Advertisement

The Role of Emerging and Neglected Viruses in the Etiology of Hepatitis

  • Anna MrzljakEmail author
  • Irena Tabain
  • Hrvoje Premac
  • Maja Bogdanic
  • Ljubo Barbic
  • Vladimir Savic
  • Vladimir Stevanovic
  • Ana Jelic
  • Danko Mikulic
  • Tatjana Vilibic-Cavlek
Intra-Abdominal Infections, Hepatitis and Gastroenteritis (T Steiner, Section Editor)
Part of the following topical collections:
  1. Topical Collection on Intra-abdominal Infections, Hepatitis, and Gastroenteritis

Abstract

Purpose of Review

In this review, we present the overview of emerging and neglected viruses associated with liver involvement.

Recent Findings

Hepatitis E virus (HEV) emerged in the last two decades, causing hepatitis in many parts of the world. Moreover, liver involvement was also described in some emerging arboviral infections. Many reports showed dengue-associated liver injury; however, chikungunya, West Nile, tick-borne encephalitis, and Zika virus are rarely associated with clinically manifest liver disease. In addition, some neglected highly prevalent viruses such as adenoviruses and parvovirus B19 are capable of causing hepatitis in specific population groups. Anelloviruses (torque teno virus/torque teno mini virus/torque teno midi virus, SEN virus), human bocavirus, pegiviruses, and lymphocytic choriomeningitis virus have shown a little potential for causing hepatitis, but their role in the etiology of liver disease remains to be determined.

Summary

In addition to the well-known hepatotropic viruses, many emerging and neglected viruses have been associated with liver diseases. The number of emerging zoonotic viruses has been increasingly recognized. While zoonotic potential of HEV is well documented, the recent identification of new hepatitis-related animal viruses such as HEV strains from rabbits and camels, non-primate hepaciviruses in domestic dogs and horses, as well as equine and porcine pegivirus highlights the possible zoonotic transmission in the context of “One Health.” However, zoonotic potential and hepatotropism of animal hepatitis viruses remain to be determined.

Keywords

Hepatotropic viruses Hepatitis E virus Arboviruses Adenoviruses Parvovirus B19 Anelloviruses Human bocavirus Pegiviruses Arenaviruses 

Notes

Funding Information

This study was supported in part by the Croatian Science Foundation, project no. HRZZ IP 2016-06-7456: Prevalence and Molecular Epidemiology of Emerging and Re-emerging Neuroinvasive Arboviral Infections in Croatia; CRONEUROARBO (to TVC).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

