Analyze Diet
Journal of virology2016; 91(1); e01711-16; doi: 10.1128/JVI.01711-16

Differential Infection Patterns and Recent Evolutionary Origins of Equine Hepaciviruses in Donkeys.

Abstract: The hepatitis C virus (HCV) is a major human pathogen. Genetically related viruses in animals suggest a zoonotic origin of HCV. The closest relative of HCV is found in horses (termed equine hepacivirus [EqHV]). However, low EqHV genetic diversity implies relatively recent acquisition of EqHV by horses, making a derivation of HCV from EqHV unlikely. To unravel the EqHV evolutionary history within equid sister species, we analyzed 829 donkeys and 53 mules sampled in nine European, Asian, African, and American countries by molecular and serologic tools for EqHV infection. Antibodies were found in 278 animals (31.5%), and viral RNA was found in 3 animals (0.3%), all of which were simultaneously seropositive. A low RNA prevalence in spite of high seroprevalence suggests a predominance of acute infection, a possible difference from the mostly chronic hepacivirus infection pattern seen in horses and humans. Limitation of transmission due to short courses of infection may explain the existence of entirely seronegative groups of animals. Donkey and horse EqHV strains were paraphyletic and 97.5 to 98.2% identical in their translated polyprotein sequences, making virus/host cospeciation unlikely. Evolutionary reconstructions supported host switches of EqHV between horses and donkeys without the involvement of adaptive evolution. Global admixture of donkey and horse hepaciviruses was compatible with anthropogenic alterations of EqHV ecology. In summary, our findings do not support EqHV as the origin of the significantly more diversified HCV. Identification of a host system with predominantly acute hepacivirus infection may enable new insights into the chronic infection pattern associated with HCV. Objective: The evolutionary origins of the human hepatitis C virus (HCV) are unclear. The closest animal-associated relative of HCV occurs in horses (equine hepacivirus [EqHV]). The low EqHV genetic diversity implies a relatively recent acquisition of EqHV by horses, limiting the time span for potential horse-to-human infections in the past. Horses are genetically related to donkeys, and EqHV may have cospeciated with these host species. Here, we investigated a large panel of donkeys from various countries using serologic and molecular tools. We found EqHV to be globally widespread in donkeys and identify potential differences in EqHV infection patterns, with donkeys potentially showing enhanced EqHV clearance compared to horses. We provide strong evidence against EqHV cospeciation and for its capability to switch hosts among equines. Differential hepacivirus infection patterns in horses and donkeys may enable new insights into the chronic infection pattern associated with HCV.
Publication Date: 2016-12-16 PubMed ID: 27795428PubMed Central: PMC5165184DOI: 10.1128/JVI.01711-16Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This study investigates the evolutionary history and infection patterns of equine hepaciviruses (EqHV), particularly in donkeys, to gain insights into the origins of the hepatitis C virus (HCV) in humans. The scientists found EqHV to be prevalent in donkeys worldwide, with potential differences in infection patterns. The results, however, refute that EqHV cospeciates with its hosts or acts as a direct source of HCV.

Research Context

  • HCV is a major human pathogen, with genetically related viruses found in animals. The closest relative to HCV is the EqHV, making it possible that HCV has a zoonotic origin.
  • A lack of genetic diversity in EqHV suggests that horses, primary carriers of EqHV, may have acquired it relatively recently. This makes the derivation of HCV from EqHV unlikely, pointing towards the need to understand EqHV’s evolutionary history.
  • Donkeys, closely related to horses, were analyzed in this study as a possibly overlooked reservoir of the virus.
  • The primary goal of the research was to discern if the HCV could have evolved from the EqHV, and to understand the patterns of EqHV infection within the equid population.

Research Methodology

  • In this study, a total of 829 donkeys and 53 mules from across nine countries in Africa, Asia, Europe, and America were analyzed using molecular and serologic examination methods.
  • The scientists looked for the presence of EqHV infection by identifying antibodies (suggesting past infection) and viral RNA (indicating current infection).
  • The study sought to uncover possible differences in the hepacivirus infection pattern seen in horses and humans, which is mostly chronic, as compared to the potential predominance of acute infection in donkeys.

Research Findings

  • Findings showed that antibodies were found in 31.5% of the sampled animals, but viral RNA was found only in 0.3%, all of which were already seropositive, hinting at predominantly past and not persistent infections.
  • The low prevalence of RNA, but high seroprevalence, suggests that infection is largely acute in donkeys, potentially distinguishing them from horses and humans.
  • Donkey and horse EqHV strains were found to be 97.5 to 98.2% identical, making virus/host cospeciation, or parallel evolution of viruses and hosts, unlikely.
  • The study also suggested that EqHV may have migrated between horses and donkeys without undergoing adaptive evolution.
  • The global presence of donkey and horse hepaciviruses may be influenced by human-mediated factors.
  • The significantly lower diversity seen in EqHV compared to HCV suggests that EqHV may not be the origin of HCV-

Significance of the Study

  • The identification of potentially different infection patterns in donkeys, where hepacivirus infection seems to be predominantly acute rather than chronic, could enable new insights into the chronic infection pattern seen with HCV.
  • The study also refutes the co-evolution of EqHV with its host species and dismisses EqHV as the source of the more diversified HCV, which could have implications on related future investigations.

