Вопросы вирусологии. 2022; 67: 173-184
Энтеральные вирусные гепатиты у обезьян
https://doi.org/10.36233/0507-4088-110Аннотация
В течение последнего десятилетия большое число вирусов, генетически связанных с вирусами гепатита человека, были обнаружены у животных, в том числе и обезьян. Множество вирусов, близких вирусу гепатита А (ВГА, Picornaviridae: Hepatovirus: Hepatovirus A) человека, было обнаружено у различных видов млекопитающих в течение 2015–2018 гг., включая главным образом летучих мышей и грызунов, а также землероек, тюленей и сумчатых животных. Зоонозные генотипы вируса гепатита Е (ВГЕ, Hepeviridae: Orthohepevirus: Orthohepevirus A) были обнаружены у диких кабанов, оленей, верблюдов и кроликов, а также у приматов. Кроме того, у летучих мышей, хорьков, грызунов, птиц и рыб были описаны вирусы, генетически близкие ВГЕ. Тем не менее именно обезьяны остаются важными лабораторными животными для изучения ВГА- и ВГЕ-инфекции. Изучение спонтанной и экспериментальной инфекции у этих животных представляет бесценный источник информации о биологии и патогенезе этих вирусов и по-прежнему является незаменимым инструментом для тестирования вакцин и лекарств. Целью данного обзора литературы являлись обобщение и анализ опубликованных данных о циркуляции ВГА и ВГЕ среди диких и содержащихся в неволе приматов, а также результатов экспериментов по моделированию на обезьянах инфекций, вызываемых ВГА и ВГЕ.
Список литературы
1. Drexler J.F., Corman V.M., Lukashev A.N., van den Brand J.M.A., Gmyl A.P., Brünink S., et al. The Hepatovirus Ecology Consortium. Evolutionary origins of hepatitis A virus in small mammals. PNAS. 2015; 112(49): 15190–5. https://doi.org/10.1073/pnas.1516992112
2. Sridhar S., Teng J.L.L., Chiu T.H., Lau S.K.P., Woo P.C.Y. Hepatitis E virus genotypes andevolution: emergence of camel hepatitis E variants. Int. J. Mol. Sci. 2017; 18(4): 1–19. https://doi.org/10.3390/ijms18040869
3. Batts W., Yun S., Hedrick R., Winton J. A novel member of the family Hepeviridae from cutthroat trout (Oncorhynchus clarkii). Virus Res. 2011; 158(1-2): 116–23. https://doi.org/10.1016/j.virusres.2011.03.019
4. ICTV. International Committee on Taxonomy of Viruses. Genus: Hepatovirus; 2021. Available at: https://talk.ictvonline.org/ictv-reports/ictv_online_report/positive-sense-rna-viruses/w/picornaviridae/709/genus-hepatovirus
5. Hillis W.D. An outbreak of infectious hepatitis among chimpanzee handlers at a United States Air Force base. Am. J. Hyg. 1961; 73: 316–28. https://doi.org/10.1093/oxfordjournals.aje.a120191
6. Mosely J.W., Reinhardt H.P., Hassler F.R. Chimpanzee-associated hepatitis: an outbreak in Oklahoma. JAMA. 1967; 199(10): 105–7.
7. Robertson B.H., Jansen R.W., Khanna B., Totsuka A., Nainan O.V., Siegl G., et al. Genetic relatedness of hepatitis A virus strains recovered from different geographical regions. J. Gen. Virol. 1992; 73(6): 1365–77. https://doi.org/10.1099/0022-1317-73-6-1365
8. Robertson B.H. Viral hepatitis and primates: historical and molecular analysis of human and nonhuman primate hepatitis A, B, and the GB-related viruses. J. Viral. Hepat. 2001; 8(4): 233–42. https://doi.org/10.1046/j.1365-2893.2001.00295.x
9. Ruddy S.J., Mosley J.W., Held J.R. Chimpanzee-associated viral hepatitis in 1963. Am. J. Epidemiol. 1967; 86(3): 634–40. https://doi.org/10.1093/oxfordjournals.aje.a120772
10. Burke D.S., Graham R.R., Heisey G.B., Coursaget R., Levesque B., Gretillat E., et al. Hepatitis A virus in primates outside captivity. Lancet. 1981; 2(8252): 928. https://doi.org/10.1016/S0140-6736(81)91411-2
11. Smith M.S., Swanepoel P.J., Bootsma M. Hepatitis A in nonhuman primates in nature. Lancet. 1980; 2(8206): 1241–2. https://doi.org/10.1016/s0140-6736(80)92495-2
12. Kalter S.S., Heberling R.L., Cooke A.W., Barry J.D., Tian P.Y., Northam W.J. Viral infections of nonhuman primates. Lab. Anim. Sci. 1997; 47(5): 461–8.