  1. 1.
    Vine LJ, Dalton HR. Hepatitis E, A and other hepatotropic viruses. Medicine. 2015;43(10):594–8.Google Scholar
  2. 2.
    Mellinger JL, Rossaro L, Naugler WE, Nadig SN, Appelman H, Lee WM, et al. Epstein-Barr virus (EBV) related acute liver failure: a case series from the US Acute Liver Failure Study Group. Dig Dis Sci. 2014;59(7):1630–7.PubMedPubMedCentralGoogle Scholar
  3. 3.
    Serna-Higuera C, González-García M, Milicua JM, Muñoz V. Acute cholestatic hepatitis by cytomegalovirus in an immunocompetent patient. J Clin Gastroenterol. 1999;29(3):276–7.PubMedGoogle Scholar
  4. 4.
    Saha AK, Maitra S, Hazra SC. Spectrum of hepatic dysfunction in 2012 dengue epidemic in Kolkata, West Bengal. Indian J Gastroenterol. 2013;32:400–3.PubMedGoogle Scholar
  5. 5.
    Ahmed F. Dengue and the liver. SM J Hepat Res Treat. 2015;1(1):1002–6.Google Scholar
  6. 6.
    Bowman S, Salgado C, DeWaay DJ. Dengue fever presenting with hepatitis. Am J Med Sci. 2012;344(4):335–6.PubMedGoogle Scholar
  7. 7.
    Gandhi K, Shetty M. Profile of liver function test in patients with dengue infection in South India. Med J DY Patil Univ. 2013;6:370–2.Google Scholar
  8. 8.
    Georges AJ, Lesbordes JL, Georges-Courbot MC, Meunier DMY, Gonzalez JP. Fatal hepatitis from West Nile virus. Ann Inst Pasteur Virol. 1987;138:237–44.Google Scholar
  9. 9.
    Paddock CD, Nicholson WL, Bhatnagar J, Goldsmith CS, Greer PW, Hayes EB, et al. Fatal hemorrhagic fever caused by West Nile virus in the United States. Clin Infect Dis. 2006;42(11):1527–35.PubMedGoogle Scholar
  10. 10.
    Lotric-Furlan S, Strle F. Thrombocytopenia, leukopenia and abnormal liver function tests in the initial phase of tick-borne encephalitis. Zbl Bakt. 1995;282:275–8.Google Scholar
  11. 11.
    Mišić-Majerus L, Bujić N, Madarić V, Avšič-Zupanc T. Hepatitis caused by tick-borne meningoencephalitis virus (TBEV)—a rare clinical manifestation outside the central nervous system involvement. Acta Med Croatica. 2005;59(4):347–52.PubMedGoogle Scholar
  12. 12.
    Wiwanitkit V. Hepatic disorder in Zika virus infection. Hepatoma Res. 2016;2:203–4.Google Scholar
  13. 13.
    Wu Y, Cui X, Wu N, Song R, Yang W, Zhang W, et al. A unique case of human Zika virus infection in association with severe liver injury and coagulation disorders. Sci Rep. 2017;7(1):11393.PubMedPubMedCentralGoogle Scholar
  14. 14.
    Perez D, McCormack L, Petrowsky H, Jochum W, Mullhaupt B, Clavien PA. Successful outcome of severe adenovirus hepatitis of the allograft following liver transplantation. Transpl Infect Dis. 2007;9:318–22.PubMedGoogle Scholar
  15. 15.
    Steiner I, Aebi C, Ridolfi Lüthy A, Wagner B, Leibundgut K. Fatal adenovirus hepatitis during maintenance therapy for childhood acute lymphoblastic leukemia. Pediatr Blood Cancer. 2008;50:647–9.PubMedGoogle Scholar
  16. 16.
    Schaberg KB, Kambham N, Sibley RK, Higgins JPT. Adenovirus hepatitis: clinicopathologic analysis of 12 consecutive cases from a single institution. Am J Surg Pathol. 2017;41(6):810–9.PubMedGoogle Scholar
  17. 17.
    Islek A, Keskin H, Agın M, Aksungur N, Korkut E, Ozturk G. Parvovirus B19 infection as a rare cause of fulminant liver failure: a case report. Transplant Proc. 2019;51(4):1169–71.PubMedGoogle Scholar
  18. 18.
    Kamar N, Bendall R, Legrand-Abravanel F, Xia NS, Ijaz S, Izopet J, et al. Hepatitis E. Lancet. 2012;379:2477–88.PubMedGoogle Scholar
  19. 19.
    Kumar A, Beniwal M, Kar P, Sharma JB, Murthy NS. Hepatitis E in pregnancy. Int J Gynaecol Obstet. 2004;85:240–4.PubMedGoogle Scholar
  20. 20.
    Kumar Acharya S, Kumar Sharma P, Singh R, Kumar Mohanty S, Madan K, Kumar Jha J, et al. Hepatitis E virus (HEV) infection in patients with cirrhosis is associated with rapid decompensation and death. J Hepatol. 2007;46:387–94.PubMedGoogle Scholar
  21. 21.
    Teshale EH, Howard CM, Grytdal SP, Handzel TR, Barry V, Kamili S, et al. Hepatitis E epidemic, Uganda. Emerg Infect Dis. 2010;16:126–9.PubMedGoogle Scholar