Cite This Article

APA
Walter S, Rasche A, Moreira-Soto A, Pfaender S, Bletsa M, Corman VM, Aguilar-Setien A, García-Lacy F, Hans A, Todt D, Schuler G, Shnaiderman-Torban A, Steinman A, Roncoroni C, Veneziano V, Rusenova N, Sandev N, Rusenov A, Zapryanova D, García-Bocanegra I, Jores J, Carluccio A, Veronesi MC, Cavalleri JMV, Drosten C, Lemey P, Steinmann E, Drexler JF. (2016). Differential Infection Patterns and Recent Evolutionary Origins of Equine Hepaciviruses in Donkeys. J Virol, 91(1), e01711-16. https://doi.org/10.1128/JVI.01711-16

Publication

ISSN: 1098-5514
NlmUniqueID: 0113724
Country: United States
Language: English
Volume: 91
Issue: 1
PII: e01711-16

Researcher Affiliations

Walter, Stephanie
  • Institute of Experimental Virology, TWINCORE, Center for Experimental and Clinical Infection Research Hannover, Hannover, Germany.
Rasche, Andrea
  • Institute of Virology, University of Bonn Medical Centre, Bonn, Germany.
  • German Centre for Infection Research (DZIF), Bonn-Cologne, Germany.
Moreira-Soto, Andrés
  • Institute of Virology, University of Bonn Medical Centre, Bonn, Germany.
Pfaender, Stephanie
  • Institute of Experimental Virology, TWINCORE, Center for Experimental and Clinical Infection Research Hannover, Hannover, Germany.
Bletsa, Magda
  • Department of Microbiology and Immunology, Rega Institute, KU Leuven-University of Leuven, Leuven, Belgium.
Corman, Victor Max
  • Institute of Virology, University of Bonn Medical Centre, Bonn, Germany.
  • German Centre for Infection Research (DZIF), Bonn-Cologne, Germany.
Aguilar-Setien, Alvaro
  • Medical Immunology Research Unit, National Medical Center Siglo XXL, Mexican Social Security Institute (IMSS), Mexico City, Mexico.
García-Lacy, Fernando
  • Equine Medicine and Surgery Department FMVZ-UNAM, Mexico City, Mexico.
Hans, Aymeric
  • ANSES, Laboratory for Equine Diseases, Goustranville, France.
Todt, Daniel
  • Institute of Experimental Virology, TWINCORE, Center for Experimental and Clinical Infection Research Hannover, Hannover, Germany.
Schuler, Gerhard
  • Clinic for Obstetrics, Gynecology and Andrology of Large and Small Animals, Justus-Liebig-Universität Giessen, Giessen, Germany.
Shnaiderman-Torban, Anat
  • Koret School of Veterinary Medicine, Rehovot, Israel.
Steinman, Amir
  • Koret School of Veterinary Medicine, Rehovot, Israel.
Roncoroni, Cristina
  • Istituto Zooprofilattico Sperimentale Lazio e Toscana, Rome, Italy.
Veneziano, Vincenzo
  • Department of Veterinary Medicine and Animal Productions, University of Naples Federico II, Naples, Italy.
Rusenova, Nikolina
  • Trakia University, Faculty of Veterinary Medicine, Department of Veterinary Microbiology, Infectious and Parasitic Diseases, Stara Zagora, Bulgaria.
Sandev, Nikolay
  • Trakia University, Faculty of Veterinary Medicine, Department of Veterinary Microbiology, Infectious and Parasitic Diseases, Stara Zagora, Bulgaria.
Rusenov, Anton
  • Trakia University, Faculty of Veterinary Medicine, Department of Internal Diseases, Stara Zagora, Bulgaria.
Zapryanova, Dimitrinka
  • Trakia University, Faculty of Veterinary Medicine, Department of Pharmacology, Veterinary Physiology, and Physiological Chemistry, Stara Zagora, Bulgaria.
García-Bocanegra, Ignacio
  • Department of Animal Health, University of Córdoba, Córdoba, Spain.
Jores, Joerg
  • International Livestock Research Institute, Nairobi, Kenya.
  • Institute of Veterinary Bacteriology, University of Bern, Bern, Switzerland.
Carluccio, Augusto
  • Faculty of Veterinary Medicine, Università degli Studi di Teramo, Teramo, Italy.
Veronesi, Maria Cristina
  • Department of Veterinary Medicine, Università degli Studi di Milano, Milan, Italy.
Cavalleri, Jessika M V
  • Clinic for Horses, University of Veterinary Medicine Hannover, Foundation, Hannover, Germany.
Drosten, Christian
  • Institute of Virology, University of Bonn Medical Centre, Bonn, Germany.
  • German Centre for Infection Research (DZIF), Bonn-Cologne, Germany.
Lemey, Philippe
  • Department of Microbiology and Immunology, Rega Institute, KU Leuven-University of Leuven, Leuven, Belgium.
Steinmann, Eike
  • Institute of Experimental Virology, TWINCORE, Center for Experimental and Clinical Infection Research Hannover, Hannover, Germany Eike.Steinmann@twincore.de drexler@virology-bonn.de.
Drexler, Jan Felix
  • Institute of Virology, University of Bonn Medical Centre, Bonn, Germany Eike.Steinmann@twincore.de drexler@virology-bonn.de.
  • German Centre for Infection Research (DZIF), Bonn-Cologne, Germany.