13. Purcell R.H., Emerson S.U. Animal models of hepatitis A and E. ILAR J. 2001; 42(2): 161–77. https://doi.org/10.1101/cshperspect.a031815
14. Korzaya L.I., Lapin B.A., Shevtsova Z.V., Krilova R.I. Spontaneous and experimental hepatitis A in Old World monkeys are the models of human hepatitis A. Baltic J. Lab. Animal. Sci. 2001; 11(2): 135–41.
15. Догадов Д.И., Корзая Л.И., Кюрегян К.К., Карлсен А.А., Михайлов М.И., Лапин Б.А. Маркёры гепатита A у обезьян Адлерского приматологического центра. Вопросы вирусологии. 2019; 64(5): 246–9. https://doi.org/10.36233/0507-4088-2019-64-5-246-249
16. Корзая Л.И., Кебурия В.В., Гончаренко А.М., Догадов Д.И., Лапин Б.А. Маркёры вирусных инфекций у лабораторных приматов. В кн.: Материалы второй международной научной конференции «Фундаментальные и прикладные аспекты медицинской приматологии». Сочи; 2011: 79–88.
17. Drewe J.A., O’Riain M.J., Beamish E., Currie H., Parsons S. Survey of infections transmissible between baboons and humans, Cape Town, South Africa. Emerg. Infect. Dis. 2012; 18(2): 298–301. https://doi.org/10.3201/eid1802.111309
18. Gust I.D., Lehmann N.I., Crowe S., McCrorie M., Locarnini S.A., Lucas C.R. The origin of the HM175 strain of hepatitis A virus. J. Infect. Dis. 1985; 151(2): 365–7. https://doi.org/10.1093/infdis/151.2.365
19. Balayan M.S., Kusov Yu.Yu., Andjaparidze A.G., Tsarev S.A., Sverdlov E.D., Chizhikov V.E., et al. Variations in genome fragments coding for RNA polymerase in human and simian hepatitis A viruses. FEBS Lett. 1989; 247(2): 425–8. https://doi.org/10.1016/0014-5793(89)81384-5
20. Nainan O.V., Margolis H.S., Robertson B.H., Balayan M., Brinton M.A. Sequence analysis of a new hepatitis A virus naturally infecting cynomolgus macaques (Macaca fascicularis). J. Gen. Virol. 1991; 72(7): 1685–9. https://doi.org/10.1099/0022-1317-72-7-1685
21. Van Cuyck-Gandré H., Cockman-Thomas R., Caudill J.D., Asher L.S., Armstrong K.L., Hauroeder B., et al. Experimental African HEV infection in cynomolgus macaques (Macaca fascicularis). J. Med. Virol. 1998; 55(3): 197–202. https://doi.org/10.1002/(SICI)1096-9071(199807)55:3<197::AID-JMV3>3.0.CO;2-X
22. Lu L., Ching K.Z., de Paula V.S., Nakano T., Siegl G., Weitz M., et al. Characterization of the complete genomic sequence of genotype II hepatitis A virus (CF53/Berne isolate). J. Gen. Viro. 2004; 85(10): 2943–52. https://doi.org/10.1099/vir.0.80304-0
23. Cristina J., Costa-Mattioli M. Genetic variability and molecular evolution of hepatitis A virus. Virus Res. 2007; 127(2): 127–57. https://doi.org/10.1016/j.virusres.2007.01.005
24. Costa-Mattioli M., Di Napoli A., Ferre V., Billaudel S., Perez-Bercoff R., Cristina J. Genetic variability of hepatitis A virus. J. Gen. Virol. 2003; 84(Pt. 12): 3191–201. https://doi.org/10.1099/vir.0.19532-0
25. Khanna B., Spelbring J.E., Innis B.L., Robertson B.H. Characterization of a genetic variant of human hepatitis A virus. J. Med. Virol. 1992; 36(2): 118–24. https://doi.org/10.1002/jmv.1890360208
26. Lemon S.M., LeDuc J.W., Binn L.N., Escajadillo A., Ishak K.G. Transmission of hepatitis A virus among recently captured Panamanian owl monkeys. J. Med. Virol. 1982; 10(1): 25–36. https://doi.org/10.1002/jmv.1890100105
27. Анджапаридзе А.Г., Каретный Ю.В., Корзая Л.И., Балаян М.С., Титова И.П., Замятина Н.А. Эпизоотия гепатита А среди африканских зеленых мартышек, содержащихся в условиях вивария. Вопросы вирусологии. 1989; 34(3): 292–6.