  22. 22.
    Dalton HR, Stableforth W, Thurairajah P, Hazeldine S, Remnarace R, Usama W, et al. Autochthonous hepatitis E in Southwest England: natural history, complications and seasonal variation, and hepatitis E virus IgG seroprevalence in blood donors, the elderly and patients with chronic liver disease. Eur J Gastroenterol Hepatol. 2008;20:784–90.PubMedGoogle Scholar
  23. 23.
    Blasco-Perrin H, Madden RG, Stanley A, Crossan C, Hunter JG, Vine L, et al. Hepatitis E virus in patients with decompensated chronic liver disease: a prospective UK/French study. Aliment Pharmacol Ther. 2015;42:574–81.PubMedGoogle Scholar
  24. 24.
    Kamar N, Selves J, Mansuy JM, Ouezzani L, Péron JM, Guitard J, et al. Hepatitis E virus and chronic hepatitis in organ-transplant recipients. N Engl J Med. 2008;358:811–7.PubMedGoogle Scholar
  25. 25.
    Dalton HR, Bendall RP, Keane FE, Tedder RS, Ijaz S. Persistent carriage of hepatitis E virus in patients with HIV infection. N Engl J Med. 2009;361:1025–7.  https://doi.org/10.1056/NEJMc0903778.CrossRefPubMedGoogle Scholar
  26. 26.
    von Felden J, Alric L, Pischke S, Aitken C, Schlabe S, Spengler U, et al. The burden of hepatitis E among patients with hematological malignancies: a retrospective European cohort study. J Hepatol. 2019;71(3):465–472.Google Scholar
  27. 27.
    Kamar N, Garrouste C, Haagsma EB, Garrigue V, Pischke S, Chauvet C, et al. Factors associated with chronic hepatitis in patients with hepatitis E virus infection who have received solid organ transplants. Gastroenterology. 2011;140:1481–9.PubMedGoogle Scholar
  28. 28.
    Galante A, Adeyi O, Lau L, Humar A, Galvin Z, Selzner N, et al. Liver transplantation for acute liver failure due to dengue fever: first successful reported case worldwide. Hepatology. 2019.  https://doi.org/10.1002/hep.30803.PubMedGoogle Scholar
  29. 29.
    Poovorawan Y, Hutagalung Y, Chongsrisawat V, Boudville I, Bock HL. Dengue virus infection: a major cause of acute hepatic failure in Thai children. Ann Trop Paediatr. 2006;26(1):17–23.PubMedGoogle Scholar
  30. 30.
    Chongsrisawat V, Hutagalung Y, Poovorawan Y. Liver function test results and outcomes in children with acute liver failure due to dengue infection. Southeast Asian J Trop Med Public Health. 2009;40:47–53.PubMedGoogle Scholar
  31. 31.
    Fabre A, Couvelard A, Degott C, Lagorce-Pagès C, Bruneel F, Bouvet E, et al. Dengue virus induced hepatitis with chronic calcific changes. Gut. 2001;49(6):864–5.PubMedPubMedCentralGoogle Scholar
  32. 32.
    Staples JE, Breiman RF, Powers AM. Chikungunya fever: an epidemiological review of a re-emerging infectious disease. Clin Infect Dis. 2009;49(6):942–8.PubMedGoogle Scholar
  33. 33.
    Garnier P, Blanchet E, Reix G, Kwiatek S, Reboux A, Huguenin B, et al. Severe acute hepatitis during Chikungunya virus infection on Reunion Island: case report from 14 observations. J Clin Virol. 2006;36(2):S60.Google Scholar
  34. 34.
    Economopoulou A, Dominguez M, Helynck B, Sissoko D, Wichmann O, Quenel P, et al. Atypical Chikungunya virus infections: clinical manifestations, mortality and risk factors for severe disease during the 2005–2006 outbreak on Reunion. Epidemiol Infect. 2009;137:534–41.PubMedGoogle Scholar
  35. 35.
    Chua HH, Abdul Rashid K, Law WC, Hamizah A, Chem YK, Khairul AH, et al. A fatal case of chikungunya virus infection with liver involvement. Med J Malaysia. 2010;65(1):83–4.PubMedGoogle Scholar
  36. 36.
    Bonifay T, Prince C, Neyra C, Demar M, Rousset D, Kallel H, et al. Atypical and severe manifestations of chikungunya virus infection in French Guiana: a hospital-based study. PLoS One. 2018;13(12):e0207406.PubMedPubMedCentralGoogle Scholar
  37. 37.
    Gyure KA. West Nile virus infections. J Neuropathol Exp Neurol. 2009;68(10):1053–60.PubMedGoogle Scholar
  38. 38.
