535-539 https://doi.org/10.1016/j.bjid.2017.05.004
30 Bezerra LA, de Oliveira-Filho EF, Silva JVJ Jr, Santos Morais VM, Gonçales JP, da Silva DM, Duarte Coêlho MRC. Risk analysis and seroprevalence of HEV in people living with HIV/AIDS in Brazil. Acta Trop. 2019; 189:65-68. https://doi.org/10.1016/j.actatropica.2018.09.026
31 Santos DC, Souto FJ, Santos DR, Vitral CL, Gaspar AM. Seroepidemiological markers of enterically transmitted viral hepatitis A and E in individuals living in a community located in the North Area of Rio de Janeiro, RJ, Brazil. Mem Inst Oswaldo Cruz. 2002; 97:637-40. https://doi.org/10.1590/S0074-02762002000500007
32 Passos-Castilho AM, de Sena A, Reinaldo MR, Granato CF. Hepatitis E virus infection in Brazil: results of laboratory-based surveillance from 1998 to 2013. Rev Soc Bras Med Trop. 2015; 48:468-70. https://doi.org/10.1590/0037-8682-0036-2015
33 Vitral CL, da Silva-Nunes M, Pinto MA, et al. Hepatitis A and E seroprevalence and associated risk factors: a community-based cross-sectional survey in rural Amazonia. BMC Infect Dis. 2014; 14:458. https://doi.org/10.1186/1471-2334-14-458
34 Huang S, Zhang X, Jiang H, et al. Profile of acute infectious markers in sporadic hepatitis E. PLoS One. 2010; 5:13560. https://doi.org/10.1371/journal.pone.0013560.
35 Aggarwal R. Diagnosis of hepatitis E. Nat Rev Gastroenterol Hepatol. 2013;10:24-33. https://doi.org/10.1038/nrgastro.2012.187.
36 Dalton HR, Kamar N, Baylis SA, Moradpour D, Wedemeyer H, Negro F. EASL Clinical practice guidelines on hepatitis E virus infection. J Hepatol. 2018; 68:1256-71. https://doi.org/10.1016/j.jhep.2018.03.005
37 Elhendawy M, Abo-Ali L, Abd-Elsalam S, et al. HCV and HEV: two players in an Egyptian village, a study of prevalence, incidence, and co-infection. Environ Sci Pollut Res Int. 2020; 27:33659-33667. https://doi.org/10.1007/s11356-020-09591-6.
38 Bayram A, Eksi F, Mehli M, Sözen E. Prevalence of hepatitis E virus antibodies in patients with chronic hepatitis B and chronic hepatitis C. Intervirology. 2007; 50:281-6. https://doi.org/10.1159/000103916.
39 Payne BA, Medhi M, Ijaz S, et al. Hepatitis E virus seroprevalence among men who have sex with men, United Kingdom. Emerg Infect Dis. 2013; 19:333-5. https://doi.org/10.3201/eid1902.121174.
40 Colson P, Borentain P, Queyriaux B, et al. Pig liver sausage as a source of hepatitis E virus transmission to humans. The Journal of Infectious Diseases.2010; 202:825–834. https://doi.org/10.1086/655898
41 Legrand-Abravanel F, Kamar N, Sandres-Saune K, et al. Characteristics of autochthonous hepatitis E virus infection in solid-organ transplant recipients in France. The Journal of infectious diseases. 2010; 202:835–844. https://doi.org/10.1086/655899
42 Arnaboldi S, Righi F, Carta V, et al. Hepatitis E Virus (HEV) Spread and Genetic Diversity in Game Animals in Northern Italy. Food Environ Virol. 2021; 13:146-153. https://doi.org/10.1007/s12560-021-09467-z.
43 Abravanel F, Lhomme S, El Costa H, et al. Rabbit hepatitis E virus infections in humans, France. Emerging Infectious Diseases.2017; 23:1191–1193. https://doi.org/10.3201/eid2307.170318
44 Arankalle VA, Chadha MS, & Chobe LP. Long-term serological follow up and cross-challenge studies in rhesus monkeys experimentally infected with hepatitis E virus. Journal of Hepatology, 1999; 30:199–204. https://doi.org/10.1016/S0168-8278(99)80062-2
45 Kukielka D, Rodriguez-Prieto V, Vicente J, & Sánchez-Vizcaíno J. Constant hepatitis E virus (HEV) circulation in wild boar and red deer in Spain: an increasing concern source of HEV zoonotic transmission. Transboundary and Emerging Diseases. 2016; 63:360–368. https://doi.org/10.1111/tbed.12311.