28. Arankalle V.A., Ramakrishnan J. Simian hepatitis A virus derived from a captive rhesus monkey in India is similar to the strain isolated from wild African green monkeys in Kenya. J. Viral. Hepat. 2009; 16(3): 214–8. https://doi.org/10.1111/j.1365-2893.2008.01060.x
29. Bennett A.J., Sibley S.D., Lauck M., Weny G., Hyeroba D., Tumukunde A., et al. Naturally circulating Hepatitis A virus in olive baboons, Uganda. Emerg. Infect. Dis. 2016; 22(7): 1308–10. https://doi.org/10.3201/eid2207.151837
30. Dogadov D.I., Korzaya L.I., Karlsen A.A., Kyuregyan K.K. Molecular genetic identification of isolates of the hepatitis A virus (HAV) from monkeys at Adler primate center. J. Med. Primatol. 2018; 47(2): 87–92. https://doi.org/10.1111/jmp.12333
31. Анджапаридзе А.Г., Полещук В.Ф., Замятина Н.А., Савинов А.П., Гавриловская И.Н., Балаян М.С. Спонтанный гепатит у яванской макаки, подвергнутой воздействию иммунодепрессантов. Вопросы вирусологии. 1985; (4-С): 468–73.
32. Tsarev S.A., Emerson S.U., Balayan M.S., Ticehurst J., Purcel R.H. Simian hepatitis A virus (HAV) strain AGM-27: comparison of genome structure and growth in cell culture with other HAV strains. J. Gen. Virol. 1991; 72(7): 1677–83. https://doi.org/10.1099/0022-1317-72-7-1677
33. Raychaudhuri G., Govindarajan S., Shapiro M., Purcell R.H., Emerson S.U. Utilization of chimeras between human (HM-175) and simian (AGM-27) strains of hepatitis A virus to study the molecular basis of virulence. J. Virol. 1998; 7(4): 7467–75. https://doi.org/10.1128/JVI.72.9.7467-7475.1998
34. Лапин Б.А., Джикидзе Э.К., Крылова Р.И., Стасилевич З.К., Яковлева Л.А. Проблемы инфекционной патологии обезьян. М.: РАМН; 2004.
35. Полещук В.Ф., Балаян М.С., Анджапаридзе А.Г., Соболь А.В., Докин В.П., Гуляева Т.В. и др. Моделирование гепатита А и энтерально передающегося гепатита ни А ни В (гепатит Е) на тамаринах Saguinus mystax. Вопросы вирусологии. 1990; 35(5): 379–82.
36. Полещук В.Ф., Михайлов М.И., Замятина Н.А. Приматные модели вирусных гепатитов человека. Вопросы вирусологии. 2006; 51(4): 6–13.
37. ICTV. International Committee on Taxonomy of Viruses. Genus: Hepeviridae; 2021. Available at: https://talk.ictvonline.org/ictv-reports/ictv_online_report/positive-sense-rna-viruses/w/hepeviridae
38. Balayan M.S., Andjaparidze A.G., Savinskaya S.S., Ketiladze E.S., Braginsky D.M., Savinov A.P., et al. Evidence for a virus in non-A, non-B hepatitis transmitted via the fecal-oral route. Intervirology. 1983; 20(1): 23–31. https://doi.org/10.1159/000149370
39. Hirano M., Ding X., Li T.C., Takeda N., Kawabata H., Koizumi N., et al. Evidence for widespread infection of hepatitis E virus among wild rats in Japan. Hepatol. Res. 2003; 27(1): 1–5. https://doi.org/10.1016/S1386-6346(03)00192-X
40. Nakamura S., Tsuchiya H., Okahara N., Nakagawa T., Ohara N., Yamamoto H., et al. Epidemiology of hepatitis E virus in indoor-captive cynomolgus monkey colony. J. Vet. Med. Sci. 2012; 74(3): 279–83. https://doi.org/10.1292/jvms.11-0394
41. Yamamoto H., Li T.C., Koshimoto C., Ito K., Kita M., Miyashita N., et al. Serological evidence for hepatitis E virus infection in laboratory monkeys and pigs in animal facilities in Japan. Exp. Anim. 2008; 57(4): 367–76. https://doi.org/10.1538/expanim.57.367
42. Корзая Л.И., Кебурия В.В., Догадов Д.И., Лапин Б.А., Кюрегян К.К., Михайлов М.И. Маркёры гепатита Е у населения Большого Сочи и обезьян Адлерского приматологического центра. Вопросы вирусологии. 2016; 61(4): 176–80. https://doi.org/10.18821/0507-4088-2016-61-4-176-180
