FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / PLoS Pathog / Absence of adaptive evolution is the main barrier against in...
PLoS pathogens2019; 15(2); e1007531; doi: 10.1371/journal.ppat.1007531

Absence of adaptive evolution is the main barrier against influenza emergence in horses in Asia despite frequent virus interspecies transmission from wild birds.

Abstract: Virus ecology and evolution play a central role in disease emergence. However, their relative roles will vary depending on the viruses and ecosystems involved. We combined field studies, phylogenetics and experimental infections to document with unprecedented detail the stages that precede initial outbreaks during viral emergence in nature. Using serological surveys we showed that in the absence of large-scale outbreaks, horses in Mongolia are routinely exposed to and infected by avian influenza viruses (AIVs) circulating among wild birds. Some of those AIVs are genetically related to an avian-origin virus that caused an epizootic in horses in 1989. Experimental infections showed that most AIVs replicate in the equine respiratory tract without causing lesions, explaining the absence of outbreaks of disease. Our results show that AIVs infect horses but do not spread, or they infect and spread but do not cause disease. Thus, the failure of AIVs to evolve greater transmissibility and to cause disease in horses is in this case the main barrier preventing disease emergence.
Get Full Text
Publication Date: 2019-02-07 PubMed ID: 30731004PubMed Central: PMC6366691DOI: 10.1371/journal.ppat.1007531Google 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.
LinkedInCopy
  • Journal Article
  • Research Support
  • Non-U.S. Gov't
  • Research Support
  • U.S. Gov't
  • P.H.S.

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.

The researchers of this study focused on understanding why influenza viruses, despite frequently being transmitted from wild birds to horses in Mongolia, don’t cause large-scale disease outbreaks. They discovered that the lack of adaptive evolution is primarily responsible as it prevents the avian influenza viruses (AIVs) from spreading much and causing disease in the infected horses.

Study Objective and Approach

  • The purpose of this research was to elucidate the factors responsible for preventing the emergence of disease in horses in Asia, despite them being regularly exposed to avian influenza viruses (AIVs).
  • Researchers combined different methodologies such as field studies, phylogenetic analysis (the study of evolutionary relationships), and experimental infections to comprehensively understand the steps leading up to initial outbreaks of viral diseases in natural environments.
  • A serological survey, a test to detect antibodies in the blood, was also carried out to determine the prevalence of AIVs in horses.

Findings

  • In the absence of significant disease outbreaks, it was discovered that horses in Mongolia often come into direct contact with and get infected by AIVs, which are commonly found in wild birds.
  • Interestingly, some of these AIVs were found to be genetically similar to an avian-origin virus that had caused an epidemic in horses in the year 1989.

Experimental Infections and Implication

  • In controlled experiments, it was observed that most AIVs can colonize the respiratory tract of horses without causing any lesions or overt signs of disease.
  • This observation helped explain the lack of disease outbreaks despite frequent infections in horses.
  • The findings demonstrate a complicated dynamic where AIVs can infect horses but don’t spread significantly. Alternatively, they might infect and spread but still don’t cause disease.
  • The lack of adaptive evolution, in other words, the inability of AIVs to change in a way that allows them to transmit more effectively and cause disease in horses, is identified to be the primary barrier that prevents large-scale disease outbreaks.

Cite This Article

APA
Zhu H, Damdinjav B, Gonzalez G, Patrono LV, Ramirez-Mendoza H, Amat JAR, Crispell J, Parr YA, Hammond TA, Shiilegdamba E, Leung YHC, Peiris M, Marshall JF, Hughes J, Gilbert M, Murcia PR. (2019). Absence of adaptive evolution is the main barrier against influenza emergence in horses in Asia despite frequent virus interspecies transmission from wild birds. PLoS Pathog, 15(2), e1007531. https://doi.org/10.1371/journal.ppat.1007531

Publication

PLoS pathogens
ISSN: 1553-7374
NlmUniqueID: 101238921
Country: United States
Language: English
Volume: 15
Issue: 2
Pages: e1007531
PII: e1007531

