1932

Abstract

Hepatitis E virus (HEV) is an important human pathogen that historically has been difficult to study. Limited levels of replication in vitro hindered our understanding of the viral life cycle. Sporadic and low-level virus shedding, lack of standardized detection methods, and subclinical infections made the development of animal models difficult. Better diagnostic techniques and understanding of the virus increased our ability to identify and characterize animal strains and animals that are amenable to model human-relevant infection. These advances are translating into the development of useful HEV animal models so that some of the greatest concerns associated with HEV infection, including host immunology, chronic infection, severe pregnancy mortality, and extrahepatic manifestations, can now be studied. Continued development of these animal models will be instrumental in understanding the many complex questions associated with HEV infection and for assessing therapeutics and prevention strategies to minimize HEV becoming a greater risk to the human population.

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2019-02-15
2024-04-15
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Literature Cited

  1. 1.  Lozano R, Naghavi M, Foreman K, Lim S, Shibuya K et al. 2012. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380:2095–128
    [Google Scholar]
  2. 2.  Rein DB, Stevens GA, Theaker J, Wittenborn JS, Wiersma ST 2012. The global burden of hepatitis E virus genotypes 1 and 2 in 2005. Hepatology 55:988–97
    [Google Scholar]
  3. 3.  Feagins AR, Opriessnig T, Guenette DK, Halbur PG, Meng XJ 2007. Detection and characterization of infectious Hepatitis E virus from commercial pig livers sold in local grocery stores in the USA. J. Gen. Virol. 88:912–17
    [Google Scholar]
  4. 4.  Cossaboom CM, Heffron CL, Cao D, Yugo DM, Houk-Miles AE et al. 2016. Risk factors and sources of foodborne hepatitis E virus infection in the United States. J. Med. Virol. 88:1641–45
    [Google Scholar]
  5. 5.  Huang F, Li Y, Yu W, Jing S, Wang J et al. 2016. Excretion of infectious hepatitis E virus into milk in cows imposes high risks of zoonosis. Hepatology 64:350–59
    [Google Scholar]
  6. 6.  Hartl J, Wehmeyer MH, Pischke S 2016. Acute Hepatitis E: two sides of the same coin. Viruses 8:299
    [Google Scholar]
  7. 7.  Wedemeyer H, Pischke S, Manns MP 2012. Pathogenesis and treatment of hepatitis E virus infection. Gastroenterology 142:1388–97.e1
    [Google Scholar]
  8. 8.  Goel A, Aggarwal R 2016. Advances in hepatitis E—II: epidemiology, clinical manifestations, treatment and prevention. Expert Rev. Gastroenterol. Hepatol. 10:1065–74
    [Google Scholar]
  9. 9.  Kamar N, Abravanel F, Lhomme S, Rostaing L, Izopet J 2015. Hepatitis E virus: chronic infection, extra-hepatic manifestations, and treatment. Clin. Res. Hepatol. Gastroenterol. 39:20–27
    [Google Scholar]
  10. 10.  Kamar N, Izopet J 2014. Does chronic hepatitis E virus infection exist in immunocompetent patients?. Hepatology 60:427
    [Google Scholar]
  11. 11.  Izopet J, Kamar N 2008. Hepatitis E: from zoonotic transmission to chronic infection in immunosuppressed patients. Med. Sci. 24:1023–25
    [Google Scholar]
  12. 12.  de Niet A, Zaaijer HL, ten Berge I, Weegink CJ, Reesink HW, Beuers U 2012. Chronic hepatitis E after solid organ transplantation. Neth. J. Med. 70:261–66
    [Google Scholar]
  13. 13.  Gauss A, Wenzel JJ, Flechtenmacher C, Navid MH, Eisenbach C et al. 2012. Chronic hepatitis E virus infection in a patient with leukemia and elevated transaminases: a case report. J. Med. Case Rep. 6:334
    [Google Scholar]
  14. 14.  Crum-Cianflone NF, Curry J, Drobeniuc J, Weintrob A, Landrum M et al. 2012. Hepatitis E virus infection in HIV-infected persons. Emerg. Infect. Dis. 18:502–6
    [Google Scholar]
  15. 15.  Kamar N, Izopet J, Dalton HR 2013. Chronic hepatitis E virus infection and treatment. J. Clin. Exp. Hepatol. 3:134–40
    [Google Scholar]
  16. 16.  Fujiwara S, Yokokawa Y, Morino K, Hayasaka K, Kawabata M, Shimizu T 2014. Chronic hepatitis E: a review of the literature. J. Viral Hepatol. 21:78–89
    [Google Scholar]