MeSH Terms

  • Acute Disease
  • Animals
  • Antibodies, Viral / blood
  • Biological Evolution
  • Equidae
  • Europe / epidemiology
  • Genetic Variation
  • Genome, Viral
  • Hepacivirus / classification
  • Hepacivirus / genetics
  • Hepacivirus / immunology
  • Hepatitis C / epidemiology
  • Hepatitis C / transmission
  • Hepatitis C / veterinary
  • Hepatitis C / virology
  • Horses
  • Host Specificity
  • Humans
  • Israel / epidemiology
  • Kenya / epidemiology
  • Latin America / epidemiology
  • Phylogeny
  • Sequence Analysis, DNA
  • Seroepidemiologic Studies

References

This article includes 57 references
  1. . Global, regional, and national incidence, prevalence, and years lived with disability for 301 acute and chronic diseases and injuries in 188 countries, 1990-2013: a systematic analysis for the Global Burden of Disease Study 2013.. Lancet 2015 Aug 22;386(9995):743-800.
  2. Smith DB, Bukh J, Kuiken C, Muerhoff AS, Rice CM, Stapleton JT, Simmonds P. Expanded classification of hepatitis C virus into 7 genotypes and 67 subtypes: updated criteria and genotype assignment web resource.. Hepatology 2014 Jan;59(1):318-27.
    doi: 10.1002/hep.26744pmc: PMC4063340pubmed: 24115039google scholar: lookup
  3. Messina JP, Humphreys I, Flaxman A, Brown A, Cooke GS, Pybus OG, Barnes E. Global distribution and prevalence of hepatitis C virus genotypes.. Hepatology 2015 Jan;61(1):77-87.
    doi: 10.1002/hep.27259pmc: PMC4303918pubmed: 25069599google scholar: lookup
  4. Magiorkinis G, Magiorkinis E, Paraskevis D, Ho SY, Shapiro B, Pybus OG, Allain JP, Hatzakis A. The global spread of hepatitis C virus 1a and 1b: a phylodynamic and phylogeographic analysis.. PLoS Med 2009 Dec;6(12):e1000198.
  5. Markov PV, Pepin J, Frost E, Deslandes S, Labbé AC, Pybus OG. Phylogeography and molecular epidemiology of hepatitis C virus genotype 2 in Africa.. J Gen Virol 2009 Sep;90(Pt 9):2086-96.
    doi: 10.1099/vir.0.011569-0pubmed: 19474244google scholar: lookup
  6. Simmonds P. The origin of hepatitis C virus.. Curr Top Microbiol Immunol 2013;369:1-15.
    pubmed: 23463195doi: 10.1007/978-3-642-27340-7_1google scholar: lookup
  7. Scheel TK, Simmonds P, Kapoor A. Surveying the global virome: identification and characterization of HCV-related animal hepaciviruses.. Antiviral Res 2015 Mar;115:83-93.
  8. Pfaender S, Brown RJ, Pietschmann T, Steinmann E. Natural reservoirs for homologs of hepatitis C virus.. Emerg Microbes Infect 2014 Mar;3(3):e21.
    doi: 10.1038/emi.2014.19pmc: PMC3974340pubmed: 26038514google scholar: lookup
  9. Makuwa M, Souquière S, Telfer P, Leroy E, Bourry O, Rouquet P, Clifford S, Wickings EJ, Roques P, Simon F. Occurrence of hepatitis viruses in wild-born non-human primates: a 3 year (1998-2001) epidemiological survey in Gabon.. J Med Primatol 2003 Dec;32(6):307-14.
  10. Pybus OG, Thézé J. Hepacivirus cross-species transmission and the origins of the hepatitis C virus.. Curr Opin Virol 2016 Feb;16:1-7.
    doi: 10.1016/j.coviro.2015.10.002pubmed: 26517843google scholar: lookup
  11. Drexler JF, Corman VM, Müller MA, Lukashev AN, Gmyl A, Coutard B, Adam A, Ritz D, Leijten LM, van Riel D, Kallies R, Klose SM, Gloza-Rausch F, Binger T, Annan A, Adu-Sarkodie Y, Oppong S, Bourgarel M, Rupp D, Hoffmann B, Schlegel M, Kümmerer BM, Krüger DH, Schmidt-Chanasit J, Setién AA, Cottontail VM, Hemachudha T, Wacharapluesadee S, Osterrieder K, Bartenschlager R, Matthee S, Beer M, Kuiken T, Reusken C, Leroy EM, Ulrich RG, Drosten C. Evidence for novel hepaciviruses in rodents.. PLoS Pathog 2013;9(6):e1003438.
  12. Corman VM, Grundhoff A, Baechlein C, Fischer N, Gmyl A, Wollny R, Dei D, Ritz D, Binger T, Adankwah E, Marfo KS, Annison L, Annan A, Adu-Sarkodie Y, Oppong S, Becher P, Drosten C, Drexler JF. Highly divergent hepaciviruses from African cattle.. J Virol 2015 Jun;89(11):5876-82.
    doi: 10.1128/JVI.00393-15pmc: PMC4442428pubmed: 25787289google scholar: lookup
  13. Thézé J, Lowes S, Parker J, Pybus OG. Evolutionary and Phylogenetic Analysis of the Hepaciviruses and Pegiviruses.. Genome Biol Evol 2015 Oct 21;7(11):2996-3008.
    doi: 10.1093/gbe/evv202pmc: PMC5635594pubmed: 26494702google scholar: lookup
  14. Pybus OG, Gray RR. Virology: The virus whose family expanded.. Nature 2013 Jun 20;498(7454):310-1.