Researcher Affiliations

Zhu, Henan
  • MRC-University of Glasgow Centre for Virus Research, Glasgow, United Kingdom.
Damdinjav, Batchuluun
  • State Central Veterinary Laboratory, Transboundary Animal Disease Laboratory, Avian Influenza Section, Ulaanbaatar, Mongolia.
Gonzalez, Gaelle
  • MRC-University of Glasgow Centre for Virus Research, Glasgow, United Kingdom.
Patrono, Livia Victoria
  • MRC-University of Glasgow Centre for Virus Research, Glasgow, United Kingdom.
  • Project Group Epidemiology of Highly Pathogenic Microorganisms, Robert Koch Institute, Berlin, Germany.
Ramirez-Mendoza, Humberto
  • Departamento de Microbiología e Inmunología, Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autónoma de México, Ciudad de Mexico, México.
Amat, Julien A R
  • MRC-University of Glasgow Centre for Virus Research, Glasgow, United Kingdom.
Crispell, Joanna
  • MRC-University of Glasgow Centre for Virus Research, Glasgow, United Kingdom.
Parr, Yasmin Amy
  • MRC-University of Glasgow Centre for Virus Research, Glasgow, United Kingdom.
Hammond, Toni-Ann
  • Animal Health Trust, Lanwades Park, Kentford, Newmarket, Suffolk, United Kingdom.
Shiilegdamba, Enkhtuvshin
  • Wildlife Conservation Society, Bronx, NY, United States of America.
Leung, Y H Connie
  • School of Public Health, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong Special Administrative Region, China.
  • Laboratory Animal Unit, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong Special Administrative Region, China.
Peiris, Malik
  • School of Public Health, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong Special Administrative Region, China.
Marshall, John F
  • Weipers Centre Equine Hospital, School of Veterinary Medicine, University of Glasgow, Glasgow, United Kingdom.
Hughes, Joseph
  • MRC-University of Glasgow Centre for Virus Research, Glasgow, United Kingdom.
Gilbert, Martin
  • Wildlife Conservation Society, Bronx, NY, United States of America.
  • Boyd Orr Centre for Population and Ecosystem Health, Institute of Biodiversity, Animal Health and Comparative Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, United Kingdom.
  • Department of Population Medicine and Diagnostic Science, College of Veterinary Medicine, Cornell University, Ithaca, NY, United States of America.
Murcia, Pablo R
  • MRC-University of Glasgow Centre for Virus Research, Glasgow, United Kingdom.

MeSH Terms

  • Animals
  • Animals, Wild
  • Asia
  • Biological Evolution
  • Birds
  • Disease Outbreaks
  • Disease Transmission, Infectious / veterinary
  • Evolution, Molecular
  • Horses / genetics
  • Horses / immunology
  • Humans
  • Influenza in Birds / genetics
  • Influenza in Birds / immunology
  • Influenza, Human
  • Orthomyxoviridae Infections / veterinary
  • Phylogeny

Grant Funding

  • MC_UU_12014/12 / Medical Research Council
  • MC_UU_12014/9 / Medical Research Council

Conflict of Interest Statement

The authors have declared that no competing interests exist.