    Özbay Hoşnut F, Canan O, Özçay F, Bilezikçi B. Adenovirus infection as possible cause of acute liver failure in a healthy child: a case report. Turk J Gastroenterol. 2008;19(4):281–3.PubMedGoogle Scholar
  39. 39.
    Ronan BA, Agrwal N, Carey EJ, De Petris G, Kusne S, Seville MT, et al. Fulminant hepatitis due to human adenovirus. Infection. 2014;42:105–11.PubMedGoogle Scholar
  40. 40.
    Peled N, Nakar C, Huberman H, Scherf E, Samra Z, Finkelstein Y, et al. Adenovirus infection in hospitalized immunocompetent children. Clin Pediatr (Phila). 2004;43(3):223–9.Google Scholar
  41. 41.
    Bihari C, Rastogi A, Saxena P, Rangegowda D, Chowdhury A, Gupta N, et al. Parvovirus B19 associated hepatitis. Hepat Res Treat. 2013;2013:472027.PubMedPubMedCentralGoogle Scholar
  42. 42.
    Lukashevich IS, Rodas JD, Tikhonov II, Zapata JC, Yang Y, Djavani M, et al. LCMV-mediated hepatitis in rhesus macaques: WE but not ARM strain activates hepatocytes and induces liver regeneration. Arch Virol. 2004;149(12):2319–36.PubMedPubMedCentralGoogle Scholar
  43. 43.
    Yun NE, Walker DH. Pathogenesis of Lassa fever. Viruses. 2012;4(10):2031–48.PubMedPubMedCentralGoogle Scholar
  44. 44.
    Beier JI, Jokinen JD, Holz GE, Whang PS, Martin AM, Warner NL, et al. Novel mechanism of arenavirus-induced liver pathology. PLoS One. 2015;10(3):e0122839.PubMedPubMedCentralGoogle Scholar
  45. 45.
    Kamal SM, Mahmoud S, Hafez T, El-Fouly R. Viral hepatitis A to E in South Mediterranean countries. Mediterr J Hematol Infect Dis. 2010;2(1):e2010001.PubMedPubMedCentralGoogle Scholar
  46. 46.
    Pavio N, Meng XJ, Doceul V. Zoonotic origin of hepatitis E. Curr Opin Virol. 2015;10:34–41.PubMedGoogle Scholar
  47. 47.
    Clemente-Casares P, Pina S, Buti M, Jardi R, MartIn M, Bofill-Mas S, et al. Hepatitis E virus epidemiology in industrialized countries. Emerg Infect Dis. 2003;9(4):448–54.PubMedGoogle Scholar
  48. 48.
    De Schryver A, De Schrijver K, François G, Hambach R, van Sprundel M, Tabibi R, et al. Hepatitis E virus infection: an emerging occupational risk? Occup Med (Lond). 2015;65(8):667–72.Google Scholar
  49. 49.
    Baylis SA, Gärtner T, Nick S, Ovemyr J, Blümel J. Occurrence of hepatitis E virus RNA in plasma donations from Sweden, Germany and the United States. Vox Sang. 2012;103(1):89–90.PubMedGoogle Scholar
  50. 50.
    Schlosser B, Stein A, Neuhaus R, Pahl S, Ramez B, Krüger DH, et al. Liver transplant from a donor with occult HEV infection induced chronic hepatitis and cirrhosis in the recipient. J Hepatol. 2012;56(2):500–2.PubMedGoogle Scholar
  51. 51.
    World Health Organization. Dengue. Available at: www.who.int/denguecontrol/en/. Accessed 2 June 2019.
  52. 52.
    Ling LM, Wilder-Smith A, Leo YS. Fulminant hepatitis in dengue hemorrhagic fever. J Clin Virol. 2007;38:265–8.PubMedGoogle Scholar
  53. 53.
    de Souza LJ, Nogueira RM, Soares LC, Soares CE, Ribas BF, Alves FP, et al. The impact of dengue on liver function as evaluated by aminotransferase levels. Braz J Infect Dis. 2007;11(4):407–10.PubMedGoogle Scholar
  54. 54.
    de Souza LJ, Goncalves Carneiro H, Souto Filho JT, Ferreira de Souza T, Azevedo Cortes V, Neto CG, et al. Hepatitis in dengue shock syndrome. Braz J Infect Dis. 2002;6(6):322–7.PubMedGoogle Scholar
  55. 55.
    Jagadishkumar K, Jain P, Manjunath VG, Umesh L. Hepatic involvement in dengue fever in children. Iran J Pediatr. 2012;22(2):231–6.PubMedPubMedCentralGoogle Scholar
  56. 56.
    Powers AM, Brault AC, Tesh RB, Weaver SC. Re-emergence of chikungunya and o’nyong-nyong viruses: evidence for distinct geographical lineages and distant evolutionary relationships. J Gen Virol. 2000;81:471–9.PubMedGoogle Scholar
  57. 57.
    Darrigo LG Jr, de Sant’Anna Carvalho AM, Machado CM. Chikungunya, dengue, and Zika in immunocompromised hosts. Curr Infect Dis Rep. 2018;20(4):5.PubMedPubMedCentralGoogle Scholar
  58. 58.
    Rizzoli A, Jimenez-Clavero MA, Barzon L, Cordioli P, Figuerola J, Koraka P, et al. The challenge of West Nile virus in Europe: knowledge gaps and research priorities. Euro Surveill. 2015;20(20):21135.PubMedGoogle Scholar
