Viraemic frequencies and seroprevalence of non-primate hepacivirus and equine pegiviruses in horses and other mammalian species Free

Abstract

Non-primate hepacivirus (NPHV), equine pegivirus (EPgV) and Theiler’s disease associated virus (TDAV) are newly discovered members of two genera in the family, and respectively, that include human hepatitis C virus (HCV) and human pegivirus (HPgV). To investigate their epidemiology, persistence and clinical features of infection, large cohorts of horses and other mammalian species were screened for NPHV, EPgV and TDAV viraemia and for past exposure through serological assays for NPHV and EPgV-specific antibodies. NPHV antibodies were detected in 43 % of 328 horses screened for antibodies to NS3 and core antibodies, of which three were viraemic by PCR. All five horses that were stablemates of a viraemic horse were seropositive, as was a dog on the same farm. With this single exception, all other species were negative for NPHV antibodies and viraemia: donkeys ( = 100), dogs ( = 112), cats ( = 131), non-human primates ( = 164) and humans ( = 362). EPgV antibodies to NS3 were detected in 66.5 % of horses, including 10 of the 12 horses that had EPgV viraemia. All donkey samples were negative for EPgV antibody and RNA. All horse and donkey samples were negative for TDAV RNA. By comparing viraemia frequencies in horses with and without liver disease, no evidence was obtained that supported an association between active NPHV and EPgV infections with hepatopathy. The study demonstrates that NPHV and EPgV infections are widespread and enzootic in the study horse population and confirms that NPHV and potentially EPgV have higher frequencies of viral clearance than HCV and HPgV infections in humans.

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2014-08-01
2024-03-29
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References

  1. Adams N. J., Prescott L. E., Jarvis L. M., Lewis J. C., McClure M. O., Smith D. B., Simmonds P. 1998; Detection in chimpanzees of a novel flavivirus related to GB virus-C/hepatitis G virus. J Gen Virol 79:1871–1877[PubMed]
    [Google Scholar]
  2. Alberti A., Morsica G., Chemello L., Cavalletto D., Noventa F., Pontisso P., Ruol A. 1992; Hepatitis C viraemia and liver disease in symptom-free individuals with anti-HCV. Lancet 340:697–698 [View Article][PubMed]
    [Google Scholar]
  3. Alter H. J., Sanchez-Pescador R., Urdea M. S., Wilber J. C., Lagier R. J., Di Bisceglie A. M., Shih J. W., Neuwald P. D. 1995; Evaluation of branched DNA signal amplification for the detection of hepatitis C virus RNA. J Viral Hepat 2:121–132 [View Article][PubMed]
    [Google Scholar]
  4. Alter M. J., Kruszon-Moran D., Nainan O. V., McQuillan G. M., Gao F., Moyer L. A., Kaslow R. A., Margolis H. S. 1999; The prevalence of hepatitis C virus infection in the United States, 1988 through 1994. N Engl J Med 341:556–562 [View Article][PubMed]
    [Google Scholar]
  5. Averhoff F. M., Glass N., Holtzman D. 2012; Global burden of hepatitis C: considerations for healthcare providers in the United States. Clin Infect Dis 55:Suppl 1S10–S15 [View Article][PubMed]
    [Google Scholar]
  6. Berg T., Müller A. R., Platz K. P., Höhne M., Bechstein W. O., Hopf U., Wiedenmann B., Neuhaus P., Schreier E. 1999; Dynamics of GB virus C viremia early after orthotopic liver transplantation indicates extrahepatic tissues as the predominant site of GB virus C replication. Hepatology 29:245–249 [View Article][PubMed]
    [Google Scholar]
  7. Birkenmeyer L. G., Desai S. M., Muerhoff A. S., Leary T. P., Simons J. N., Montes C. C., Mushahwar I. K. 1998; Isolation of a GB virus-related genome from a chimpanzee. J Med Virol 56:44–51 [View Article][PubMed]
    [Google Scholar]