46 Treagus S, Wright C, Baker-Austin C, Longdon B, Lowther J. The Foodborne Transmission of Hepatitis E Virus to Humans. Food Environ Virol. 2021; 13:127-145. https://doi.org/10.1007/s12560-021-09461-5
47 Kamar N, Izopet J, Pavio N, et al. Hepatitis E virus infection. Nat Rev Dis Primers. 2017; 16:17086. https://doi.org/10.1128/CMR.00057-13
2 World Health Organization Global Hepatitis Report,
http://www.who.int/mediacentre/factsheets/fs280/en ; 2017 [accessed 06 Dec 2021].
3 Souza AJS, Oliveira CMA, Sarmento VP, et al. Hepatitis E virus infection among rural Afro-descendant communities from the eastern Brazilian Amazon. Rev Soc Bras Med Trop. 2018; 51:803-807. https://doi.org/10.1590/0037-8682-0394-2017
4 Hering T, Passos AM, Perez RM, et al. Past and current hepatitis E virus infection in renal transplant patients. J. Med. Virol. 2014; 86:948–953. https://doi.org/10.1002/jmv.23915
5 Passos-Castilho AM, de Sena A, Geraldo A, Spada C, Granato CF. High prevalence of hepatitis E virus antibodies among blood donors in Southern Brazil. J. Med. Virol. 2016; 88:361–364. https://doi.org/10.1002/jmv.24336.
6 Bricks G, Senise JF, Pott H Jr, et al. Seroprevalence of hepatitis E virus in chronic hepatitis C in Brazil. Braz J Infect Dis, 2018; 22:85-91. https://doi.org/10.1016/j.bjid.2018.02.001
7 Bricks G, Senise JF, Pott-Jr H, et al. Previous hepatitis E virus infection, cirrhosis and insulin resistance in patients with chronic hepatitis C. Braz. J. Infect. Dis. 2019; 23:45–52. https://doi.org/10.1016/j.bjid.2019.02.002
8 Castro VOL, Tejada-Strop A, Weis SMS, et al. Evidence of hepatitis E virus infections among persons who use crack cocaine from the Midwest region of Brazil. J. Med. Virol. 2019; 91:151–154. https://doi.org/10.1002/jmv.25288
9 Kumar AS, Kumar SP, Singh R, et al. Hepatitis E virus (HEV) infection in patients with cirrhosis is associated with rapid decompensation and death. J Hepatol, 2007; 46:387-394. https://doi.org/10.1016/j.jhep.2006.09.016
10 Vento S. Fulminant hepatitis associated with hepatitis A virus superinfection in patients with chronic hepatitis C. J Viral Hepat.2000; 7:7-8. https://doi.org/10.1046/j.1365-2893.2000.00019.x
11 Sagnelli NE e Coppola V M, et al. HBV superinfection in hepatitis C virus chronic carriers, viral interaction, and clinical course. Hepatology, 2002; 36:1285-1291. https://doi.org/10.1053/jhep.2002.36509
12 Costa MB, Gouvêa MSG, Chuffi S, et al. Seroprevalence of hepatitis E virus in risk populations and blood donors in a referral hospital in the south of Brazil. Sci Rep. 2021; 16:6011. https://doi.org/10.1038/s41598-021-85365-5
13 Hardtke S, Rocco R, Ogata J, et al. Risk factors and seroprevalence of hepatitis E evaluated in frozen-serum samples (2002–2003) of pregnant women compared with female blood donors in a Southern region of Brazil. J. Med. Virol. 2018; 90:1856–1862. https://doi.org/10.1002/jmv.25274
14 Kiesslich D, Rocha JE Jr e Crispim MA. Prevalence of hepatitis E virus antibodies among different groups in the Amazonian basin. Transactions of the Royal Society of Tropical Medicine and hygiene. 2002; 96:215 https://doi.org/10.1016/S0035-9203(02)90311-1
15 Purdy MA, Khudyakov YE. The molecular epidemiology of hepatitis E virus infection. Virus Res. 2011;161:319. https://doi.org/10.1016/j.virusres.2011.04.030
16 Pischke S, Behrendt P, Bock CT, Jilg W, Manns MP, Wedemeyer H. Hepatitis E in Germany--an under-reported infectious disease. Dtsch Arztebl Int. 2014; 111: 577-83. https://doi.org/10.3238/arztebl.2014.0577
17 Kaene F, Gompels M, Bendall R, et al. Hepatitis E virus coinfection in patients with HIV infection. HIV Med. 2012; 13:83-8. https://doi.org/10.1111/j.1468-1293.2011.00942.x
18 Junge N, Pischke S, Baumann U, Goldschmidt I, Manns M, Wedemeyer H, et al. Results of single-center screening for chronic hepatitis e in children after liver transplantation and report on successful treatment with ribavirin. Pediatr Transplant. 2013; 17:343–7. https://doi.org/10.1111/petr.12077
19 De Niet A, Zaaijer HL, Ten Berge I, Weegink CJ, Reesink HW, Beuers U. Chronic hepatitis E after solid organ transplantation. Neth J Med. 2012; 70:261–6. PMID: 22859417.