  59. 59.
    Sejvar JJ. West Nile virus infection. Microbiol Spectr. 2016;4(3).  https://doi.org/10.1128/microbiolspec.EI10-0021-2016.
  60. 60.
    Haberle S. Case series of the patients with severe neuroinvasive West Nile virus infection treated at the University Hospital for Infections Diseases “Dr Fran Mihaljević”, Zagreb. Graduate thesis. School of Medicine, University of Zagreb, 2019.Google Scholar
  61. 61.
    Beaver JT, Lelutiu N, Habib R, Skountzou I. Evolution of two major Zika virus lineages: implications for pathology, immune response, and vaccine development. Front Immunol. 2018;9:1640.PubMedPubMedCentralGoogle Scholar
  62. 62.
    Sherman KE, Rouster SD, Kong LX, Aliota MT, Blackard JT, Dean GE. Zika virus replication and cytopathic effects in liver cells. PLoS One. 2019;14(3):e0214016.PubMedPubMedCentralGoogle Scholar
  63. 63.
    Dowall SD, Graham VA, Rayner E, Atkinson B, Hall G, Watson RJ, et al. A susceptible mouse model for Zika virus infection. PLoS Negl Trop Dis. 2016;10:e0004658.PubMedPubMedCentralGoogle Scholar
  64. 64.
    Bogovic P, Strle F. Tick-borne encephalitis: a review of epidemiology, clinical characteristics, and management. World J Clin Cases. 2015;3(5):430–41.PubMedPubMedCentralGoogle Scholar
  65. 65.
    McKillop SJ, Belletrutti MJ, Lee BE, Yap JY, Noga ML, Desai SJ, et al. Adenovirus necrotizing hepatitis complicating atypical teratoid rhabdoid tumor. Pediatr Int. 2015;57:974–7.PubMedGoogle Scholar
  66. 66.
    Matoq A, Salahuddin A. Acute hepatitis and pancytopenia in healthy infant with adenovirus. Case Rep Pediatr. 2016;2016:8648190.PubMedPubMedCentralGoogle Scholar
  67. 67.
    Khameneh ZR, Hanifian H, Barzegari R, Sepehrvand N. Human parvovirus B19 in Iranian pregnant women: a serologic survey. Indian J Pathol Microbiol. 2014;57(3):442–4.  https://doi.org/10.4103/0377-4929.138748.CrossRefPubMedGoogle Scholar
  68. 68.
    Qiu J, Söderlund-Venermo M, Young NS. Human parvoviruses. Clin Microbiol Rev. 2017;30(1):43–113.PubMedGoogle Scholar
  69. 69.
    Wang C, Heim A, Schlaphoff V, Suneetha PV, Stegmann KA, Jiang H, et al. Intrahepatic long-term persistence of parvovirus B19 and its role in chronic viral hepatitis. J Med Virol. 2009;81(12):2079–88.PubMedGoogle Scholar
  70. 70.
    MacNeil A, Ströher U, Farnon E, Campbell S, Cannon D, Paddock CD, et al. Solid organ transplant–associated lymphocytic choriomeningitis, United States, 2011. Emerg Infect Dis. 2012;18(8):1256–62.PubMedPubMedCentralGoogle Scholar
  71. 71.
    Schafer IJ, Miller R, Ströher U, Knust B, Nichol ST, Rollin PE. Notes from the field: a cluster of lymphocytic choriomeningitis virus infections transmitted through organ transplantation-Iowa, 2013. Am J Transplant. 2014;14(6):1459.PubMedGoogle Scholar
  72. 72.
    Allander T, Tammi MT, Eriksson M, Bjerkner A, Tiveljung-Lindell A, Andersson B. Cloning of a human parvovirus by molecular screening of respiratory tract samples. Proc Natl Acad Sci U S A. 2005;102:12891–6.PubMedPubMedCentralGoogle Scholar
  73. 73.
    Kapoor A, Slikas E, Simmonds P, Chieochansin T, Naeem A, Shaukat S, et al. A newly identified bocavirus species in human stool. J Infect Dis. 2009;199(2):196–200.PubMedPubMedCentralGoogle Scholar
  74. 74.
    Arthur JL, Higgins GD, Davidson GP, Givney RC, Ratcliff RM. A novel bocavirus associated with acute gastroenteritis in Australian children. PLoS Pathog. 2009;5(4):e1000391.PubMedPubMedCentralGoogle Scholar
  75. 75.
    Allander T, Jartti T, Gupta S, Niesters HG, Lehtinen P, Osterback R, et al. Human bocavirus and acute wheezing in children. Clin Infect Dis. 2007;44(7):904–10.PubMedGoogle Scholar
  76. 76.
    Haytoğlu Z, Canan O. Bocavirus viremia and hepatitis in an immunocompetent child. Balkan Med J. 2017;34(3):281–3.PubMedPubMedCentralGoogle Scholar
  77. 77.