    doi: 10.1038/498310apmc: PMC7095075pubmed: 23783626google scholar: lookup
  15. Kapoor A, Simmonds P, Gerold G, Qaisar N, Jain K, Henriquez JA, Firth C, Hirschberg DL, Rice CM, Shields S, Lipkin WI. Characterization of a canine homolog of hepatitis C virus.. Proc Natl Acad Sci U S A 2011 Jul 12;108(28):11608-13.
    doi: 10.1073/pnas.1101794108pmc: PMC3136326pubmed: 21610165google scholar: lookup
  16. El-Attar LMR, Mitchell JA, Brooks Brownlie H, Priestnall SL, Brownlie J. Detection of non-primate hepaciviruses in UK dogs.. Virology 2015 Oct;484:93-102.
    doi: 10.1016/j.virol.2015.05.005pmc: PMC7111718pubmed: 26086431google scholar: lookup
  17. Lyons S, Kapoor A, Schneider BS, Wolfe ND, Culshaw G, Corcoran B, Durham AE, Burden F, McGorum BC, Simmonds P. Viraemic frequencies and seroprevalence of non-primate hepacivirus and equine pegiviruses in horses and other mammalian species.. J Gen Virol 2014 Aug;95(Pt 8):1701-1711.
    doi: 10.1099/vir.0.065094-0pubmed: 24814924google scholar: lookup
  18. Outram AK, Stear NA, Bendrey R, Olsen S, Kasparov A, Zaibert V, Thorpe N, Evershed RP. The earliest horse harnessing and milking.. Science 2009 Mar 6;323(5919):1332-5.
    doi: 10.1126/science.1168594pubmed: 19265018google scholar: lookup
  19. Orlando L, Ginolhac A, Zhang G, Froese D, Albrechtsen A, Stiller M, Schubert M, Cappellini E, Petersen B, Moltke I, Johnson PL, Fumagalli M, Vilstrup JT, Raghavan M, Korneliussen T, Malaspinas AS, Vogt J, Szklarczyk D, Kelstrup CD, Vinther J, Dolocan A, Stenderup J, Velazquez AM, Cahill J, Rasmussen M, Wang X, Min J, Zazula GD, Seguin-Orlando A, Mortensen C, Magnussen K, Thompson JF, Weinstock J, Gregersen K, Røed KH, Eisenmann V, Rubin CJ, Miller DC, Antczak DF, Bertelsen MF, Brunak S, Al-Rasheid KA, Ryder O, Andersson L, Mundy J, Krogh A, Gilbert MT, Kjær K, Sicheritz-Ponten T, Jensen LJ, Olsen JV, Hofreiter M, Nielsen R, Shapiro B, Wang J, Willerslev E. Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse.. Nature 2013 Jul 4;499(7456):74-8.
    doi: 10.1038/nature12323pubmed: 23803765google scholar: lookup
  20. Lyons S, Kapoor A, Sharp C, Schneider BS, Wolfe ND, Culshaw G, Corcoran B, McGorum BC, Simmonds P. Nonprimate hepaciviruses in domestic horses, United kingdom.. Emerg Infect Dis 2012 Dec;18(12):1976-82.
    doi: 10.3201/eid1812.120498pmc: PMC3557883pubmed: 23171728google scholar: lookup
  21. Gemaque BS, Junior Souza de Souza A, do Carmo Pereira Soares M, Malheiros AP, Silva AL, Alves MM, Gomes-Gouvêa MS, Pinho JR, Ferreira de Figueiredo H, Ribeiro DB, Souza da Silva J, Moraes LA, Ribeiro AS, Pereira WL. Hepacivirus infection in domestic horses, Brazil, 2011-2013.. Emerg Infect Dis 2014 Dec;20(12):2180-2.
    pmc: PMC4257787pubmed: 25420101doi: 10.3201/eid2012.140603google scholar: lookup
  22. Lu G, Sun L, Xu T, He D, Wang Z, Ou S, Jia K, Yuan L, Li S. First Description of Hepacivirus and Pegivirus Infection in Domestic Horses in China: A Study in Guangdong Province, Heilongjiang Province and Hong Kong District.. PLoS One 2016;11(5):e0155662.
  23. Scheel TK, Kapoor A, Nishiuchi E, Brock KV, Yu Y, Andrus L, Gu M, Renshaw RW, Dubovi EJ, McDonough SP, Van de Walle GR, Lipkin WI, Divers TJ, Tennant BC, Rice CM. Characterization of nonprimate hepacivirus and construction of a functional molecular clone.. Proc Natl Acad Sci U S A 2015 Feb 17;112(7):2192-7.
    doi: 10.1073/pnas.1500265112pmc: PMC4343093pubmed: 25646476google scholar: lookup
  24. Burbelo PD, Dubovi EJ, Simmonds P, Medina JL, Henriquez JA, Mishra N, Wagner J, Tokarz R, Cullen JM, Iadarola MJ, Rice CM, Lipkin WI, Kapoor A. Serology-enabled discovery of genetically diverse hepaciviruses in a new host.. J Virol 2012 Jun;86(11):6171-8.
    doi: 10.1128/JVI.00250-12pmc: PMC3372197pubmed: 22491452google scholar: lookup
  25. Pfaender S, Cavalleri JM, Walter S, Doerrbecker J, Campana B, Brown RJ, Burbelo PD, Postel A, Hahn K, Anggakusuma, Riebesehl N, Baumgärtner W, Becher P, Heim MH, Pietschmann T, Feige K, Steinmann E. Clinical course of infection and viral tissue tropism of hepatitis C virus-like nonprimate hepaciviruses in horses.. Hepatology 2015 Feb;61(2):447-59.
    doi: 10.1002/hep.27440pubmed: 25212983google scholar: lookup