  8. Blair C. S., Davidson F., Lycett C., McDonald D. M., Haydon G. H., Yap P. L., Hayes P. C., Simmonds P., Gillon J. 1998; Prevalence, incidence, and clinical characteristics of hepatitis G virus/GB virus C infection in Scottish blood donors. J Infect Dis 178:1779–1782 [View Article][PubMed]
    [Google Scholar]
  9. Bukh J., Apgar C. L., Govindarajan S., Purcell R. H. 2001; Host range studies of GB virus-B hepatitis agent, the closest relative of hepatitis C virus, in New World monkeys and chimpanzees. J Med Virol 65:694–697 [View Article][PubMed]
    [Google Scholar]
  10. Burbelo P. D., Dubovi E. J., Simmonds P., Medina J. L., Henriquez J. A., Mishra N., Wagner J., Tokarz R., Cullen J. M.other authors 2012; Serology-enabled discovery of genetically diverse hepaciviruses in a new host. J Virol 86:6171–6178 [View Article][PubMed]
    [Google Scholar]
  11. Chandriani S., Skewes-Cox P., Zhong W., Ganem D. E., Divers T. J., Van Blaricum A. J., Tennant B. C., Kistler A. L. 2013; 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 110:E1407–E1415 [View Article][PubMed]
    [Google Scholar]
  12. Crofts N., Aitken C. K. 1997; Incidence of bloodborne virus infection and risk behaviours in a cohort of injecting drug users in Victoria, 1990-1995. Med J Aust 167:17–20[PubMed]
    [Google Scholar]
  13. Drexler J. F., Corman V. M., Müller M. A., Lukashev A. N., Gmyl A., Coutard B., Adam A., Ritz D., Leijten L. M.other authors 2013; Evidence for novel hepaciviruses in rodents. PLoS Pathog 9:e1003438 [View Article][PubMed]
    [Google Scholar]
  14. Engel M., Malta F. M., Gomes M. M., Mello I. M., Pinho J. R., Ono-Nita S. K., Carrilho F. J. 2007; Acute hepatitis C virus infection assessment among chronic hemodialysis patients in the Southwest Parana State, Brazil. BMC Public Health 7:50 [View Article][PubMed]
    [Google Scholar]
  15. Epstein J. H., Quan P. L., Briese T., Street C., Jabado O., Conlan S., Ali Khan S., Verdugo D., Hossain M. J.other authors 2010; Identification of GBV-D, a novel GB-like flavivirus from Old World frugivorous bats (Pteropus giganteus) in Bangladesh. PLoS Pathog 6:e1000972 [View Article][PubMed]
    [Google Scholar]
  16. Fierer D. S., Uriel A. J., Carriero D. C., Klepper A., Dieterich D. T., Mullen M. P., Thung S. N., Fiel M. I., Branch A. D. 2008; Liver fibrosis during an outbreak of acute hepatitis C virus infection in HIV-infected men: a prospective cohort study. J Infect Dis 198:683–686 [View Article][PubMed]
    [Google Scholar]
  17. Gómara M. J., Fernández L., Pérez T., Ercilla G., Haro I. 2010; Assessment of synthetic chimeric multiple antigenic peptides for diagnosis of GB virus C infection. Anal Biochem 396:51–58 [View Article][PubMed]
    [Google Scholar]
  18. Gutierrez R. A., Dawson G. J., Knigge M. F., Melvin S. L., Heynen C. A., Kyrk C. R., Young C. E., Carrick R. J., Schlauder G. G.other authors 1997; Seroprevalence of GB virus C and persistence of RNA and antibody. J Med Virol 53:167–173 [View Article][PubMed]
    [Google Scholar]
  19. Kapoor A., Simmonds P., Gerold G., Qaisar N., Jain K., Henriquez J. A., Firth C., Hirschberg D. L., Rice C. M.other authors 2011; Characterization of a canine homolog of hepatitis C virus. Proc Natl Acad Sci U S A 108:11608–11613 [View Article][PubMed]
    [Google Scholar]
  20. Kapoor A., Simmonds P., Cullen J. M., Scheel T. K., Medina J. L., Giannitti F., Nishiuchi E., Brock K. V., Burbelo P. D.other authors 2013a; Identification of a pegivirus (GB virus-like virus) that infects horses. J Virol 87:7185–7190 [View Article][PubMed]
    [Google Scholar]
  21. Kapoor A., Simmonds P., Scheel T. K. H., Hjelle B., Cullen J. M., Burbelo P. D., Chauhan L. V., Duraisamy R., Sanchez Leon M.other authors 2013b; Identification of rodent homologs of hepatitis C virus and pegiviruses. MBio 4:e00216–e13 [View Article][PubMed]
    [Google Scholar]
  22. King A. M., Adams M. J., Lefkowitz E. J., Carstens E. B. 2011; Virus taxonomy: IXth report of the International Committee on Taxonomy of Viruses: Access Online via Elsevier.