20 Calisti G, Irish D, Ijaz S, Tedder R, Moore K. Acute hepatitis E mimicking a flare of disease in a patient with chronic autoimmune hepatitis. Ann Hepatol. 2017; 16:160163. https://doi.org/10.5604/16652681.1226952
21 Jothikumar N, Cromeans TL, Robertson BH, Meng XJ, Hill VR. A broadly reactive one-step real-time RT-PCR assay for rapid and sensitive detection of hepatitis E virus. J Virol Methods. 2006; 131:65-71. https://doi.org/10.1016/j.jviromet.2005.07.004
22 de Moraes ACP, Gouvea MG, Ferreira AC, et al. The impact of hepatitis E infection on hepatic fibrosis in liver transplanted patients for hepatitis C infection. Braz J Infect Dis. 2021; 25(3):101587. https://doi.org/10.1016/j.bjid.2021.101587
23 Tengan FM, Figueiredo GM, Nunes AKS, et al. Seroprevalence of hepatitis E in adults in Brazil: a systematic review and meta-analysis. Infect Dis Poverty.2019; 8:3. https://doi.org/10.1186/s40249-018-0514-4
24 Trinta KS, Liberto MI, de Paula VS, Yoshida CF, Gaspar AM. Hepatitis E virus infection in selected Brazilian populations. Mem Inst Oswaldo Cruz. 2001; 96:25–9. https://doi.org/10.1590/s0074-02762001000100004
25 Parana R, Cotrim HP, Cortey-Boennec ML, Trepo C, Lyra L. Prevalence of hepatitis E virus IgG antibodies in patients from a referral unit of liver diseases in Salvador, Bahia, Brazil. Am J Trop Med Hyg. 1997; 57:60–1. https://doi.org/10.4269/ajtmh.1997.57.60
26 Ferreira AC, Gomes-Gouvea MS, Lisboa-Neto G, et al. Serological and molecular markers of hepatitis E virus infection in HIV-infected patients in Brazil. Arch Virol. 2018; 163:43–9. https://doi.org/10.1007/s00705-017-3562-3
27 de Oliveira J, Freitas NR, Teles SA, et al. Prevalence of hepatitis E virus RNA and antibodies in a cohort of kidney transplant recipients in Central Brazil. Int J Infect Dis. 2018; 69:41–3. https://doi.org/10.1016/j.ijid.2018.01.032
28 Bortoliero AL, Bonametti AM, Morimoto HK, Matsuo T, Reiche EM. Seroprevalence for hepatitis E virus (HEV) infection among volunteer blood donors of the Regional Blood Bank of Londrina, State of Paraná, Brazil. Rev Inst Med Trop Sao Paulo. 2006; 48:87-92. https://doi.org/10.1590/S0036-46652006000200006.