  26. Drexler JF, Kupfer B, Petersen N, Grotto RM, Rodrigues SM, Grywna K, Panning M, Annan A, Silva GF, Douglas J, Koay ES, Smuts H, Netto EM, Simmonds P, Pardini MI, Roth WK, Drosten C. A novel diagnostic target in the hepatitis C virus genome.. PLoS Med 2009 Feb 10;6(2):e31.
  27. Tanaka T, Kasai H, Yamashita A, Okuyama-Dobashi K, Yasumoto J, Maekawa S, Enomoto N, Okamoto T, Matsuura Y, Morimatsu M, Manabe N, Ochiai K, Yamashita K, Moriishi K. Hallmarks of hepatitis C virus in equine hepacivirus.. J Virol 2014 Nov;88(22):13352-66.
    doi: 10.1128/JVI.02280-14pmc: PMC4249100pubmed: 25210167google scholar: lookup
  28. Matsuu A, Hobo S, Ando K, Sanekata T, Sato F, Endo Y, Amaya T, Osaki T, Horie M, Masatani T, Ozawa M, Tsukiyama-Kohara K. Genetic and serological surveillance for non-primate hepacivirus in horses in Japan.. Vet Microbiol 2015 Sep 30;179(3-4):219-27.
    doi: 10.1016/j.vetmic.2015.05.028pubmed: 26070772google scholar: lookup
  29. Burden FA, Hazell-Smith E, Mulugeta G, Patrick V, Trawford R, Brooks-Brownlie HW. Reference intervals for biochemical and haematological parameters in mature domestic donkeys (Equus asinus) in the UK. Equine Vet Educ 28:134–139.
    doi: 10.1111/eve.12512google scholar: lookup
  30. Yang Z. Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution.. Mol Biol Evol 1998 May;15(5):568-73.
  31. Gray RR, Parker J, Lemey P, Salemi M, Katzourakis A, Pybus OG. The mode and tempo of hepatitis C virus evolution within and among hosts.. BMC Evol Biol 2011 May 19;11:131.
    doi: 10.1186/1471-2148-11-131pmc: PMC3112090pubmed: 21595904google scholar: lookup
  32. Pfafferott K, Gaudieri S, Ulsenheimer A, James I, Heeg M, Nolan D, John M, Rauch A, Mallal S, Lucas A, Klenerman P, Diepolder HM, Lucas M. Constrained pattern of viral evolution in acute and early HCV infection limits viral plasticity.. PLoS One 2011 Feb 8;6(2):e16797.
  33. Simmonds P, Tuplin A, Evans DJ. Detection of genome-scale ordered RNA structure (GORS) in genomes of positive-stranded RNA viruses: Implications for virus evolution and host persistence.. RNA 2004 Sep;10(9):1337-51.
    doi: 10.1261/rna.7640104pmc: PMC1370621pubmed: 15273323google scholar: lookup
  34. Ramsay JD, Evanoff R, Wilkinson TE Jr, Divers TJ, Knowles DP, Mealey RH. Experimental transmission of equine hepacivirus in horses as a model for hepatitis C virus.. Hepatology 2015 May;61(5):1533-46.
    doi: 10.1002/hep.27689pubmed: 25580897google scholar: lookup
  35. Thomas DL. Global control of hepatitis C: where challenge meets opportunity.. Nat Med 2013 Jul;19(7):850-8.
    doi: 10.1038/nm.3184pmc: PMC4937625pubmed: 23836235google scholar: lookup
  36. Turner SS, Gianella S, Yip MJ, van Seggelen WO, Gillies RD, Foster AL, Barbati ZR, Smith DM, Fierer DS. Shedding of Hepatitis C Virus in Semen of Human Immunodeficiency Virus-Infected Men.. Open Forum Infect Dis 2016 Mar;3(2):ofw057.
    doi: 10.1093/ofid/ofw057pmc: PMC4866572pubmed: 27186582google scholar: lookup
  37. Gather T, Walter S, Todt D, Pfaender S, Brown RJP, Postel A, Becher P, Moritz A, Hansmann F, Baumgaertner W, Feige K, Steinmann E, Cavalleri JV. Vertical transmission of hepatitis C virus-like non-primate hepacivirus in horses.. J Gen Virol 2016 Oct;97(10):2540-2551.
    pubmed: 27461949doi: 10.1099/jgv.0.000561google scholar: lookup
  38. Longdon B, Brockhurst MA, Russell CA, Welch JJ, Jiggins FM. The evolution and genetics of virus host shifts.. PLoS Pathog 2014 Nov;10(11):e1004395.
  39. Rossel S, Marshall F, Peters J, Pilgram T, Adams MD, O'Connor D. Domestication of the donkey: timing, processes, and indicators.. Proc Natl Acad Sci U S A 2008 Mar 11;105(10):3715-20.
    doi: 10.1073/pnas.0709692105pmc: PMC2268817pubmed: 18332433google scholar: lookup
  40. Beja-Pereira A, England PR, Ferrand N, Jordan S, Bakhiet AO, Abdalla MA, Mashkour M, Jordana J, Taberlet P, Luikart G. African origins of the domestic donkey.. Science 2004 Jun 18;304(5678):1781.
    doi: 10.1126/science.1096008pubmed: 15205528google scholar: lookup
  41. Kimura B, Marshall FB, Chen S, Rosenbom S, Moehlman PD, Tuross N, Sabin RC, Peters J, Barich B, Yohannes H, Kebede F, Teclai R, Beja-Pereira A, Mulligan CJ. Ancient DNA from Nubian and Somali wild ass provides insights into donkey ancestry and domestication.. Proc Biol Sci 2011 Jan 7;278(1702):50-7.
    doi: 10.1098/rspb.2010.0708pmc: PMC2992715pubmed: 20667880google scholar: lookup