  17. 17.  Peron JM 2016. Hepatitis E virus infection and cirrhosis of the liver. Gastroenterol. Hepatol. 12:565–67
    [Google Scholar]
  18. 18.  Williams TP, Kasorndorkbua C, Halbur PG, Haqshenas G, Guenette DK et al. 2001. Evidence of extrahepatic sites of replication of the hepatitis E virus in a swine model. J. Clin. Microbiol. 39:3040–46
    [Google Scholar]
  19. 19.  Kamar N, Bendall RP, Peron JM, Cintas P, Prudhomme L et al. 2011. Hepatitis E virus and neurologic disorders. Emerg. Infect. Dis. 17:173–79
    [Google Scholar]
  20. 20.  van Tong H, Hoan NX, Wang B, Wedemeyer H, Bock CT, Velavan TP 2016. Hepatitis E virus mutations: functional and clinical relevance. EBioMedicine 11:31–42
    [Google Scholar]
  21. 21.  Kumar A, Beniwal M, Kar P, Sharma JB, Murthy NS 2004. Hepatitis E in pregnancy. Int. J. Gynaecol. Obstet. 85:240–44
    [Google Scholar]
  22. 22.  Chaudhry SA, Verma N, Koren G 2015. Hepatitis E infection during pregnancy. Can. Fam. Physician 61:607–8
    [Google Scholar]
  23. 23.  Patra S, Kumar A, Trivedi SS, Puri M, Sarin SK 2007. Maternal and fetal outcomes in pregnant women with acute hepatitis E virus infection. Ann. Intern. Med. 147:28–33
    [Google Scholar]
  24. 24.  Fiore S, Savasi V 2009. Treatment of viral hepatitis in pregnancy. Expert Opin. Pharmacother. 10:2801–9
    [Google Scholar]
  25. 25.  Cronin S, McNicholas R, Kavanagh E, Reid V, O'Rourke K 2011. Anti-glycolipid GM2-positive Guillain-Barre syndrome due to hepatitis E infection. Ir. J. Med. Sci. 180:255–57
    [Google Scholar]
  26. 26.  Fong F, Illahi M 2009. Neuralgic amyotrophy associated with hepatitis E virus. Clin. Neurol. Neurosurg. 111:193–95
    [Google Scholar]
  27. 27.  Murkey JA, Chew KW, Carlson M, Shannon CL, Sirohi D et al. 2017. Hepatitis E virus-associated meningoencephalitis in a lung transplant recipient diagnosed by clinical metagenomic sequencing. Open Forum. Infect. Dis. 4:ofx121
    [Google Scholar]
  28. 28.  Perrin HB, Cintas P, Abravanel F, Gérolami R, d'Alteroche L et al. 2015. Neurologic disorders in immunocompetent patients with autochthonous acute hepatitis E. Emerg. Infect. Dis. 21:1928–34
    [Google Scholar]
  29. 29.  Dixit VK, Abhilash VB, Kate MP, Jain AK 2006. Hepatitis E infection with Bell's palsy. J. Assoc. Physicians India 54:418
    [Google Scholar]
  30. 30.  Bazerbachi F, Haffar S, Garg SK, Lake JR 2016. Extra-hepatic manifestations associated with hepatitis E virus infection: a comprehensive review of the literature. Gastroenterol. Rep. 4:1–15
    [Google Scholar]
  31. 31.  Woolson KL, Forbes A, Vine L, Beynon L, McElhinney L et al. 2014. Extra-hepatic manifestations of autochthonous hepatitis E infection. Aliment. Pharmacol. Ther. 40:1282–91
    [Google Scholar]
  32. 32.  Kamar N, Marion O, Abravanel F, Izopet J, Dalton HR 2016. Extrahepatic manifestations of hepatitis E virus. Liver Int 36:467–72
    [Google Scholar]
  33. 33.  Smith DB, Simmonds P, Izopet J, Oliveira-Filho EF, Ulrich RG et al. 2016. Proposed reference sequences for hepatitis E virus subtypes. J. Gen. Virol. 97:537–42
    [Google Scholar]
  34. 34.  de Deus N, Casas M, Peralta B, Nofrarias M, Pina S et al. 2008. Hepatitis E virus infection dynamics and organic distribution in naturally infected pigs in a farrow-to-finish farm. Vet. Microbiol. 132:19–28
    [Google Scholar]
  35. 35.  Meng XJ, Purcell RH, Halbur PG, Lehman JR, Webb DM et al. 1997. A novel virus in swine is closely related to the human hepatitis E virus. PNAS 94:9860–65
    [Google Scholar]
  36. 36.  Takahashi K, Kitajima N, Abe N, Mishiro S 2004. Complete or near-complete nucleotide sequences of hepatitis E virus genome recovered from a wild boar, a deer, and four patients who ate the deer. Virology 330:501–5
    [Google Scholar]
  37. 37.  Nakamura M, Takahashi K, Taira K, Taira M, Ohno A et al. 2006. Hepatitis E virus infection in wild mongooses of Okinawa, Japan: demonstration of anti-HEV antibodies and a full-genome nucleotide sequence. Hepatol. Res. 34:137–40
    [Google Scholar]
  38. 38.  Lack JB, Volk K, Van Den Bussche RA 2012. Hepatitis E virus genotype 3 in wild rats, United States. Emerg. Infect. Dis. 18:1268–73
    [Google Scholar]
