1887

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.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.065094-0
2014-08-01
2019-11-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/95/8/1701.html?itemId=/content/journal/jgv/10.1099/vir.0.065094-0&mimeType=html&fmt=ahah

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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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 1), S10–S15. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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: (Suppl), S15–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. [CrossRef] [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. [CrossRef] [PubMed]
    [Google Scholar]
  43. Sharp P. M., Simmonds P.. ( 2011; ). Evaluating the evidence for virus/host co-evolution. . Curr Opin Virol 1:, 436–441. [CrossRef] [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. [CrossRef] [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. [CrossRef] [PubMed]
    [Google Scholar]
  46. Simmonds P.. ( 2012; ). SSE: a nucleotide and amino acid sequence analysis platform. . BMC Res Notes 5:, 50. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.065094-0
Loading
/content/journal/jgv/10.1099/vir.0.065094-0
Loading

Data & Media loading...

Supplements

Supplementary Material 

PDF

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error