  42. Pfaender S, Walter S, Todt D, Behrendt P, Doerrbecker J, Wölk B, Engelmann M, Gravemann U, Seltsam A, Steinmann J, Burbelo PD, Klawonn F, Feige K, Pietschmann T, Cavalleri JV, Steinmann E. Assessment of cross-species transmission of hepatitis C virus-related non-primate hepacivirus in a population of humans at high risk of exposure.. J Gen Virol 2015 Sep;96(9):2636-2642.
    doi: 10.1099/vir.0.000208pmc: PMC4857452pubmed: 26041875google scholar: lookup
  43. Levi JE, Cabral SP, Nishiya A, Ferreira S, Romano CM, Polite MB, Pereira RA, Mota MA, Kutner JM. Absence of nonprimate hepacivirus-related genomes in blood donors seroreactive for hepatitis C virus displaying indeterminate blot patterns.. J Viral Hepat 2014 Nov;21(11):e164-6.
    doi: 10.1111/jvh.12252pubmed: 24689976google scholar: lookup
  44. Baechlein C, Fischer N, Grundhoff A, Alawi M, Indenbirken D, Postel A, Baron AL, Offinger J, Becker K, Beineke A, Rehage J, Becher P. Identification of a Novel Hepacivirus in Domestic Cattle from Germany.. J Virol 2015 Jul;89(14):7007-15.
    doi: 10.1128/JVI.00534-15pmc: PMC4473572pubmed: 25926652google scholar: lookup
  45. Gray RR, Tanaka Y, Takebe Y, Magiorkinis G, Buskell Z, Seeff L, Alter HJ, Pybus OG. Evolutionary analysis of hepatitis C virus gene sequences from 1953.. Philos Trans R Soc Lond B Biol Sci 2013 Sep 19;368(1626):20130168.
    doi: 10.1098/rstb.2013.0168pmc: PMC3758194pubmed: 23938759google scholar: lookup
  46. Nyaga PN, Wiggins AD, Priester WA. Epidemiology of equine influenza, risk by age, breed and sex.. Comp Immunol Microbiol Infect Dis 1980;3(1-2):67-73.
    doi: 10.1016/0147-9571(80)90040-5pubmed: 6258851google scholar: lookup
  47. Huang J, Zhao Y, Bai D, Shiraigol W, Li B, Yang L, Wu J, Bao W, Ren X, Jin B, Zhao Q, Li A, Bao S, Bao W, Xing Z, An A, Gao Y, Wei R, Bao Y, Bao T, Han H, Bai H, Bao Y, Zhang Y, Daidiikhuu D, Zhao W, Liu S, Ding J, Ye W, Ding F, Sun Z, Shi Y, Zhang Y, Meng H, Dugarjaviin M. Donkey genome and insight into the imprinting of fast karyotype evolution.. Sci Rep 2015 Sep 16;5:14106.
    doi: 10.1038/srep14106pmc: PMC4571621pubmed: 26373886google scholar: lookup
  48. Bukh J. Animal models for the study of hepatitis C virus infection and related liver disease.. Gastroenterology 2012 May;142(6):1279-1287.e3.
    doi: 10.1053/j.gastro.2012.02.016pubmed: 22537434google scholar: lookup
  49. Alcaide M, Rico C, Ruiz S, Soriguer R, Muñoz J, Figuerola J. Disentangling vector-borne transmission networks: a universal DNA barcoding method to identify vertebrate hosts from arthropod bloodmeals.. PLoS One 2009 Sep 21;4(9):e7092.
  50. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0.. Mol Biol Evol 2013 Dec;30(12):2725-9.
    doi: 10.1093/molbev/mst197pmc: PMC3840312pubmed: 24132122google scholar: lookup
  51. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies.. Bioinformatics 2014 May 1;30(9):1312-3.
  52. Pond SL, Frost SD, Muse SV. HyPhy: hypothesis testing using phylogenies.. Bioinformatics 2005 Mar 1;21(5):676-9.
    doi: 10.1093/bioinformatics/bti079pubmed: 15509596google scholar: lookup
  53. Lemey P, Kosakovsky Pond SL, Drummond AJ, Pybus OG, Shapiro B, Barroso H, Taveira N, Rambaut A. Synonymous substitution rates predict HIV disease progression as a result of underlying replication dynamics.. PLoS Comput Biol 2007 Feb 16;3(2):e29.
  54. Yang Z. PAML: a program package for phylogenetic analysis by maximum likelihood.. Comput Appl Biosci 1997 Oct;13(5):555-6.
  55. Murrell B, Weaver S, Smith MD, Wertheim JO, Murrell S, Aylward A, Eren K, Pollner T, Martin DP, Smith DM, Scheffler K, Kosakovsky Pond SL. Gene-wide identification of episodic selection.. Mol Biol Evol 2015 May;32(5):1365-71.
    doi: 10.1093/molbev/msv035pmc: PMC4408417pubmed: 25701167google scholar: lookup
  56. Murrell B, Moola S, Mabona A, Weighill T, Sheward D, Kosakovsky Pond SL, Scheffler K. FUBAR: a fast, unconstrained bayesian approximation for inferring selection.. Mol Biol Evol 2013 May;30(5):1196-205.
    doi: 10.1093/molbev/mst030pmc: PMC3670733pubmed: 23420840google scholar: lookup
  57. Rambaut A, Lam TT, Max Carvalho L, Pybus OG. Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen).. Virus Evol 2016 Jan;2(1):vew007.
    pmc: PMC4989882pubmed: 27774300doi: 10.1093/ve/vew007google scholar: lookup