  39. 39.  Zhao C, Ma Z, Harrison TJ, Feng R, Zhang C et al. 2009. A novel genotype of hepatitis E virus prevalent among farmed rabbits in China. J. Med. Virol. 81:1371–79
    [Google Scholar]
  40. 40.  Meng XJ 2010. Hepatitis E virus: animal reservoirs and zoonotic risk. Vet. Microbiol. 140:256–65
    [Google Scholar]
  41. 41.  Meng XJ 2013. Zoonotic and foodborne transmission of hepatitis E virus. Semin. Liver Dis. 33:41–49
    [Google Scholar]
  42. 42.  Wu J, Si F, Jiang C, Li T, Jin M 2015. Molecular detection of hepatitis E virus in sheep from southern Xinjiang, China. Virus Genes 50:410–17
    [Google Scholar]
  43. 43.  Takahashi M, Nishizawa T, Nagashima S, Jirintai S, Kawakami M et al. 2014. Molecular characterization of a novel hepatitis E virus (HEV) strain obtained from a wild boar in Japan that is highly divergent from the previously recognized HEV strains. Virus Res 180:59–69
    [Google Scholar]
  44. 44.  Takahashi M, Nishizawa T, Sato H, Sato Y, Jirintai et al. 2011. 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. 92:902–8
    [Google Scholar]
  45. 45.  Lee GH, Tan BH, Teo EC, Lim SG, Dan YY et al. 2016. Chronic infection with camelid hepatitis E virus in a liver transplant recipient who regularly consumes camel meat and milk. Gastroenterology 150:355–57.e3
    [Google Scholar]
  46. 46.  Sridhar S, Teng JLL, Chiu TH, Lau SKP, Woo PCY 2017. Hepatitis E virus genotypes and evolution: emergence of camel hepatitis E variants. Int. J. Mol. Sci. 18:869
    [Google Scholar]
  47. 47.  Zhang M, Purcell RH, Emerson SU 2001. Identification of the 5′ terminal sequence of the SAR-55 and MEX-14 strains of hepatitis E virus and confirmation that the genome is capped. J. Med. Virol. 65:293–95
    [Google Scholar]
  48. 48.  Nair VP, Anang S, Subramani C, Madhvi A, Bakshi K et al. 2016. Endoplasmic reticulum stress induced synthesis of a novel viral factor mediates efficient replication of genotype-1 hepatitis E virus. PLOS Pathog 12:e1005521
    [Google Scholar]
  49. 49.  Graff J, Torian U, Nguyen H, Emerson SU 2006. A bicistronic subgenomic mRNA encodes both the ORF2 and ORF3 proteins of hepatitis E virus. J. Virol. 80:5919–26
    [Google Scholar]
  50. 50.  Huang YW, Opriessnig T, Halbur PG, Meng XJ 2007. Initiation at the third in-frame AUG codon of open reading frame 3 of the hepatitis E virus is essential for viral infectivity in vivo. J. Virol. 81:3018–26
    [Google Scholar]
  51. 51.  Agrawal S, Gupta D, Panda SK 2001. The 3′ end of hepatitis E virus (HEV) genome binds specifically to the viral RNA-dependent RNA polymerase (RdRp). Virology 282:87–101
    [Google Scholar]
  52. 52.  Batts W, Yun S, Hedrick R, Winton J 2011. A novel member of the family Hepeviridae from cutthroat trout (Oncorhynchus clarkii). Virus Res 158:116–23
    [Google Scholar]
  53. 53.  Smith DB, Simmonds P, Int. Comm. Taxon. Viruses Hepeviridae Study Group, Jameel S, Emerson SU et al. 2014. Consensus proposals for classification of the family Hepeviridae. J. Gen. Virol. 95:2223–32
    [Google Scholar]
  54. 54.  Sun ZF, Larsen CT, Dunlop A, Huang FF, Pierson FW et al. 2004. Genetic identification of avian hepatitis E virus (HEV) from healthy chicken flocks and characterization of the capsid gene of 14 avian HEV isolates from chickens with hepatitis-splenomegaly syndrome in different geographical regions of the United States. J. Gen. Virol. 85:693–700
    [Google Scholar]
  55. 55.  Zhang X, Bilic I, Troxler S, Hess M 2017. Evidence of genotypes 1 and 3 of avian hepatitis E virus in wild birds. Virus Res 228:75–78
    [Google Scholar]
  56. 56.  Haqshenas G, Shivaprasad HL, Woolcock PR, Read DH, Meng XJ 2001. Genetic identification and characterization of a novel virus related to human hepatitis E virus from chickens with hepatitis-splenomegaly syndrome in the United States. J. Gen. Virol. 82:2449–62
    [Google Scholar]
  57. 57.  Bilic I, Jaskulska B, Basic A, Morrow CJ, Hess M 2009. Sequence analysis and comparison of avian hepatitis E viruses from Australia and Europe indicate the existence of different genotypes. J. Gen. Virol. 90:863–73
    [Google Scholar]
  58. 58.  Reuter G, Boros A, Matics R, Kapusinszky B, Delwart E, Pankovics P 2016. A novel avian-like hepatitis E virus in wild aquatic bird, little egret (Egretta garzetta), in Hungary. Infect. Genet. Evol. 46:74–77