43. Корзая Л.И., Догадов Д.И., Гончаренко А.М., Карлсен А.А., Кюрегян К.К., Михайлов М.И. Распространение маркёров респираторных вирусов человека среди обезьян Адлерского приматологического центра. Вопросы вирусологии. 2021; 66(6): 425–33. https://doi.org/10.36233/0507-4088-77
44. Yamamoto H., Suzuki J., Matsuda A., Ishida T., Ami Y., Suzaki Y., et al. Hepatitis E virus outbreak in monkey facility, Japan. Emerg. Infect. Dis. 2012; 18(12): 2032–4. https://doi.org/10.3201/eid1812.120884
45. Huang F., Yu W., Hua X., Jing S., Zeng W., He Z. Seroepidemiology and molecular characterization of hepatitis E virus in Macaca Mulatta from a village in Yunnan, China, where infection with this virus is endemic. Hepat. Mon. 2011; 11(9): 745–9. https://doi.org/10.5812/kowsar.1735143X.730
46. Yang F., Duan S., Guo Y., Li Y., Yoshizaki S., Takeda N., et al. Current status of hepatitis E virus infection at a rhesus monkey farm in China. Vet. Microbiol. 2019; 230: 244–8. https://doi.org/10.1016/j.vetmic.2019.01.021
47. Dogadov D.I., Korzaya L.I., Kyuregyan K.K., Karlsen A.A., Kichatova V.S., Potemkin I.A., et al. Natural infection of captive cynomolgus monkeys (Macaca fascicularis) with hepatitis E virus genotype 4. Arch. Virol. 2019; 164(10): 2515–8. https://doi.org/10.1007/s00705-019-04337-3
48. Кюрегян К.К., Полещук В.Ф., Гордейчук И.В., Гуляева Т.В., Исаева О.В., Морозов И.А. и др. Моделирование вирусного гепатита Е на игрунковых обезьянах. Бюллетень эксперимен- тальной биологии и медицины. 2015; 160(9): 355–9. https://doi.org/10.1007/s10517-016-3173-0
49. Gordeychuk I., Kyuregyan K., Kondrashova A., Bayurova E., Gulyaev S., Gulyaeva T., et al. Immunization with recombinant ORF2 p551 protein protects common marmosets (Callithrix jacchus) against homologous and heterologous hepatitis E virus challenge. Vaccine. 2022; 40(1): 89–99. https://doi.org/10.1016/j.vaccine.2021.11.042
50. Longer C.F., Denny S.L., Caudill J.D., Miele T.A., Asher L.V., Myint K.S., et al. Experimental hepatitis E: pathogenesis in cynomolgus macaques (Macaca fascicularis). J. Infect. Dis. 1993; 168(3): 602–9. https://doi.org/10.1093/infdis/168.3.602
51. Van Cuyck-Gandré H., Cockman-Thomas R., Caudill J.D., Asher L.S., Armstrong K.L., Hauroeder B., et al. Experimental African HEV infection in cynomolgus macaques (Macaca fascicularis). J. Med. Virol. 1998; 55(3): 197–202. https://doi.org/10.1002/(SICI)1096-9071(199807)55:3<197::AID-JMV3>3.0.CO;2-X
52. Tsarev S.A., Tsareva T.S., Emerson S.U., Rippy M.K., Zack P., Shapiro M., et al. 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. 1995; 172(1): 31–7. https://doi.org/10.1093/infdis/172.1.31
53. de Carvalho L.G., Marchevsky R.S., dos Santos D.R., de Oliveira J.M., de Paula V.S., Lopes L.M., et al. Infection by Brazilian and Dutch swine hepatitis E virus strains induces haematological changes in Macaca fascicularis. BMC Infect. Dis. 2013; 13(495): 495. https://doi.org/10.1186/1471-2334-13-495
54. Purcell R.H., Engle R.E., Rood M.P., Kabrane-Lazizi Y., Nguyen H.T., Govindarajan S., et al. Hepatitis E virus in rats, Los Angeles, California, USA. Emerg. Infect. Dis. 2011; 17(12): 2216–22. https://doi.org/10.3201/eid1712.110482
55. Yang F., Li Y., Li Y., Jin W., Duan S., Xu H., et al. Experimental Cross-Species Transmission of Rat Hepatitis E Virus to Rhesus and Cynomolgus Monkeys. Viruses. 2022; 14(2): 293. https://doi.org/10.3390/v14020293
56. Huang F.F., Sun Z.F., Emerson S.U., Purcell R.H. 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. 2004; 85(6): 1609–18. https://doi.org/10.1099/vir.0.79841-0
57. Михайлов М.И., Кюрегян К.К., Груздева К.Н. Вирус гепатита Е птиц. Мир вирусных гепатитов. 2005; (10): 8–11.