Citations

This article has been cited 28 times.
  1. Li YQ, Ghafari M, Holbrook AJ, Boonen I, Amor N, Catalano S, Webster JP, Li YY, Li HT, Vergote V, Maes P, Chong YL, Laudisoit A, Baelo P, Ngoy S, Mbalitini SG, Gembu GC, Akawa PM, Goüy de Bellocq J, Leirs H, Verheyen E, Pybus OG, Katzourakis A, Alagaili AN, Gryseels S, Li YC, Suchard MA, Bletsa M, Lemey P. The evolutionary history of hepaciviruses.. bioRxiv 2023 Jun 30;.
    doi: 10.1101/2023.06.30.547218pubmed: 37425679google scholar: lookup
  2. Yuan S, Yao XY, Lian CY, Kong S, Shao JW, Zhang XL. Molecular detection and genetic characterization of bovine hepacivirus identified in ticks collected from cattle in Harbin, northeastern China.. Front Vet Sci 2023;10:1093898.
    doi: 10.3389/fvets.2023.1093898pubmed: 36937022google scholar: lookup
  3. Khan MZI, Nazli A, Al-Furas H, Asad MI, Ajmal I, Khan D, Shah J, Farooq MA, Jiang W. An overview of viral mutagenesis and the impact on pathogenesis of SARS-CoV-2 variants.. Front Immunol 2022;13:1034444.
    doi: 10.3389/fimmu.2022.1034444pubmed: 36518757google scholar: lookup
  4. Cavalleri JV, Korbacska-Kutasi O, Leblond A, Paillot R, Pusterla N, Steinmann E, Tomlinson J. European College of Equine Internal Medicine consensus statement on equine flaviviridae infections in Europe.. J Vet Intern Med 2022 Nov;36(6):1858-1871.
    doi: 10.1111/jvim.16581pubmed: 36367340google scholar: lookup
  5. Pacchiarotti G, Nardini R, Scicluna MT. Equine Hepacivirus: A Systematic Review and a Meta-Analysis of Serological and Biomolecular Prevalence and a Phylogenetic Update.. Animals (Basel) 2022 Sep 20;12(19).
    doi: 10.3390/ani12192486pubmed: 36230228google scholar: lookup
  6. Jiang J, Hao Y, He B, Su L, Li X, Liu X, Chen C, Chen L, Zhao Z, Mi S, Deng X, Gong W, Tu C. Severe Acute Hepatitis Outbreaks Associated with a Novel Hepacivirus in Rhizomys pruinosus in Hainan, China.. J Virol 2022 Sep 14;96(17):e0078222.
    doi: 10.1128/jvi.00782-22pubmed: 36005760google scholar: lookup
  7. Gömer A, Delarocque J, Puff C, Nocke MK, Reinecke B, Baumgärtner W, Cavalleri JMV, Feige K, Steinmann E, Todt D. Dose-Dependent Hepacivirus Infection Reveals Linkage between Infectious Dose and Immune Response.. Microbiol Spectr 2022 Oct 26;10(5):e0168622.
    doi: 10.1128/spectrum.01686-22pubmed: 35993785google scholar: lookup
  8. Hufsky F, Abecasis A, Agudelo-Romero P, Bletsa M, Brown K, Claus C, Deinhardt-Emmer S, Deng L, Friedel CC, Gismondi MI, Kostaki EG, Kühnert D, Kulkarni-Kale U, Metzner KJ, Meyer IM, Miozzi L, Nishimura L, Paraskevopoulou S, Pérez-Cataluña A, Rahlff J, Thomson E, Tumescheit C, van der Hoek L, Van Espen L, Vandamme AM, Zaheri M, Zuckerman N, Marz M. Women in the European Virus Bioinformatics Center.. Viruses 2022 Jul 12;14(7).
    doi: 10.3390/v14071522pubmed: 35891501google scholar: lookup
  9. Breitfeld J, Fischer N, Tsachev I, Marutsov P, Baymakova M, Plhal R, Keuling O, Becher P, Baechlein C. Expanded Diversity and Host Range of Bovine Hepacivirus-Genomic and Serological Evidence in Domestic and Wild Ruminant Species.. Viruses 2022 Jun 30;14(7).
    doi: 10.3390/v14071457pubmed: 35891438google scholar: lookup
  10. Gömer A, Puff C, Reinecke B, Bracht S, Conze M, Baumgärtner W, Steinmann J, Feige K, Cavalleri JMV, Steinmann E, Todt D. Experimental cross-species infection of donkeys with equine hepacivirus and analysis of host immune signatures.. One Health Outlook 2022 May 9;4(1):9.
    doi: 10.1186/s42522-022-00065-ypubmed: 35527255google scholar: lookup
  11. Zhang XL, Yao XY, Zhang YQ, Lv ZH, Liu H, Sun J, Shao JW. A Highly Divergent Hepacivirus Identified in Domestic Ducks Further Reveals the Genetic Diversity of Hepaciviruses.. Viruses 2022 Feb 11;14(2).
    doi: 10.3390/v14020371pubmed: 35215964google scholar: lookup
  12. Röhrs S, Begeman L, Straub BK, Boadella M, Hanke D, Wernike K, Drewes S, Hoffmann B, Keller M, Drexler JF, Drosten C, Höper D, Kuiken T, Ulrich RG, Beer M. The Bank Vole (Clethrionomys glareolus)-Small Animal Model for Hepacivirus Infection.. Viruses 2021 Dec 3;13(12).
    doi: 10.3390/v13122421pubmed: 34960690google scholar: lookup
  13. Shao JW, Guo LY, Yuan YX, Ma J, Chen JM, Liu Q. A Novel Subtype of Bovine Hepacivirus Identified in Ticks Reveals the Genetic Diversity and Evolution of Bovine Hepacivirus.. Viruses 2021 Nov 2;13(11).
    doi: 10.3390/v13112206pubmed: 34835012google scholar: lookup