    [Google Scholar]
  59. 59.  Yugo DM, Cossaboom CM, Meng XJ 2014. Naturally occurring animal models of human hepatitis E virus infection. ILAR J 55:187–99
    [Google Scholar]
  60. 60.  Raj VS, Smits SL, Pas SD, Provacia LB, Moorman-Roest H et al. 2012. Novel hepatitis E virus in ferrets, the Netherlands. Emerg. Infect. Dis. 18:1369–70
    [Google Scholar]
  61. 61.  Krog JS, Breum SO, Jensen TH, Larsen LE 2013. Hepatitis E virus variant in farmed mink, Denmark. Emerg. Infect. Dis. 19:2028–30
    [Google Scholar]
  62. 62.  Johne R, Heckel G, Plenge-Bonig A, Kindler E, Maresch C et al. 2010. Novel hepatitis E virus genotype in Norway rats, Germany. Emerg. Infect. Dis. 16:1452–55
    [Google Scholar]
  63. 63.  Bodewes R, van der Giessen J, Haagmans BL, Osterhaus AD, Smits SL 2013. Identification of multiple novel viruses, including a parvovirus and a hepevirus, in feces of red foxes. J. Virol. 87:7758–64
    [Google Scholar]
  64. 64.  Smith DB, Simmonds P, Int. Comm. Taxon. Viruses Hepeviridae Study Group, Jameel S, Emerson SU et al. 2015. Consensus proposals for classification of the family Hepeviridae. J. Gen. Virol. 96:1191–92
    [Google Scholar]
  65. 65.  Lin J, Karlsson M, Olofson AS, Belak S, Malmsten J et al. 2015. High prevalence of hepatitis E virus in Swedish moose—a phylogenetic characterization and comparison of the virus from different regions. PLOS ONE 10:e0122102
    [Google Scholar]
  66. 66.  Reuter G, Boros A, Matics R, Kapusinszky B, Delwart E, Pankovics P 2016. Divergent hepatitis E virus in birds of prey, common kestrel (Falco tinnunculus) and red-footed falcon (F. vespertinus), Hungary. Infect. Genet. Evol. 43:343–46
    [Google Scholar]
  67. 67.  Kenney SP, Meng XJ 2018. Hepatitis E virus genome structure and replication strategy. Cold Spring Harb. Perspect. Med. In press
  68. 68.  Holla P, Ahmad I, Ahmed Z, Jameel S 2015. Hepatitis E virus enters liver cells through a dynamin-2, clathrin and membrane cholesterol-dependent pathway. Traffic 16:398–416
    [Google Scholar]
  69. 69.  Ichiyama K, Yamada K, Tanaka T, Nagashima S, Jirintai et al. 2009. Determination of the 5′-terminal sequence of subgenomic RNA of hepatitis E virus strains in cultured cells. Arch. Virol. 154:1945–51
    [Google Scholar]
  70. 70.  Cao D, Huang YW, Meng XJ 2010. The nucleotides on the stem-loop RNA structure in the junction region of the hepatitis E virus genome are critical for virus replication. J. Virol. 84:13040–44
    [Google Scholar]
  71. 71.  Parvez MK 2015. The intergenic-junction variant (genotype 2 isolate) of hepatitis E virus restores the CREX “stem-loop” structural integrity, essential for viral life cycle. Gene 559:149–54
    [Google Scholar]
  72. 72.  Emerson SU, Zhang M, Meng XJ, Nguyen H, St. Claire M et al. 2001. Recombinant hepatitis E virus genomes infectious for primates: importance of capping and discovery of a cis-reactive element. PNAS 98:15270–75
    [Google Scholar]
  73. 73.  Magden J, Takeda N, Li T, Auvinen P, Ahola T et al. 2001. Virus-specific mRNA capping enzyme encoded by hepatitis E virus. J. Virol. 75:6249–55
    [Google Scholar]
  74. 74.  Cao D, Meng X-J 2012. Molecular biology and replication of hepatitis E virus. Emerg. Microbes Infect. 1:e17
    [Google Scholar]
  75. 75.  Zhou X, Xu L, Wang Y, Wang W, Sprengers D et al. 2015. Requirement of the eukaryotic translation initiation factor 4F complex in hepatitis E virus replication. Antivir. Res. 124:11–19
    [Google Scholar]
  76. 76.  Emerson SU, Nguyen H, Graff J, Stephany DA, Brockington A, Purcell RH 2004. In vitro replication of hepatitis E virus (HEV) genomes and of an HEV replicon expressing green fluorescent protein. J. Virol. 78:4838–46
    [Google Scholar]
  77. 77.  Surjit M, Jameel S, Lal SK 2004. The ORF2 protein of hepatitis E virus binds the 5′ region of viral RNA. J. Virol. 78:320–28
    [Google Scholar]
  78. 78.  Emerson SU, Nguyen HT, Torian U, Burke D, Engle R, Purcell RH 2010. Release of genotype 1 hepatitis E virus from cultured hepatoma and polarized intestinal cells depends on open reading frame 3 protein and requires an intact PXXP motif. J. Virol. 84:9059–69