Problems of Virology. 2022; 67: 173-184
Enteral viral hepatitis in monkeys
https://doi.org/10.36233/0507-4088-110Abstract
Within the last decade, a large number of viruses genetically related to human hepatitis viruses have been identified in different animal species, including monkeys. Numerous viruses related to human hepatitis A virus (HAV, Picornaviridae: Hepatovirus: Hepatovirus A) were detected in various mammalian species in 2015–2018, predominantly in bats and rodents, but also in shrews, seals and marsupials. Zoonotic hepatitis E virus (HEV, Hepeviridae: Orthohepevirus: Orthohepevirus A) genotypes have been found in wild boars, deer, camels, and rabbits, as well as in non human primates. In addition, viruses that are genetically close to HEV have been described in bats, ferrets, rodents, birds, and fish. Nevertheless, monkeys remain important laboratory animals in HAV and HEV research. The study of spontaneous and experimental infection in these animals is an invaluable source of information about the biology and pathogenesis of these viruses and continues to be an indispensable tool for vaccine and drug testing. The purpose of this literature review was to summarize and analyze published data on the circulation of HAV and HEV among wild and captive primates, as well as the results of experimental studies of HAV and HEV infections in monkeys.
References
1. Drexler J.F., Corman V.M., Lukashev A.N., van den Brand J.M.A., Gmyl A.P., Brünink S., et al. The Hepatovirus Ecology Consortium. Evolutionary origins of hepatitis A virus in small mammals. PNAS. 2015; 112(49): 15190–5. https://doi.org/10.1073/pnas.1516992112
2. Sridhar S., Teng J.L.L., Chiu T.H., Lau S.K.P., Woo P.C.Y. Hepatitis E virus genotypes andevolution: emergence of camel hepatitis E variants. Int. J. Mol. Sci. 2017; 18(4): 1–19. https://doi.org/10.3390/ijms18040869
3. Batts W., Yun S., Hedrick R., Winton J. A novel member of the family Hepeviridae from cutthroat trout (Oncorhynchus clarkii). Virus Res. 2011; 158(1-2): 116–23. https://doi.org/10.1016/j.virusres.2011.03.019
4. ICTV. International Committee on Taxonomy of Viruses. Genus: Hepatovirus; 2021. Available at: https://talk.ictvonline.org/ictv-reports/ictv_online_report/positive-sense-rna-viruses/w/picornaviridae/709/genus-hepatovirus
5. Hillis W.D. An outbreak of infectious hepatitis among chimpanzee handlers at a United States Air Force base. Am. J. Hyg. 1961; 73: 316–28. https://doi.org/10.1093/oxfordjournals.aje.a120191
6. Mosely J.W., Reinhardt H.P., Hassler F.R. Chimpanzee-associated hepatitis: an outbreak in Oklahoma. JAMA. 1967; 199(10): 105–7.
7. Robertson B.H., Jansen R.W., Khanna B., Totsuka A., Nainan O.V., Siegl G., et al. Genetic relatedness of hepatitis A virus strains recovered from different geographical regions. J. Gen. Virol. 1992; 73(6): 1365–77. https://doi.org/10.1099/0022-1317-73-6-1365
8. Robertson B.H. Viral hepatitis and primates: historical and molecular analysis of human and nonhuman primate hepatitis A, B, and the GB-related viruses. J. Viral. Hepat. 2001; 8(4): 233–42. https://doi.org/10.1046/j.1365-2893.2001.00295.x
9. Ruddy S.J., Mosley J.W., Held J.R. Chimpanzee-associated viral hepatitis in 1963. Am. J. Epidemiol. 1967; 86(3): 634–40. https://doi.org/10.1093/oxfordjournals.aje.a120772
10. Burke D.S., Graham R.R., Heisey G.B., Coursaget R., Levesque B., Gretillat E., et al. Hepatitis A virus in primates outside captivity. Lancet. 1981; 2(8252): 928. https://doi.org/10.1016/S0140-6736(81)91411-2
11. Smith M.S., Swanepoel P.J., Bootsma M. Hepatitis A in nonhuman primates in nature. Lancet. 1980; 2(8206): 1241–2. https://doi.org/10.1016/s0140-6736(80)92495-2
12. Kalter S.S., Heberling R.L., Cooke A.W., Barry J.D., Tian P.Y., Northam W.J. Viral infections of nonhuman primates. Lab. Anim. Sci. 1997; 47(5): 461–8.