    [Google Scholar]
  23. Lauck M., Sibley S. D., Lara J., Purdy M. A., Khudyakov Y., Hyeroba D., Tumukunde A., Weny G., Switzer W. M.other authors 2013; A novel hepacivirus with an unusually long and intrinsically disordered NS5A protein in a wild Old World primate. J Virol 87:8971–8981 [View Article][PubMed]
    [Google Scholar]
  24. Lavoie M., Sharp C. P., Pépin J., Pennington C., Foupouapouognigni Y., Pybus O. G., Njouom R., Simmonds P. 2012; Human parvovirus 4 infection, Cameroon. Emerg Infect Dis 18:680–683 [View Article][PubMed]
    [Google Scholar]
  25. Lyons S., Kapoor A., Sharp C., Schneider B. S., Wolfe N. D., Culshaw G., Corcoran B., McGorum B. C., Simmonds P. 2012; Nonprimate hepaciviruses in domestic horses, United Kingdom. Emerg Infect Dis 18:1976–1982 [View Article][PubMed]
    [Google Scholar]
  26. Mathurin P., Moussalli J., Cadranel J. F., Thibault V., Charlotte F., Dumouchel P., Cazier A., Huraux J. M., Devergie B.other authors 1998; Slow progression rate of fibrosis in hepatitis C virus patients with persistently normal alanine transaminase activity. Hepatology 27:868–872 [View Article][PubMed]
    [Google Scholar]
  27. Miller F. D., Abu-Raddad L. J. 2010; Evidence of intense ongoing endemic transmission of hepatitis C virus in Egypt. Proc Natl Acad Sci U S A 107:14757–14762 [View Article][PubMed]
    [Google Scholar]
  28. Mohr E. L., Stapleton J. T. 2009; GB virus type C interactions with HIV: the role of envelope glycoproteins. J Viral Hepat 16:757–768 [View Article][PubMed]
    [Google Scholar]
  29. Muerhoff A. S., Leary T. P., Simons J. N., Pilot-Matias T. J., Dawson G. J., Erker J. C., Chalmers M. L., Schlauder G. G., Desai S. M., Mushahwar I. K. 1995; Genomic organization of GB viruses A and B: two new members of the Flaviviridae associated with GB agent hepatitis. J Virol 69:5621–5630[PubMed]
    [Google Scholar]
  30. Nalpas B., Thiers V., Pol S., Driss F., Thepot V., Berthelot P., Brechot C. 1992; Hepatitis C viremia and anti-HCV antibodies in alcoholics. J Hepatol 14:381–384 [View Article][PubMed]
    [Google Scholar]
  31. Pavlova B. G., Heinz R., Selim U., Tüchler H., Pittermann E., Eder G. 1999; Association of GB virus C (GBV-C)/hepatitis G virus (HGV) with haematological diseases of different malignant potential. J Med Virol 57:361–366 [View Article][PubMed]
    [Google Scholar]
  32. Perz J. F., Farrington L. A., Pecoraro C., Hutin Y. J., Armstrong G. L. 2004; Estimated global prevalence of hepatitis C virus infection. 42nd Annual Meeting of the Infectious Diseases Society of America. Boston, MA, USA.