    [Google Scholar]
  79. 79.  Yamada K, Takahashi M, Hoshino Y, Takahashi H, Ichiyama K et al. 2009. ORF3 protein of hepatitis E virus is essential for virion release from infected cells. J. Gen. Virol. 90:1880–91
    [Google Scholar]
  80. 80.  Ding Q, Heller B, Capuccino JM, Song B, Nimgaonkar I et al. 2017. Hepatitis E virus ORF3 is a functional ion channel required for release of infectious particles. PNAS 114:1147–52
    [Google Scholar]
  81. 81.  Pavio N, Meng XJ, Renou C 2010. Zoonotic hepatitis E: animal reservoirs and emerging risks. Vet. Res. 41:46
    [Google Scholar]
  82. 82.  Johne R, Plenge-Bonig A, Hess M, Ulrich RG, Reetz J, Schielke A 2010. Detection of a novel hepatitis E-like virus in faeces of wild rats using a nested broad-spectrum RT-PCR. J. Gen. Virol. 91:750–58
    [Google Scholar]
  83. 83.  Saad MD, Hussein HA, Bashandy MM, Kamel HH, Earhart KC et al. 2007. Hepatitis E virus infection in work horses in Egypt. Infect. Genet. Evol. 7:368–73
    [Google Scholar]
  84. 84.  Zhang W, Shen Q, Mou J, Gong G, Yang Z et al. 2008. Hepatitis E virus infection among domestic animals in eastern China. Zoonoses Public Health 55:291–98
    [Google Scholar]
  85. 85.  Huang FF, Sun ZF, Emerson SU, Purcell RH, Shivaprasad HL et al. 2004. Determination and analysis of the complete genomic sequence of avian hepatitis E virus (avian HEV) and attempts to infect rhesus monkeys with avian HEV. J. Gen. Virol. 85:1609–18
    [Google Scholar]
  86. 86.  Meng XJ, Wiseman B, Elvinger F, Guenette DK, Toth TE et al. 2002. Prevalence of antibodies to hepatitis E virus in veterinarians working with swine and in normal blood donors in the United States and other countries. J. Clin. Microbiol. 40:117–22
    [Google Scholar]
  87. 87.  Meng XJ 2011. From barnyard to food table: the omnipresence of hepatitis E virus and risk for zoonotic infection and food safety. Virus Res 161:23–30
    [Google Scholar]
  88. 88.  Karetnyi YV, Gilchrist MJ, Naides SJ 1999. Hepatitis E virus infection prevalence among selected populations in Iowa. J. Clin. Virol. 14:51–55
    [Google Scholar]
  89. 89.  Grierson S, Heaney J, Cheney T, Morgan D, Wyllie S et al. 2015. Prevalence of hepatitis E virus infection in pigs at the time of slaughter, United Kingdom, 2013. Emerg. Infect. Dis. 21:1396–401
    [Google Scholar]
  90. 90.  Renou C, Afonso AM, Pavio N 2014. Foodborne transmission of hepatitis E virus from raw pork liver sausage, France. Emerg. Infect. Dis. 20:1945–47
    [Google Scholar]
  91. 91.  Crossan C, Baker PJ, Craft J, Takeuchi Y, Dalton HR, Scobie L 2012. Hepatitis E virus genotype 3 in shellfish, United Kingdom. Emerg. Infect. Dis. 18:2085–87
    [Google Scholar]
  92. 92.  Brassard J, Gagne MJ, Genereux M, Cote C 2012. Detection of human food-borne and zoonotic viruses on irrigated, field-grown strawberries. Appl. Environ. Microbiol. 78:3763–66
    [Google Scholar]
  93. 93.  Barnaud E, Rogee S, Garry P, Rose N, Pavio N 2012. Thermal inactivation of infectious hepatitis E virus in experimentally contaminated food. Appl. Environ. Microbiol. 78:5153–59
    [Google Scholar]
  94. 94.  Arankalle VA, Ticehurst J, Sreenivasan MA, Kapikian AZ, Popper H et al. 1988. Aetiological association of a virus-like particle with enterically transmitted non-A, non-B hepatitis. Lancet 1:550–54
    [Google Scholar]
  95. 95.  Kane MA, Bradley DW, Shrestha SM, Maynard JE, Cook EH et al. 1984. Epidemic non-A, non-B hepatitis in Nepal: recovery of a possible etiologic agent and transmission studies in marmosets. JAMA 252:3140–45
    [Google Scholar]
  96. 96.  Tam AW, White R, Reed E, Short M, Zhang Y et al. 1996. In vitro propagation and production of hepatitis E virus from in vivo–infected primary macaque hepatocytes. Virology 215:1–9
    [Google Scholar]
  97. 97.  Tam AW, White R, Yarbough PO, Murphy BJ, McAtee CP et al. 1997. In vitro infection and replication of hepatitis E virus in primary cynomolgus macaque hepatocytes. Virology 238:94–102
    [Google Scholar]
  98. 98.  Huang RT, Li DR, Wei J, Huang XR, Yuan XT, Tian X 1992. Isolation and identification of hepatitis E virus in Xinjiang, China. J. Gen. Virol. 73:51143–48
    [Google Scholar]