13. Purcell R.H., Emerson S.U. Animal models of hepatitis A and E. ILAR J. 2001; 42(2): 161–77. https://doi.org/10.1101/cshperspect.a031815
14. Korzaya L.I., Lapin B.A., Shevtsova Z.V., Krilova R.I. Spontaneous and experimental hepatitis A in Old World monkeys are the models of human hepatitis A. Baltic J. Lab. Animal. Sci. 2001; 11(2): 135–41.
15. Dogadov D.I., Korzaya L.I., Kyuregyan K.K., Karlsen A.A., Mikhailov M.I., Lapin B.A. Markery gepatita A u obez'yan Adlerskogo primatologicheskogo tsentra. Voprosy virusologii. 2019; 64(5): 246–9. https://doi.org/10.36233/0507-4088-2019-64-5-246-249
16. Korzaya L.I., Keburiya V.V., Goncharenko A.M., Dogadov D.I., Lapin B.A. Markery virusnykh infektsii u laboratornykh primatov. V kn.: Materialy vtoroi mezhdunarodnoi nauchnoi konferentsii «Fundamental'nye i prikladnye aspekty meditsinskoi primatologii». Sochi; 2011: 79–88.
17. Drewe J.A., O’Riain M.J., Beamish E., Currie H., Parsons S. Survey of infections transmissible between baboons and humans, Cape Town, South Africa. Emerg. Infect. Dis. 2012; 18(2): 298–301. https://doi.org/10.3201/eid1802.111309
18. Gust I.D., Lehmann N.I., Crowe S., McCrorie M., Locarnini S.A., Lucas C.R. The origin of the HM175 strain of hepatitis A virus. J. Infect. Dis. 1985; 151(2): 365–7. https://doi.org/10.1093/infdis/151.2.365
19. Balayan M.S., Kusov Yu.Yu., Andjaparidze A.G., Tsarev S.A., Sverdlov E.D., Chizhikov V.E., et al. Variations in genome fragments coding for RNA polymerase in human and simian hepatitis A viruses. FEBS Lett. 1989; 247(2): 425–8. https://doi.org/10.1016/0014-5793(89)81384-5
20. Nainan O.V., Margolis H.S., Robertson B.H., Balayan M., Brinton M.A. Sequence analysis of a new hepatitis A virus naturally infecting cynomolgus macaques (Macaca fascicularis). J. Gen. Virol. 1991; 72(7): 1685–9. https://doi.org/10.1099/0022-1317-72-7-1685
21. Van Cuyck-Gandré H., Cockman-Thomas R., Caudill J.D., Asher L.S., Armstrong K.L., Hauroeder B., et al. Experimental African HEV infection in cynomolgus macaques (Macaca fascicularis). J. Med. Virol. 1998; 55(3): 197–202. https://doi.org/10.1002/(SICI)1096-9071(199807)55:3<197::AID-JMV3>3.0.CO;2-X
22. Lu L., Ching K.Z., de Paula V.S., Nakano T., Siegl G., Weitz M., et al. Characterization of the complete genomic sequence of genotype II hepatitis A virus (CF53/Berne isolate). J. Gen. Viro. 2004; 85(10): 2943–52. https://doi.org/10.1099/vir.0.80304-0
23. Cristina J., Costa-Mattioli M. Genetic variability and molecular evolution of hepatitis A virus. Virus Res. 2007; 127(2): 127–57. https://doi.org/10.1016/j.virusres.2007.01.005
24. Costa-Mattioli M., Di Napoli A., Ferre V., Billaudel S., Perez-Bercoff R., Cristina J. Genetic variability of hepatitis A virus. J. Gen. Virol. 2003; 84(Pt. 12): 3191–201. https://doi.org/10.1099/vir.0.19532-0
25. Khanna B., Spelbring J.E., Innis B.L., Robertson B.H. Characterization of a genetic variant of human hepatitis A virus. J. Med. Virol. 1992; 36(2): 118–24. https://doi.org/10.1002/jmv.1890360208
26. Lemon S.M., LeDuc J.W., Binn L.N., Escajadillo A., Ishak K.G. Transmission of hepatitis A virus among recently captured Panamanian owl monkeys. J. Med. Virol. 1982; 10(1): 25–36. https://doi.org/10.1002/jmv.1890100105
27. Andzhaparidze A.G., Karetnyi Yu.V., Korzaya L.I., Balayan M.S., Titova I.P., Zamyatina N.A. Epizootiya gepatita A sredi afrikanskikh zelenykh martyshek, soderzhashchikhsya v usloviyakh vivariya. Voprosy virusologii. 1989; 34(3): 292–6.