    Kainulainen L, Waris M, Söderlund-Venermo M, Allander T, Hedman K, Ruuskanen O. Hepatitis and human bocavirus primary infection in a child with T-cell deficiency. J Clin Microbiol. 2008;46:4104–5.PubMedPubMedCentralGoogle Scholar
  78. 78.
    Tong R, Zhou WM, Liu XJ, Wang Y, Lou YL, Tan WJ. Detection of human parvovirus B19, human bocavirus and human parvovirus 4 infections in blood samples among 95 patients with liver disease in Nanjing by nested PCR. Zhonghua Shi Yan He Lin Chuang Bing Du Xue Za Zhi. 2013;27(2):135–7.PubMedGoogle Scholar
  79. 79.
    Simons JN, Leary TP, Dawson GJ, Pilot-Matias TJ, Muerhoff AS, Schlauder GG, et al. Isolation of novel virus-like sequences associated with human hepatitis. Nat Med. 1995;1(6):564–9.PubMedGoogle Scholar
  80. 80.
    Mohr EL, Stapleton JT. GB virus type C interactions with HIV: the role of envelope glycoproteins. J Viral Hepat. 2009;16:757–68.PubMedPubMedCentralGoogle Scholar
  81. 81.
    Chivero ET, Stapleton JT. Tropism of human pegivirus (formerly known as GB virus C/hepatitis G virus) and host immunomodulation: insights into a highly successful viral infection. J Gen Virol. 2015;96(Pt 7):1521–32.PubMedPubMedCentralGoogle Scholar
  82. 82.
    Williams CF, Klinzman D, Yamashita TE, Xiang J, Polgreen PM, Rinaldo C, et al. Persistent GB virus C infection and survival in HIV-infected men. N Engl J Med. 2004;350:981–90.PubMedGoogle Scholar
  83. 83.
    Stapleton JT, Foung S, Muerhoff AS, Bukh J, Simmonds P. The GB viruses: a review and proposed classification of GBV-A, GBV-C (HGV), and GBV-D in genus Pegivirus within the family Flaviviridae. J Gen Virol. 2011;92:233–46.PubMedPubMedCentralGoogle Scholar
  84. 84.
    Berg MG, Lee D, Coller K, Frankel M, Aronsohn A, Cheng K, et al. Discovery of a novel human pegivirus in blood associated with hepatitis C virus co-infection. PLoS Pathog. 2015;11:e1005325.PubMedPubMedCentralGoogle Scholar
  85. 85.
    Chandriani S, Skewes-Cox P, Zhong W, Ganem DE, Divers TJ, Van Blaricum AJ, et al. Identification of a previously undescribed divergent virus from the Flaviviridae family in an outbreak of equine serum hepatitis. Proc Natl Acad Sci U S A. 2013;10:E1407–15.Google Scholar
  86. 86.
    Wang H, Wan Z, Xu R, Guan Y, Zhu N, Li J, et al. A novel human pegivirus, HPgV-2 (HHpgV-1), is tightly associated with hepatitis C virus (HCV) infection and HCV/human immunodeficiency virus type 1 coinfection. Clin Infect Dis. 2018;66(1):29–35.PubMedGoogle Scholar
  87. 87.
    Shui J, Liu W, Liang Y, Zhang J, Wan Z, Wang H, et al. Infection of human pegivirus 2 (HPgV-2) is associated with hepatitis C virus but not hepatitis B virus infection in people who inject drugs. J Gen Virol. 2019;100(6):968–74.PubMedGoogle Scholar
  88. 88.
    Kapoor A, Kumar A, Simmonds P, Bhuva N, Singh Chauhan L, Lee B, et al. Virome analysis of transfusion recipients reveals a novel human virus that shares genomic features with hepaciviruses and pegiviruses. MBio. 2015;6:e01466–15.PubMedPubMedCentralGoogle Scholar
  89. 89.
    Nishizawa T, Okamoto H, Konishi K, Yoshizawa H, Miyakawa Y, Mayumi M. A novel DNA virus (TTV) associated with elevated transaminase levels in posttransfusion hepatitis of unknown etiology. Biochem Biophys Res Commun. 1997;241(1):92–7.PubMedGoogle Scholar
  90. 90.
    Spandole S, Cimponeriu D, Berca LM, Mihăescu G. Human anelloviruses: an update of molecular, epidemiological and clinical aspects. Arch Virol. 2015;160(4):893–908.PubMedGoogle Scholar
  91. 91.
    Peng YH, Nishizawa T, Takahashi M, Ishikawa T, Yoshikawa A, Okamoto H. Analysis of the entire genomes of thirteen TT virus variants classifiable into the fourth and fifth genetic groups, isolated from viremic infants. Arch Virol. 2002;147(1):21–41.PubMedGoogle Scholar
  92. 92.
    Hussain T, Manzoor S, Waheed Y, Tariq H, Hanif K. Phylogenetic analysis of torque teno virus genome from Pakistani isolate and incidence of co-infection among HBV/HCV infected patients. Virol J. 2012;9:320.PubMedPubMedCentralGoogle Scholar