  99. 99.  Huang R, Nakazono N, Ishii K, Li D, Kawamata O et al. 1995. Hepatitis E virus (87A strain) propagated in A549 cells. J. Med. Virol. 47:299–302
    [Google Scholar]
  100. 100.  Huang R, Li D, Wei S, Li Q, Yuan X et al. 1999. Cell culture of sporadic hepatitis E virus in China. Clin. Diagn. Lab. Immunol. 6:729–33
    [Google Scholar]
  101. 101.  Kazachkov YA, Balayan MS, Ivannikova TA, Panina LI, Orlova TM et al. 1992. Hepatitis E virus in cultivated cells. Arch. Virol. 127:399–402
    [Google Scholar]
  102. 102.  Wei S, Walsh P, Huang R, To SS 2000. 93G, a novel sporadic strain of hepatitis E virus in South China isolated by cell culture. J. Med. Virol. 61:311–18
    [Google Scholar]
  103. 103.  Okamoto H 2011. Hepatitis E virus cell culture models. Virus Res 161:65–77
    [Google Scholar]
  104. 104.  Tanaka T, Takahashi M, Takahashi H, Ichiyama K, Hoshino Y et al. 2009. Development and characterization of a genotype 4 hepatitis E virus cell culture system using a HE-JF5/15F strain recovered from a fulminant hepatitis patient. J. Clin. Microbiol. 47:1906–10
    [Google Scholar]
  105. 105.  Shukla P, Nguyen HT, Torian U, Engle RE, Faulk K et al. 2011. Cross-species infections of cultured cells by hepatitis E virus and discovery of an infectious virus-host recombinant. PNAS 108:2438–43
    [Google Scholar]
  106. 106.  Shukla P, Nguyen HT, Faulk K, Mather K, Torian U et al. 2012. Adaptation of a genotype 3 hepatitis E virus to efficient growth in cell culture depends on an inserted human gene segment acquired by recombination. J. Virol. 86:5697–707
    [Google Scholar]
  107. 107.  von Nordheim M, Boinay M, Leisi R, Kempf C, Ros C 2016. Cutthroat trout virus—towards a virus model to support hepatitis E research. Viruses 8:289
    [Google Scholar]
  108. 108.  Balayan MS, Andjaparidze AG, Savinskaya SS, Ketiladze ES, Braginsky DM et al. 1983. Evidence for a virus in non-A, non-B hepatitis transmitted via the fecal-oral route. Intervirology 20:23–31
    [Google Scholar]
  109. 109.  Bradley DW, Krawczynski K, Cook EH Jr., McCaustland KA, Humphrey CD et al. 1987. Enterically transmitted non-A, non-B hepatitis: serial passage of disease in cynomolgus macaques and tamarins and recovery of disease-associated 27- to 34-nm viruslike particles. PNAS 84:6277–81
    [Google Scholar]
  110. 110.  Tsarev SA, Tsareva TS, Emerson SU, Kapikian AZ, Ticehurst J et al. 1993. ELISA for antibody to hepatitis E virus (HEV) based on complete open-reading frame-2 protein expressed in insect cells: identification of HEV infection in primates. J. Infect. Dis. 168:369–78
    [Google Scholar]
  111. 111.  Ticehurst J, Rhodes LL Jr., Krawczynski K, Asher LV, Engler WF et al. 1992. Infection of owl monkeys (Aotus trivirgatus) and cynomolgus monkeys (Macaca fascicularis) with hepatitis E virus from Mexico. J. Infect. Dis. 165:835–45
    [Google Scholar]
  112. 112.  Arankalle VA, Goverdhan MK, Banerjee K 1994. Antibodies against hepatitis E virus in Old World monkeys. J. Viral Hepatol. 1:125–29
    [Google Scholar]
  113. 113.  Purcell RH, Emerson SU 2001. Animal models of hepatitis A and E. ILAR J 42:161–77
    [Google Scholar]
  114. 114.  Krawczynski K, Meng XJ, Rybczynska J 2011. Pathogenetic elements of hepatitis E and animal models of HEV infection. Virus Res 161:78–83
    [Google Scholar]
  115. 115.  Shrestha MP, Scott RM, Joshi DM, Mammen MP Jr., Thapa GB et al. 2007. Safety and efficacy of a recombinant hepatitis E vaccine. N. Engl. J. Med. 356:895–903
    [Google Scholar]
  116. 116.  Zhu FC, Zhang J, Zhang XF, Zhou C, Wang ZZ et al. 2010. Efficacy and safety of a recombinant hepatitis E vaccine in healthy adults: a large-scale, randomised, double-blind placebo-controlled, phase 3 trial. Lancet 376:895–902
    [Google Scholar]
  117. 117.  Proffitt A 2012. First HEV vaccine approved. Nat. Biotechnol. 30:300
    [Google Scholar]
  118. 118.  Bouwknegt M, Rutjes SA, Reusken CB, Stockhofe-Zurwieden N, Frankena K et al. 2009. The course of hepatitis E virus infection in pigs after contact-infection and intravenous inoculation. BMC Vet. Res. 5:7
    [Google Scholar]