    [Google Scholar]
  33. Pilot-Matias T. J., Carrick R. J., Coleman P. F., Leary T. P., Surowy T. K., Simons J. N., Muerhoff A. S., Buijk S. L., Chalmers M. L.other authors 1996a; Expression of the GB virus C E2 glycoprotein using the Semliki Forest virus vector system and its utility as a serologic marker. Virology 225:282–292 [View Article][PubMed]
    [Google Scholar]
  34. Pilot-Matias T. J., Muerhoff A. S., Simons J. N., Leary T. P., Buijk S. L., Chalmers M. L., Erker J. C., Dawson G. J., Desai S. M., Mushahwar I. K. 1996b; Identification of antigenic regions in the GB hepatitis viruses GBV-A, GBV-B, and GBV-C. J Med Virol 48:329–338 [View Article][PubMed]
    [Google Scholar]
  35. Polgreen P. M., Xiang J., Chang Q., Stapleton J. T. 2003; GB virus type C/hepatitis G virus: a non-pathogenic flavivirus associated with prolonged survival in HIV-infected individuals. Microbes Infect 5:1255–1261 [View Article][PubMed]
    [Google Scholar]
  36. Pradat P., Alberti A., Poynard T., Esteban J. I., Weiland O., Marcellin P., Badalamenti S., Trépo C. 2002; Predictive value of ALT levels for histologic findings in chronic hepatitis C: a European collaborative study. Hepatology 36:973–977 [View Article][PubMed]
    [Google Scholar]
  37. Puoti C. 2003; HCV carriers with persistently normal aminotransferase levels: normal does not always mean healthy. J Hepatol 38:529–532 [View Article][PubMed]
    [Google Scholar]
  38. Puoti C., Magrini A., Stati T., Rigato P., Montagnese F., Rossi P., Aldegheri L., Resta S. 1997; Clinical, histological, and virological features of hepatitis C virus carriers with persistently normal or abnormal alanine transaminase levels. Hepatology 26:1393–1398 [View Article][PubMed]
    [Google Scholar]
  39. Quan P. L., Firth C., Conte J. M., Williams S. H., Zambrana-Torrelio C. M., Anthony S. J., Ellison J. A., Gilbert A. T., Kuzmin I. V.other authors 2013; Bats are a major natural reservoir for hepaciviruses and pegiviruses. Proc Natl Acad Sci U S A 110:8194–8199 [View Article][PubMed]
    [Google Scholar]
  40. Qureshi H., Bile K. M., Jooma R., Alam S. E., Afridi H. U. 2010; Prevalence of hepatitis B and C viral infections in Pakistan: findings of a national survey appealing for effective prevention and control measures. East Mediterr Health J 16:SupplS15–S23[PubMed]
    [Google Scholar]
  41. Scallan M. F., Clutterbuck D., Jarvis L. M., Scott G. R., Simmonds P. 1998; Sexual transmission of GB virus C/hepatitis G virus. J Med Virol 55:203–208 [View Article][PubMed]
    [Google Scholar]
  42. Schwarze-Zander C., Blackard J. T., Zheng H., Addo M. M., Lin W., Robbins G. K., Sherman K. E., Zdunek D., Hess G., Chung R. T.AIDS Clinical Trial Group A5071 Study Team 2006; GB virus C (GBV-C) infection in hepatitis C virus (HCV)/HIV-coinfected patients receiving HCV treatment: importance of the GBV-C genotype. J Infect Dis 194:410–419 [View Article][PubMed]
    [Google Scholar]
  43. Sharp P. M., Simmonds P. 2011; Evaluating the evidence for virus/host co-evolution. Curr Opin Virol 1:436–441 [View Article][PubMed]
    [Google Scholar]
  44. Sharp C. P., LeBreton M., Kantola K., Nana A., Diffo Jle. D., Djoko C. F., Tamoufe U., Kiyang J. A., Babila T. G.other authors 2010; Widespread infection with homologues of human parvoviruses B19, PARV4, and human bocavirus of chimpanzees and gorillas in the wild. J Virol 84:10289–10296 [View Article][PubMed]
    [Google Scholar]