  93. 93.
    Mi Z, Yuan X, Pei G, Wang W, An X, Zhang Z, et al. High-throughput sequencing exclusively identified a novel torque teno virus genotype in serum of a patient with fatal fever. Virol Sin. 2014;2:112–8.  https://doi.org/10.1007/s12250-014-3424-z.CrossRefGoogle Scholar
  94. 94.
    Peng J, Fang Y, Zhao X, Peng Y. New prevalence estimate of torque teno virus (TTV) infection in healthy population and patients with chronic viral hepatitis in Jiujiang, China. Virol Sin. 2015;30(3):218–20.PubMedGoogle Scholar
  95. 95.
    Mancuso R, Saresella M, Hernis A, Agostini S, Piancone F, Caputo D, et al. Torque teno virus (TTV) in multiple sclerosis patients with different patterns of disease. J Med Virol. 2013;85(12):2176–83.PubMedGoogle Scholar
  96. 96.
    Rosa AS, Araujo OC, Savassi-Ribas F, Fernandes CA, Coelho HS, Niel C, et al. Prevalence of occult hepatitis B virus infection and torque teno virus infection and their association with hepatocellular carcinoma in chronic hepatitis C patients. Virus Res. 2017;242:166–72.PubMedGoogle Scholar
  97. 97.
    Ohto H, Ujiie N, Takeuchi C, Sato A, Hayashi A, Ishiko H, et al. TT virus infection during childhood. Transfusion. 2002;42(7):892–8.PubMedGoogle Scholar
  98. 98.
    Han TH, Chung JY. Detection of small anellovirus DNA from blood products. Kor J Blood Transfus. 2006;17(2):126–34.Google Scholar
  99. 99.
    Béland K, Dore-Nguyen M, Gagné MJ, Patey N, Brassard J, Alvarez F, et al. Torque teno virus in children who underwent orthotopic liver transplantation: new insights about a common pathogen. J Infect Dis. 2014;209(2):247–54.PubMedGoogle Scholar
  100. 100.
    Ruiz P, Martínez-Picola M, Santana M, Muñoz J, Pérez-Del-Pulgar S, Koutsoudakis G, et al. Torque teno virus is associated with the state of immune suppression early after liver transplantation. Liver Transpl. 2019;25(2):302–10.PubMedGoogle Scholar
  101. 101.
    Primi D, Fiordalisi G, Mantero JL, Mattioli S, Sottini A, Bonelli F, et al. Identification of SEN-V genotypes. World Intellectual Property Organization. Available at: http://ep.espacenet.com. Accessed 2 June 2019.
  102. 102.
    Umemura T, Tanaka Y, Kiyosawa K, Alter HJ, Shih JWK. Observation of positive selection within hypervariable regions of a newly identified DNA virus (SEN virus). FEBS Lett. 2002;510:171–4.PubMedGoogle Scholar
  103. 103.
    Akiba J, Umemura T, Alter HJ, Kojiro M, Tabor E. SEN virus: epidemiology and characteristics of a transfusion-transmitted virus. Transfusion. 2005;45(7):1084–8.PubMedGoogle Scholar
  104. 104.
    Sagir A, Kirschberg O, Heintges T, Erhardt A, Häussinger D. SEN virus infection. Rev Med Virol. 2004;14(3):141–8.PubMedGoogle Scholar
  105. 105.
    Umemura T, Yeo AE, Sottini A, Moratto D, Tanaka Y, Wang Richard YH, et al. SEN virus infection and its relationship to transfusion-associated hepatitis. Hepatology. 2001;33(5):1303–11.PubMedGoogle Scholar
  106. 106.
    Kobayashi N, Tanaka E, Umemura T, Matsumoto A, Iijima T, Higuchi M, et al. Clinical significance of SEN virus infection in patients on maintenance haemodialysis. Nephrol Dial Transplant. 2003;18(2):348–52.PubMedGoogle Scholar
  107. 107.
    Umemura T, Alter HJ, Tanaka E, Yeo AE, Shih JW, Orii K, et al. Association between SEN virus infection and hepatitis C in Japan. J Infect Dis. 2001;184(10):1246–51.PubMedGoogle Scholar
  108. 108.
    Umemura T, Alter HJ, Tanaka E, Orii K, Yeo AE, Shih JW, et al. SEN virus: response to interferon alfa and influence on the severity and treatment response of coexistent hepatitis C. Hepatology. 2002;35(4):953–9.PubMedGoogle Scholar
  109. 109.
    Momosaki S, Umemura T, Scudamore CH, Kojiro M, Alter HJ, Tabor E. SEN virus infection in patients with hepatocellular carcinoma. J Viral Hepat. 2005;12(4):435–8.PubMedGoogle Scholar
  110. 110.
    Yoshida H, Kato N, Shiratori Y, Shao R, Wang Y, Shiina S, et al. Weak association between SEN virus viremia and liver disease. J Clin Microbiol. 2002;40(9):3140–5.PubMedPubMedCentralGoogle Scholar