  14. Reinecke B, Klöhn M, Brüggemann Y, Kinast V, Todt D, Stang A, Badenhorst M, Koeppel K, Guthrie A, Groner U, Puff C, de le Roi M, Baumgärtner W, Cavalleri JV, Steinmann E. Clinical Course of Infection and Cross-Species Detection of Equine Parvovirus-Hepatitis.. Viruses 2021 Jul 26;13(8).
    doi: 10.3390/v13081454pubmed: 34452320google scholar: lookup
  15. Bletsa M, Vrancken B, Gryseels S, Boonen I, Fikatas A, Li Y, Laudisoit A, Lequime S, Bryja J, Makundi R, Meheretu Y, Akaibe BD, Mbalitini SG, Van de Perre F, Van Houtte N, Těšíková J, Wollants E, Van Ranst M, Pybus OG, Drexler JF, Verheyen E, Leirs H, Gouy de Bellocq J, Lemey P. Molecular detection and genomic characterization of diverse hepaciviruses in African rodents.. Virus Evol 2021 Jan;7(1):veab036.
    doi: 10.1093/ve/veab036pubmed: 34221451google scholar: lookup
  16. Ramsauer AS, Badenhorst M, Cavalleri JV. Equine parvovirus hepatitis.. Equine Vet J 2021 Sep;53(5):886-894.
    doi: 10.1111/evj.13477pubmed: 34101906google scholar: lookup
  17. Rasche A, Lehmann F, Goldmann N, Nagel M, Moreira-Soto A, Nobach D, de Oliveira Carneiro I, Osterrieder N, Greenwood AD, Steinmann E, Lukashev AN, Schuler G, Glebe D, Drexler JF. A hepatitis B virus causes chronic infections in equids worldwide.. Proc Natl Acad Sci U S A 2021 Mar 30;118(13).
    doi: 10.1073/pnas.2013982118pubmed: 33723007google scholar: lookup
  18. Câmara RJF, Bueno BL, Resende CF, Balasuriya UBR, Sakamoto SM, Reis JKPD. Viral Diseases that Affect Donkeys and Mules.. Animals (Basel) 2020 Nov 25;10(12).
    doi: 10.3390/ani10122203pubmed: 33255568google scholar: lookup
  19. Moreira-Soto A, Arroyo-Murillo F, Sander AL, Rasche A, Corman V, Tegtmeyer B, Steinmann E, Corrales-Aguilar E, Wieseke N, Avey-Arroyo J, Drexler JF. Cross-order host switches of hepatitis C-related viruses illustrated by a novel hepacivirus from sloths.. Virus Evol 2020 Jul;6(2):veaa033.
    doi: 10.1093/ve/veaa033pubmed: 32704383google scholar: lookup
  20. Cagliani R, Forni D, Sironi M. Mode and tempo of human hepatitis virus evolution.. Comput Struct Biotechnol J 2019;17:1384-1395.
    doi: 10.1016/j.csbj.2019.09.007pubmed: 31768229google scholar: lookup
  21. Tomlinson JE, Kapoor A, Kumar A, Tennant BC, Laverack MA, Beard L, Delph K, Davis E, Schott Ii H, Lascola K, Holbrook TC, Johnson P, Taylor SD, McKenzie E, Carter-Arnold J, Setlakwe E, Fultz L, Brakenhoff J, Ruby R, Trivedi S, Van de Walle GR, Renshaw RW, Dubovi EJ, Divers TJ. Viral testing of 18 consecutive cases of equine serum hepatitis: A prospective study (2014-2018).. J Vet Intern Med 2019 Jan;33(1):251-257.
    doi: 10.1111/jvim.15368pubmed: 30520162google scholar: lookup
  22. Rasche A, Sander AL, Corman VM, Drexler JF. Evolutionary biology of human hepatitis viruses.. J Hepatol 2019 Mar;70(3):501-520.
    doi: 10.1016/j.jhep.2018.11.010pubmed: 30472320google scholar: lookup
  23. Geoghegan JL, Holmes EC. The phylogenomics of evolving virus virulence.. Nat Rev Genet 2018 Dec;19(12):756-769.
    doi: 10.1038/s41576-018-0055-5pubmed: 30305704google scholar: lookup
  24. Ramsay JD, Evanoff R, Mealey RH. Hepacivirus A Infection in Horses Defines Distinct Envelope Hypervariable Regions and Elucidates Potential Roles of Viral Strain and Adaptive Immune Status in Determining Envelope Diversity and Infection Outcome.. J Virol 2018 Sep 15;92(18).
    doi: 10.1128/JVI.00314-18pubmed: 29976666google scholar: lookup
  25. Forni D, Cagliani R, Pontremoli C, Pozzoli U, Vertemara J, De Gioia L, Clerici M, Sironi M. Evolutionary Analysis Provides Insight Into the Origin and Adaptation of HCV.. Front Microbiol 2018;9:854.
    doi: 10.3389/fmicb.2018.00854pubmed: 29765366google scholar: lookup
  26. Tanaka T, Otoguro T, Yamashita A, Kasai H, Fukuhara T, Matsuura Y, Moriishi K. Roles of the 5' Untranslated Region of Nonprimate Hepacivirus in Translation Initiation and Viral Replication.. J Virol 2018 Apr 1;92(7).
    doi: 10.1128/JVI.01997-17pubmed: 29343570google scholar: lookup
  27. Geoghegan JL, Holmes EC. Predicting virus emergence amid evolutionary noise.. Open Biol 2017 Oct;7(10).
    doi: 10.1098/rsob.170189pubmed: 29070612google scholar: lookup
  28. Geoghegan JL, Duchêne S, Holmes EC. Comparative analysis estimates the relative frequencies of co-divergence and cross-species transmission within viral families.. PLoS Pathog 2017 Feb;13(2):e1006215.
    doi: 10.1371/journal.ppat.1006215pubmed: 28178344google scholar: lookup