  45. Shepard C. W., Finelli L., Alter M. J. 2005; Global epidemiology of hepatitis C virus infection. Lancet Infect Dis 5:558–567 [View Article][PubMed]
    [Google Scholar]
  46. Simmonds P. 2012; SSE: a nucleotide and amino acid sequence analysis platform. BMC Res Notes 5:50 [View Article][PubMed]
    [Google Scholar]
  47. Simmonds P. 2013; The origin of hepatitis C virus. Curr Top Microbiol Immunol 369:1–15[PubMed]
    [Google Scholar]
  48. Simons J. N., Leary T. P., Dawson G. J., Pilot-Matias T. J., Muerhoff A. S., Schlauder G. G., Desai S. M., Mushahwar I. K. 1995a; Isolation of novel virus-like sequences associated with human hepatitis. Nat Med 1:564–569 [View Article][PubMed]
    [Google Scholar]
  49. Simons J. N., Pilot-Matias T. J., Leary T. P., Dawson G. J., Desai S. M., Schlauder G. G., Muerhoff A. S., Erker J. C., Buijk S. L.other authors 1995b; Identification of two flavivirus-like genomes in the GB hepatitis agent. Proc Natl Acad Sci U S A 92:3401–3405 [View Article][PubMed]
    [Google Scholar]
  50. Stapleton J. T., Foung S., Muerhoff A. S., Bukh J., Simmonds P. 2011; 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 92:233–246 [View Article][PubMed]
    [Google Scholar]
  51. Sugitani M., Inchauspé G., Shindo M., Prince A. M. 1992; Sensitivity of serological assays to identify blood donors with hepatitis C viraemia. Lancet 339:1018–1019 [View Article][PubMed]
    [Google Scholar]
  52. Tacke M., Kiyosawa K., Stark K., Schlueter V., Ofenloch-Haehnle B., Hess G., Engel A. M. 1997; Detection of antibodies to a putative hepatitis G virus envelope protein. Lancet 349:318–320 [View Article][PubMed]
    [Google Scholar]
  53. Takaki A., Wiese M., Maertens G., Depla E., Seifert U., Liebetrau A., Miller J. L., Manns M. P., Rehermann B. 2000; Cellular immune responses persist and humoral responses decrease two decades after recovery from a single-source outbreak of hepatitis C. Nat Med 6:578–582 [View Article][PubMed]
    [Google Scholar]
  54. Takikawa S., Engle R. E., Faulk K. N., Emerson S. U., Purcell R. H., Bukh J. 2010; Molecular evolution of GB virus B hepatitis virus during acute resolving and persistent infections in experimentally infected tamarins. J Gen Virol 91:727–733 [View Article][PubMed]
    [Google Scholar]
  55. Tan D., Matsumoto A., Conry-Cantilena C., Melpolder J. C., Shih J. W., Leuther M., Hess G., Gibble J. W., Ness P. M., Alter H. J. 1999; Analysis of hepatitis G virus (HGV) RNA, antibody to HGV envelope protein, and risk factors for blood donors coinfected with HGV and hepatitis C virus. J Infect Dis 179:1055–1061 [View Article][PubMed]
    [Google Scholar]
  56. Tanaka E., Kiyosawa K., Shimoda K., Hino K., Tacke M., Schmolke S., Engel A. M., Hess G. 1998; Evolution of hepatitis G virus infection and antibody response to envelope protein in patients with transfusion-associated non-A, non-B hepatitis. J Viral Hepat 5:153–159 [View Article][PubMed]
    [Google Scholar]
  57. Van der Bij A. K., Kloosterboer N., Prins M., Boeser-Nunnink B., Geskus R. B., Lange J. M., Coutinho R. A., Schuitemaker H. 2005; GB virus C coinfection and HIV-1 disease progression: The Amsterdam Cohort Study. J Infect Dis 191:678–685 [View Article][PubMed]
    [Google Scholar]
  58. Williams C. F., Klinzman D., Yamashita T. E., Xiang J., Polgreen P. M., Rinaldo C., Liu C., Phair J., Margolick J. B.other authors 2004; Persistent GB virus C infection and survival in HIV-infected men. N Engl J Med 350:981–990 [View Article][PubMed]
    [Google Scholar]
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