  111. 111.
    Shibata M, Wang RY, Yoshiba M, Shih JW, Alter HJ, Mitamura K. The presence of a newly identified infectious agent (SEN virus) in patients with liver diseases and in blood donors in Japan. J Infect Dis. 2001;184(4):400–4.PubMedGoogle Scholar
  112. 112.
    Rasche A, Sander AL, Corman VM, Drexler JF. Evolutionary biology of human hepatitis viruses. J Hepatol. 2019;70(3):501–20.PubMedGoogle Scholar
  113. 113.
    Jemeršić L, Keros T, Lj M, Barbić LJ, Vilibić-Čavlek T, Jeličić P, et al. Differences in hepatitis E virus (HEV) presence in naturally infected seropositive domestic pigs and wild boars—confirmation of wild boars having a key role in HEV epidemiology. Vet Arh. 2017;87(6):651–63.Google Scholar
  114. 114.
    Izopet J, Dubois M, Bertagnoli S, Lhomme S, Marchandeau S, Boucher S, et al. Hepatitis E virus strains in rabbits and evidence of a closely related strain in humans, France. Emerg Infect Dis. 2012;18:1274–81.PubMedPubMedCentralGoogle Scholar
  115. 115.
    Woo PC, Lau SK, Teng JL, Tsang AK, Joseph M, Wong EY, et al. New hepatitis E virus genotype in camels, the Middle East. Emerg Infect Dis. 2014;20(6):1044–8.PubMedPubMedCentralGoogle Scholar
  116. 116.
    Burbelo PD, Dubovi EJ, Simmonds P, Medina JL, Henriquez JA, Mishra N, et al. Serology-enabled discovery of genetically diverse hepaciviruses in a new host. J Virol. 2012;86:6171–8.PubMedPubMedCentralGoogle Scholar
  117. 117.
    Kapoor A, Simmonds P, Gerold G, Qaisar N, Jain K, Henriquez JA, et al. Characterization of a canine homolog of hepatitis C virus. Proc Natl Acad Sci U S A. 2011;108:11608–13.PubMedPubMedCentralGoogle Scholar
  118. 118.
    Schlottau K, Fereidouni S, Beer M, Hoffmann B. Molecular identification and characterization of nonprimate hepaciviruses in equines. Arch Virol. 2019;164(2):391–400.PubMedGoogle Scholar
  119. 119.
    Drexler JF, Corman VM, Müller MA, Lukashev AN, Gmyl A, Coutard B, et al. Evidence for novel hepaciviruses in rodents. PLoS Pathog. 2013;9(6):e1003438.PubMedPubMedCentralGoogle Scholar
  120. 120.
    Quan PL, Firth C, Conte JM, Williams SH, Zambrana-Torrelio CM, Anthony SJ, et al. Bats are a major natural reservoir for hepaciviruses and pegiviruses. Proc Natl Acad Sci U S A. 2013;110:8194–9.PubMedPubMedCentralGoogle Scholar
  121. 121.
    Corman VM, Grundhoff A, Baechlein C, Fischer N, Gmyl A, Wollny R, et al. Highly divergent hepaciviruses from African cattle. J Virol. 2015;89:5876–82.PubMedPubMedCentralGoogle Scholar
  122. 122.
    Kapoor A, Simmonds P, Cullen JM, Scheel TK, Medina JL, Giannitti F, et al. Identification of a pegivirus (GB virus-like virus) that infects horses. J Virol. 2013;87:7185–90.PubMedPubMedCentralGoogle Scholar
  123. 123.
    Kennedy J, Pfankuche VM, Hoeltig D, Postel A, Keuling O, Ciurkiewicz M, et al. Genetic variability of porcine pegivirus in pigs from Europe and China and insights into tissue tropism. Sci Rep. 2019;9(1):8174.PubMedPubMedCentralGoogle Scholar
  124. 124.
    Lyons S, Kapoor A, Schneider BS, Wolfe ND, Culshaw G, Corcoran B, et al. Viraemic frequencies and seroprevalence of non-primate hepacivirus and equine pegiviruses in horses and other mammalian species. J Gen Virol. 2014;95(Pt8):1701–11.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of MedicineMerkur University HospitalZagrebCroatia
  2. 2.School of MedicineUniversity of ZagrebZagrebCroatia
  3. 3.Department of VirologyCroatian Institute of Public HealthZagrebCroatia
  4. 4.Department of MedicineVarazdin General HospitalVarazdinCroatia
  5. 5.Department of Microbiology and Infectious Diseases with Clinic, Faculty of Veterinary MedicineUniversity of ZagrebZagrebCroatia
  6. 6.Poultry Center, Laboratory for Virology and SerologyCroatian Veterinary InstituteZagrebCroatia
  7. 7.Department of SurgeryMerkur University HospitalZagrebCroatia

Personalised recommendations