29 Passos-Castilho, A M, Reinaldo, M R, Sena, A G, Celso F.H. High prevalence of hepatitis E virus antibodies in Sao Paulo, Southeastern Brazil: analysis of a group of blood donors representative of the general population. The Brazilian Journal of Infectious Diseases. 2017; 21:535-539 https://doi.org/10.1016/j.bjid.2017.05.004
30 Bezerra LA, de Oliveira-Filho EF, Silva JVJ Jr, Santos Morais VM, Gonçales JP, da Silva DM, Duarte Coêlho MRC. Risk analysis and seroprevalence of HEV in people living with HIV/AIDS in Brazil. Acta Trop. 2019; 189:65-68. https://doi.org/10.1016/j.actatropica.2018.09.026
31 Santos DC, Souto FJ, Santos DR, Vitral CL, Gaspar AM. Seroepidemiological markers of enterically transmitted viral hepatitis A and E in individuals living in a community located in the North Area of Rio de Janeiro, RJ, Brazil. Mem Inst Oswaldo Cruz. 2002; 97:637-40. https://doi.org/10.1590/S0074-02762002000500007
32 Passos-Castilho AM, de Sena A, Reinaldo MR, Granato CF. Hepatitis E virus infection in Brazil: results of laboratory-based surveillance from 1998 to 2013. Rev Soc Bras Med Trop. 2015; 48:468-70. https://doi.org/10.1590/0037-8682-0036-2015
33 Vitral CL, da Silva-Nunes M, Pinto MA, et al. Hepatitis A and E seroprevalence and associated risk factors: a community-based cross-sectional survey in rural Amazonia. BMC Infect Dis. 2014; 14:458. https://doi.org/10.1186/1471-2334-14-458
34 Huang S, Zhang X, Jiang H, et al. Profile of acute infectious markers in sporadic hepatitis E. PLoS One. 2010; 5:13560. https://doi.org/10.1371/journal.pone.0013560.
35 Aggarwal R. Diagnosis of hepatitis E. Nat Rev Gastroenterol Hepatol. 2013;10:24-33. https://doi.org/10.1038/nrgastro.2012.187.
36 Dalton HR, Kamar N, Baylis SA, Moradpour D, Wedemeyer H, Negro F. EASL Clinical practice guidelines on hepatitis E virus infection. J Hepatol. 2018; 68:1256-71. https://doi.org/10.1016/j.jhep.2018.03.005
37 Elhendawy M, Abo-Ali L, Abd-Elsalam S, et al. HCV and HEV: two players in an Egyptian village, a study of prevalence, incidence, and co-infection. Environ Sci Pollut Res Int. 2020; 27:33659-33667. https://doi.org/10.1007/s11356-020-09591-6.
38 Bayram A, Eksi F, Mehli M, Sözen E. Prevalence of hepatitis E virus antibodies in patients with chronic hepatitis B and chronic hepatitis C. Intervirology. 2007; 50:281-6. https://doi.org/10.1159/000103916.
39 Payne BA, Medhi M, Ijaz S, et al. Hepatitis E virus seroprevalence among men who have sex with men, United Kingdom. Emerg Infect Dis. 2013; 19:333-5. https://doi.org/10.3201/eid1902.121174.
40 Colson P, Borentain P, Queyriaux B, et al. Pig liver sausage as a source of hepatitis E virus transmission to humans. The Journal of Infectious Diseases.2010; 202:825–834. https://doi.org/10.1086/655898
41 Legrand-Abravanel F, Kamar N, Sandres-Saune K, et al. Characteristics of autochthonous hepatitis E virus infection in solid-organ transplant recipients in France. The Journal of infectious diseases. 2010; 202:835–844. https://doi.org/10.1086/655899
42 Arnaboldi S, Righi F, Carta V, et al. Hepatitis E Virus (HEV) Spread and Genetic Diversity in Game Animals in Northern Italy. Food Environ Virol. 2021; 13:146-153. https://doi.org/10.1007/s12560-021-09467-z.
43 Abravanel F, Lhomme S, El Costa H, et al. Rabbit hepatitis E virus infections in humans, France. Emerging Infectious Diseases.2017; 23:1191–1193. https://doi.org/10.3201/eid2307.170318
44 Arankalle VA, Chadha MS, & Chobe LP. Long-term serological follow up and cross-challenge studies in rhesus monkeys experimentally infected with hepatitis E virus. Journal of Hepatology, 1999; 30:199–204. https://doi.org/10.1016/S0168-8278(99)80062-2
45 Kukielka D, Rodriguez-Prieto V, Vicente J, & Sánchez-Vizcaíno J. Constant hepatitis E virus (HEV) circulation in wild boar and red deer in Spain: an increasing concern source of HEV zoonotic transmission. Transboundary and Emerging Diseases. 2016; 63:360–368. https://doi.org/10.1111/tbed.12311.
46 Treagus S, Wright C, Baker-Austin C, Longdon B, Lowther J. The Foodborne Transmission of Hepatitis E Virus to Humans. Food Environ Virol. 2021; 13:127-145. https://doi.org/10.1007/s12560-021-09461-5
47 Kamar N, Izopet J, Pavio N, et al. Hepatitis E virus infection. Nat Rev Dis Primers. 2017; 16:17086. https://doi.org/10.1128/CMR.00057-13