  119. 119.  Pudupakam RS, Huang YW, Opriessnig T, Halbur PG, Pierson FW, Meng XJ 2009. Deletions of the hypervariable region (HVR) in open reading frame 1 of hepatitis E virus do not abolish virus infectivity: evidence for attenuation of HVR deletion mutants in vivo. J. Virol. 83:384–95
    [Google Scholar]
  120. 120.  Pudupakam RS, Kenney SP, Cordoba L, Huang YW, Dryman BA et al. 2011. Mutational analysis of the hypervariable region of hepatitis E virus reveals its involvement in the efficiency of viral RNA replication. J. Virol. 85:10031–40
    [Google Scholar]
  121. 121.  Feagins AR, Cordoba L, Sanford BJ, Dryman BA, Huang YW et al. 2011. Intergenotypic chimeric hepatitis E viruses (HEVs) with the genotype 4 human HEV capsid gene in the backbone of genotype 3 swine HEV are infectious in pigs. Virus Res 156:141–46
    [Google Scholar]
  122. 122.  Sanford BJ, Opriessnig T, Kenney SP, Dryman BA, Cordoba L, Meng XJ 2012. Assessment of the cross-protective capability of recombinant capsid proteins derived from pig, rat, and avian hepatitis E viruses (HEV) against challenge with a genotype 3 HEV in pigs. Vaccine 30:6249–55
    [Google Scholar]
  123. 123.  Sanford BJ, Dryman BA, Huang YW, Feagins AR, Leroith T, Meng XJ 2011. Prior infection of pigs with a genotype 3 swine hepatitis E virus (HEV) protects against subsequent challenges with homologous and heterologous genotypes 3 and 4 human HEV. Virus Res 159:17–22
    [Google Scholar]
  124. 124.  Billam P, Huang FF, Sun ZF, Pierson FW, Duncan RB et al. 2005. Systematic pathogenesis and replication of avian hepatitis E virus in specific-pathogen-free adult chickens. J. Virol. 79:3429–37
    [Google Scholar]
  125. 125.  Guo H, Zhou EM, Sun ZF, Meng XJ 2007. Egg whites from eggs of chickens infected experimentally with avian hepatitis E virus contain infectious virus, but evidence of complete vertical transmission is lacking. J. Gen. Virol. 88:1532–37
    [Google Scholar]
  126. 126.  Guo H, Zhou EM, Sun ZF, Meng XJ 2008. Immunodominant epitopes mapped by synthetic peptides on the capsid protein of avian hepatitis E virus are non-protective. Viral Immunol 21:61–67
    [Google Scholar]
  127. 127.  Zhou EM, Guo H, Huang FF, Sun ZF, Meng XJ 2008. Identification of two neutralization epitopes on the capsid protein of avian hepatitis E virus. J. Gen. Virol. 89:500–8
    [Google Scholar]
  128. 128.  Guo H, Zhou EM, Sun ZF, Meng XJ 2007. Protection of chickens against avian hepatitis E virus (avian HEV) infection by immunization with recombinant avian HEV capsid protein. Vaccine 25:2892–99
    [Google Scholar]
  129. 129.  Cossaboom CM, Cordoba L, Dryman BA, Meng XJ 2011. Hepatitis E virus in rabbits, Virginia, USA. Emerg. Infect. Dis. 17:2047–49
    [Google Scholar]
  130. 130.  Izopet J, Dubois M, Bertagnoli S, Lhomme S, Marchandeau S et al. 2012. Hepatitis E virus strains in rabbits and evidence of a closely related strain in humans, France. Emerg. Infect. Dis. 18:1274–81
    [Google Scholar]
  131. 131.  Ma H, Zheng L, Liu Y, Zhao C, Harrison TJ et al. 2010. Experimental infection of rabbits with rabbit and genotypes 1 and 4 hepatitis E viruses. PLOS ONE 5:e9160
    [Google Scholar]
  132. 132.  Liu P, Bu QN, Wang L, Han J, Du RJ et al. 2013. Transmission of hepatitis E virus from rabbits to cynomolgus macaques. Emerg. Infect. Dis. 19:559–65
    [Google Scholar]
  133. 133.  Cossaboom CM, Cordoba L, Sanford BJ, Pineyro P, Kenney SP et al. 2012. Cross-species infection of pigs with a novel rabbit, but not rat, strain of hepatitis E virus isolated in the United States. J. Gen. Virol. 93:1687–95
    [Google Scholar]
  134. 134.  Han J, Lei Y, Liu L, Liu P, Xia J et al. 2014. SPF rabbits infected with rabbit hepatitis E virus isolate experimentally showing the chronicity of hepatitis. PLOS ONE 9:e99861
    [Google Scholar]
  135. 135.  Xia J, Liu L, Wang L, Zhang Y, Zeng H et al. 2015. Experimental infection of pregnant rabbits with hepatitis E virus demonstrating high mortality and vertical transmission. J. Viral Hepatol. 22:850–57
    [Google Scholar]
  136. 136.  Purcell RH, Engle RE, Rood MP, Kabrane-Lazizi Y, Nguyen HT et al. 2011. Hepatitis E virus in rats, Los Angeles, California, USA. Emerg. Infect. Dis. 17:2216–22
    [Google Scholar]
  137. 137.  Debing Y, Mishra N, Verbeken E, Ramaekers K, Dallmeier K, Neyts J 2016. A rat model for hepatitis E virus. Dis. Models Mech. 9:1203–10