28. Arankalle V.A., Ramakrishnan J. Simian hepatitis A virus derived from a captive rhesus monkey in India is similar to the strain isolated from wild African green monkeys in Kenya. J. Viral. Hepat. 2009; 16(3): 214–8. https://doi.org/10.1111/j.1365-2893.2008.01060.x
29. Bennett A.J., Sibley S.D., Lauck M., Weny G., Hyeroba D., Tumukunde A., et al. Naturally circulating Hepatitis A virus in olive baboons, Uganda. Emerg. Infect. Dis. 2016; 22(7): 1308–10. https://doi.org/10.3201/eid2207.151837
30. Dogadov D.I., Korzaya L.I., Karlsen A.A., Kyuregyan K.K. Molecular genetic identification of isolates of the hepatitis A virus (HAV) from monkeys at Adler primate center. J. Med. Primatol. 2018; 47(2): 87–92. https://doi.org/10.1111/jmp.12333
31. Andzhaparidze A.G., Poleshchuk V.F., Zamyatina N.A., Savinov A.P., Gavrilovskaya I.N., Balayan M.S. Spontannyi gepatit u yavanskoi makaki, podvergnutoi vozdeistviyu immunodepressantov. Voprosy virusologii. 1985; (4-S): 468–73.
32. Tsarev S.A., Emerson S.U., Balayan M.S., Ticehurst J., Purcel R.H. Simian hepatitis A virus (HAV) strain AGM-27: comparison of genome structure and growth in cell culture with other HAV strains. J. Gen. Virol. 1991; 72(7): 1677–83. https://doi.org/10.1099/0022-1317-72-7-1677
33. Raychaudhuri G., Govindarajan S., Shapiro M., Purcell R.H., Emerson S.U. Utilization of chimeras between human (HM-175) and simian (AGM-27) strains of hepatitis A virus to study the molecular basis of virulence. J. Virol. 1998; 7(4): 7467–75. https://doi.org/10.1128/JVI.72.9.7467-7475.1998
34. Lapin B.A., Dzhikidze E.K., Krylova R.I., Stasilevich Z.K., Yakovleva L.A. Problemy infektsionnoi patologii obez'yan. M.: RAMN; 2004.
35. Poleshchuk V.F., Balayan M.S., Andzhaparidze A.G., Sobol' A.V., Dokin V.P., Gulyaeva T.V. i dr. Modelirovanie gepatita A i enteral'no peredayushchegosya gepatita ni A ni V (gepatit E) na tamarinakh Saguinus mystax. Voprosy virusologii. 1990; 35(5): 379–82.
36. Poleshchuk V.F., Mikhailov M.I., Zamyatina N.A. Primatnye modeli virusnykh gepatitov cheloveka. Voprosy virusologii. 2006; 51(4): 6–13.
37. ICTV. International Committee on Taxonomy of Viruses. Genus: Hepeviridae; 2021. Available at: https://talk.ictvonline.org/ictv-reports/ictv_online_report/positive-sense-rna-viruses/w/hepeviridae
38. Balayan M.S., Andjaparidze A.G., Savinskaya S.S., Ketiladze E.S., Braginsky D.M., Savinov A.P., et al. Evidence for a virus in non-A, non-B hepatitis transmitted via the fecal-oral route. Intervirology. 1983; 20(1): 23–31. https://doi.org/10.1159/000149370
39. Hirano M., Ding X., Li T.C., Takeda N., Kawabata H., Koizumi N., et al. Evidence for widespread infection of hepatitis E virus among wild rats in Japan. Hepatol. Res. 2003; 27(1): 1–5. https://doi.org/10.1016/S1386-6346(03)00192-X
40. Nakamura S., Tsuchiya H., Okahara N., Nakagawa T., Ohara N., Yamamoto H., et al. Epidemiology of hepatitis E virus in indoor-captive cynomolgus monkey colony. J. Vet. Med. Sci. 2012; 74(3): 279–83. https://doi.org/10.1292/jvms.11-0394
41. Yamamoto H., Li T.C., Koshimoto C., Ito K., Kita M., Miyashita N., et al. Serological evidence for hepatitis E virus infection in laboratory monkeys and pigs in animal facilities in Japan. Exp. Anim. 2008; 57(4): 367–76. https://doi.org/10.1538/expanim.57.367
42. Korzaya L.I., Keburiya V.V., Dogadov D.I., Lapin B.A., Kyuregyan K.K., Mikhailov M.I. Markery gepatita E u naseleniya Bol'shogo Sochi i obez'yan Adlerskogo primatologicheskogo tsentra. Voprosy virusologii. 2016; 61(4): 176–80. https://doi.org/10.18821/0507-4088-2016-61-4-176-180