    [Google Scholar]
  138. 138.  Jirintai S, Tanggis, Mulyanto, Suparyatmo JB, Takahashi M et al. 2014. Rat hepatitis E virus derived from wild rats (Rattus rattus) propagates efficiently in human hepatoma cell lines. Virus Res 185:92–102
    [Google Scholar]
  139. 139.  Maneerat Y, Clayson ET, Myint KS, Young GD, Innis BL 1996. Experimental infection of the laboratory rat with the hepatitis E virus. J. Med. Virol. 48:121–28
    [Google Scholar]
  140. 140.  Li TC, Yoshizaki S, Ami Y, Suzaki Y, Yasuda SP et al. 2013. Susceptibility of laboratory rats against genotypes 1, 3, 4, and rat hepatitis E viruses. Vet. Microbiol. 163:54–61
    [Google Scholar]
  141. 141.  Li TC, Suzaki Y, Ami Y, Tsunemitsu H, Miyamura T, Takeda N 2008. Mice are not susceptible to hepatitis E virus infection. J. Vet. Med. Sci. 70:1359–62
    [Google Scholar]
  142. 142.  Huang F, Zhang W, Gong G, Yuan C, Yan Y et al. 2009. Experimental infection of Balb/c nude mice with hepatitis E virus. BMC Infect. Dis. 9:93
    [Google Scholar]
  143. 143.  Allweiss L, Gass S, Giersch K, Groth A, Kah J et al. 2016. Human liver chimeric mice as a new model of chronic hepatitis E virus infection and preclinical drug evaluation. J. Hepatol. 64:1033–40
    [Google Scholar]
  144. 144.  Yang T, Kataoka M, Ami Y, Suzaki Y, Kishida N et al. 2013. Characterization of self-assembled virus-like particles of ferret hepatitis E virus generated by recombinant baculoviruses. J. Gen. Virol. 94:2647–56
    [Google Scholar]
  145. 145.  Li TC, Yoshizaki S, Ami Y, Suzaki Y, Yang T et al. 2015. Monkeys and rats are not susceptible to ferret hepatitis E virus infection. Intervirology 58:139–42
    [Google Scholar]
  146. 146.  Li TC, Yang T, Yoshizaki S, Ami Y, Suzaki Y et al. 2016. Ferret hepatitis E virus infection induces acute hepatitis and persistent infection in ferrets. Vet. Microbiol. 183:30–36
    [Google Scholar]
  147. 147.  Li TC, Yoshizaki S, Yang T, Kataoka M, Nakamura T et al. 2016. Production of infectious ferret hepatitis E virus in a human hepatocarcinoma cell line PLC/PRF/5. Virus Res 213:283–88
    [Google Scholar]
  148. 148.  van de Garde MDB, Pas SD, van Oord GW, Gama L, Choi Y et al. 2017. Interferon-alpha treatment rapidly clears Hepatitis E virus infection in humanized mice. Sci. Rep. 7:8267
    [Google Scholar]
  149. 149.  Gardinali NR, Guimaraes JR, Melgaco JG, Kevorkian YB, Bottino FO et al. 2017. Cynomolgus monkeys are successfully and persistently infected with hepatitis E virus genotype 3 (HEV-3) after long-term immunosuppressive therapy. PLOS ONE 12:e0174070
    [Google Scholar]
  150. 150.  Meng XJ, Halbur PG, Haynes JS, Tsareva TS, Bruna JD et al. 1998. Experimental infection of pigs with the newly identified swine hepatitis E virus (swine HEV), but not with human strains of HEV. Arch. Virol. 143:1405–15
    [Google Scholar]
  151. 151.  Cao D, Cao QM, Subramaniam S, Yugo DM, Heffron CL et al. 2017. Pig model mimicking chronic hepatitis E virus infection in immunocompromised patients to assess immune correlates during chronicity. PNAS 114:6914–23
    [Google Scholar]
  152. 152.  van de Garde MD, Pas SD, van der Net G, de Man RA, Osterhaus AD et al. 2016. Hepatitis E virus (HEV) genotype 3 infection of human liver chimeric mice as a model for chronic HEV infection. J. Virol. 90:4394–401
    [Google Scholar]
  153. 153.  Tsarev SA, Tsareva TS, Emerson SU, Rippy MK, Zack P et al. 1995. Experimental hepatitis E in pregnant rhesus monkeys: failure to transmit hepatitis E virus (HEV) to offspring and evidence of naturally acquired antibodies to HEV. J. Infect. Dis. 172:31–37
    [Google Scholar]
  154. 154.  Kasorndorkbua C, Thacker BJ, Halbur PG, Guenette DK, Buitenwerf RM et al. 2003. Experimental infection of pregnant gilts with swine hepatitis E virus. Can. J. Vet. Res. 67:303–6
    [Google Scholar]
  155. 155.  Tamura K, Nei M 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10:512–26
    [Google Scholar]
  156. 156.  Kumar S, Stecher G, Tamura K 2016. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for bigger datasets. Mol. Biol. Evol. 33:1870–74
    [Google Scholar]
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