43. Korzaya L.I., Dogadov D.I., Goncharenko A.M., Karlsen A.A., Kyuregyan K.K., Mikhailov M.I. Rasprostranenie markerov respiratornykh virusov cheloveka sredi obez'yan Adlerskogo primatologicheskogo tsentra. Voprosy virusologii. 2021; 66(6): 425–33. https://doi.org/10.36233/0507-4088-77
44. Yamamoto H., Suzuki J., Matsuda A., Ishida T., Ami Y., Suzaki Y., et al. Hepatitis E virus outbreak in monkey facility, Japan. Emerg. Infect. Dis. 2012; 18(12): 2032–4. https://doi.org/10.3201/eid1812.120884
45. Huang F., Yu W., Hua X., Jing S., Zeng W., He Z. Seroepidemiology and molecular characterization of hepatitis E virus in Macaca Mulatta from a village in Yunnan, China, where infection with this virus is endemic. Hepat. Mon. 2011; 11(9): 745–9. https://doi.org/10.5812/kowsar.1735143X.730
46. Yang F., Duan S., Guo Y., Li Y., Yoshizaki S., Takeda N., et al. Current status of hepatitis E virus infection at a rhesus monkey farm in China. Vet. Microbiol. 2019; 230: 244–8. https://doi.org/10.1016/j.vetmic.2019.01.021
47. Dogadov D.I., Korzaya L.I., Kyuregyan K.K., Karlsen A.A., Kichatova V.S., Potemkin I.A., et al. Natural infection of captive cynomolgus monkeys (Macaca fascicularis) with hepatitis E virus genotype 4. Arch. Virol. 2019; 164(10): 2515–8. https://doi.org/10.1007/s00705-019-04337-3
48. Kyuregyan K.K., Poleshchuk V.F., Gordeichuk I.V., Gulyaeva T.V., Isaeva O.V., Morozov I.A. i dr. Modelirovanie virusnogo gepatita E na igrunkovykh obez'yanakh. Byulleten' eksperimen- tal'noi biologii i meditsiny. 2015; 160(9): 355–9. https://doi.org/10.1007/s10517-016-3173-0
49. Gordeychuk I., Kyuregyan K., Kondrashova A., Bayurova E., Gulyaev S., Gulyaeva T., et al. Immunization with recombinant ORF2 p551 protein protects common marmosets (Callithrix jacchus) against homologous and heterologous hepatitis E virus challenge. Vaccine. 2022; 40(1): 89–99. https://doi.org/10.1016/j.vaccine.2021.11.042
50. Longer C.F., Denny S.L., Caudill J.D., Miele T.A., Asher L.V., Myint K.S., et al. Experimental hepatitis E: pathogenesis in cynomolgus macaques (Macaca fascicularis). J. Infect. Dis. 1993; 168(3): 602–9. https://doi.org/10.1093/infdis/168.3.602
51. Van Cuyck-Gandré H., Cockman-Thomas R., Caudill J.D., Asher L.S., Armstrong K.L., Hauroeder B., et al. Experimental African HEV infection in cynomolgus macaques (Macaca fascicularis). J. Med. Virol. 1998; 55(3): 197–202. https://doi.org/10.1002/(SICI)1096-9071(199807)55:3<197::AID-JMV3>3.0.CO;2-X
52. Tsarev S.A., Tsareva T.S., Emerson S.U., Rippy M.K., Zack P., Shapiro M., et al. 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. 1995; 172(1): 31–7. https://doi.org/10.1093/infdis/172.1.31
53. de Carvalho L.G., Marchevsky R.S., dos Santos D.R., de Oliveira J.M., de Paula V.S., Lopes L.M., et al. Infection by Brazilian and Dutch swine hepatitis E virus strains induces haematological changes in Macaca fascicularis. BMC Infect. Dis. 2013; 13(495): 495. https://doi.org/10.1186/1471-2334-13-495
54. Purcell R.H., Engle R.E., Rood M.P., Kabrane-Lazizi Y., Nguyen H.T., Govindarajan S., et al. Hepatitis E virus in rats, Los Angeles, California, USA. Emerg. Infect. Dis. 2011; 17(12): 2216–22. https://doi.org/10.3201/eid1712.110482
55. Yang F., Li Y., Li Y., Jin W., Duan S., Xu H., et al. Experimental Cross-Species Transmission of Rat Hepatitis E Virus to Rhesus and Cynomolgus Monkeys. Viruses. 2022; 14(2): 293. https://doi.org/10.3390/v14020293
56. Huang F.F., Sun Z.F., Emerson S.U., Purcell R.H. 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. 2004; 85(6): 1609–18. https://doi.org/10.1099/vir.0.79841-0
57. Mikhailov M.I., Kyuregyan K.K., Gruzdeva K.N. Virus gepatita E ptits. Mir virusnykh gepatitov. 2005; (10): 8–11.