References

This article includes 58 references
  1. Anthony SJ, Epstein JH, Murray KA, Navarrete-Macias I, Zambrana-Torrelio CM, Solovyov A, Ojeda-Flores R, Arrigo NC, Islam A, Ali Khan S, Hosseini P, Bogich TL, Olival KJ, Sanchez-Leon MD, Karesh WB, Goldstein T, Luby SP, Morse SS, Mazet JA, Daszak P, Lipkin WI. A strategy to estimate unknown viral diversity in mammals.. mBio 2013 Sep 3;4(5):e00598-13.
    doi: 10.1128/mBio.00598-13pmc: PMC3760253pubmed: 24003179google scholar: lookup
  2. Ayouba A, Souquières S, Njinku B, Martin PM, Müller-Trutwin MC, Roques P, Barré-Sinoussi F, Mauclère P, Simon F, Nerrienet E. HIV-1 group N among HIV-1-seropositive individuals in Cameroon.. AIDS 2000 Nov 10;14(16):2623-5.
    pubmed: 11101082doi: 10.1097/00002030-200011100-00033google scholar: lookup
  3. Peeters M, Gueye A, Mboup S, Bibollet-Ruche F, Ekaza E, Mulanga C, Ouedrago R, Gandji R, Mpele P, Dibanga G, Koumare B, Saidou M, Esu-Williams E, Lombart JP, Badombena W, Luo N, Vanden Haesevelde M, Delaporte E. Geographical distribution of HIV-1 group O viruses in Africa.. AIDS 1997 Mar 15;11(4):493-8.
    pubmed: 9084797doi: 10.1097/00002030-199704000-00013google scholar: lookup
  4. Vallari A, Holzmayer V, Harris B, Yamaguchi J, Ngansop C, Makamche F, Mbanya D, Kaptué L, Ndembi N, Gürtler L, Devare S, Brennan CA. Confirmation of putative HIV-1 group P in Cameroon.. J Virol 2011 Feb;85(3):1403-7.
    doi: 10.1128/JVI.02005-10pmc: PMC3020498pubmed: 21084486google scholar: lookup
  5. Kirkland PD, Finlaison DS, Crispe E, Hurt AC. Influenza virus transmission from horses to dogs, Australia.. Emerg Infect Dis 2010 Apr;16(4):699-702.
    doi: 10.3201/eid1604.091489pmc: PMC3321956pubmed: 20350392google scholar: lookup
  6. Daly JM, Blunden AS, Macrae S, Miller J, Bowman SJ, Kolodziejek J, Nowotny N, Smith KC. Transmission of equine influenza virus to English foxhounds.. Emerg Infect Dis 2008 Mar;14(3):461-4.
    doi: 10.3201/eid1403.070643pmc: PMC2570814pubmed: 18325262google scholar: lookup
  7. Crawford PC, Dubovi EJ, Castleman WL, Stephenson I, Gibbs EP, Chen L, Smith C, Hill RC, Ferro P, Pompey J, Bright RA, Medina MJ, Johnson CM, Olsen CW, Cox NJ, Klimov AI, Katz JM, Donis RO. Transmission of equine influenza virus to dogs.. Science 2005 Oct 21;310(5747):482-5.
    doi: 10.1126/science.1117950pubmed: 16186182google scholar: lookup
  8. Lai S, Qin Y, Cowling BJ, Ren X, Wardrop NA, Gilbert M, Tsang TK, Wu P, Feng L, Jiang H, Peng Z, Zheng J, Liao Q, Li S, Horby PW, Farrar JJ, Gao GF, Tatem AJ, Yu H. Global epidemiology of avian influenza A H5N1 virus infection in humans, 1997-2015: a systematic review of individual case data.. Lancet Infect Dis 2016 Jul;16(7):e108-e118.
    doi: 10.1016/S1473-3099(16)00153-5pmc: PMC4933299pubmed: 27211899google scholar: lookup
  9. Dalziel BD, Huang K, Geoghegan JL, Arinaminpathy N, Dubovi EJ, Grenfell BT, Ellner SP, Holmes EC, Parrish CR. Contact heterogeneity, rather than transmission efficiency, limits the emergence and spread of canine influenza virus.. PLoS Pathog 2014 Oct;10(10):e1004455.
    doi: 10.1371/journal.ppat.1004455pmc: PMC4207809pubmed: 25340642google scholar: lookup
  10. Geoghegan JL, Senior AM, Holmes EC. Pathogen population bottlenecks and adaptive landscapes: overcoming the barriers to disease emergence.. Proc Biol Sci 2016 Aug 31;283(1837).
    doi: 10.1098/rspb.2016.0727pmc: PMC5013787pubmed: 27581875google scholar: lookup
  11. Worobey M, Han GZ, Rambaut A. Genesis and pathogenesis of the 1918 pandemic H1N1 influenza A virus.. Proc Natl Acad Sci U S A 2014 Jun 3;111(22):8107-12.
    doi: 10.1073/pnas.1324197111pmc: PMC4050607pubmed: 24778238google scholar: lookup
  12. Gostic KM, Ambrose M, Worobey M, Lloyd-Smith JO. Potent protection against H5N1 and H7N9 influenza via childhood hemagglutinin imprinting.. Science 2016 Nov 11;354(6313):722-726.
    doi: 10.1126/science.aag1322pmc: PMC5134739pubmed: 27846599google scholar: lookup
  13. Lo Iacono G, Cunningham AA, Fichet-Calvet E, Garry RF, Grant DS, Leach M, Moses LM, Nichols G, Schieffelin JS, Shaffer JG, Webb CT, Wood JL. A Unified Framework for the Infection Dynamics of Zoonotic Spillover and Spread.. PLoS Negl Trop Dis 2016 Sep;10(9):e0004957.
    doi: 10.1371/journal.pntd.0004957pmc: PMC5010258pubmed: 27588425google scholar: lookup
  14. Dugan VG, Chen R, Spiro DJ, Sengamalay N, Zaborsky J, Ghedin E, Nolting J, Swayne DE, Runstadler JA, Happ GM, Senne DA, Wang R, Slemons RD, Holmes EC, Taubenberger JK. The evolutionary genetics and emergence of avian influenza viruses in wild birds.. PLoS Pathog 2008 May 30;4(5):e1000076.
    doi: 10.1371/journal.ppat.1000076pmc: PMC2387073pubmed: 18516303google scholar: lookup
  15. Olson SH, Parmley J, Soos C, Gilbert M, Latorre-Margalef N, Hall JS, Hansbro PM, Leighton F, Munster V, Joly D. Sampling strategies and biodiversity of influenza A subtypes in wild birds.. PLoS One 2014;9(3):e90826.
    doi: 10.1371/journal.pone.0090826pmc: PMC3944928pubmed: 24599502google scholar: lookup
  16. WADDELL GH, TEIGLAND MB, SIGEL MM. A NEW INFLUENZA VIRUS ASSOCIATED WITH EQUINE RESPIRATORY DISEASE.. J Am Vet Med Assoc 1963 Sep 15;143:587-90.
    pubmed: 14077956
  17. Anthony SJ, St Leger JA, Pugliares K, Ip HS, Chan JM, Carpenter ZW, Navarrete-Macias I, Sanchez-Leon M, Saliki JT, Pedersen J, Karesh W, Daszak P, Rabadan R, Rowles T, Lipkin WI. Emergence of fatal avian influenza in New England harbor seals.. mBio 2012;3(4):e00166-12.
    doi: 10.1128/mBio.00166-12pmc: PMC3419516pubmed: 22851656google scholar: lookup
  18. Tu J, Zhou H, Jiang T, Li C, Zhang A, Guo X, Zou W, Chen H, Jin M. Isolation and molecular characterization of equine H3N8 influenza viruses from pigs in China.. Arch Virol 2009;154(5):887-90.
    doi: 10.1007/s00705-009-0381-1pubmed: 19396578google scholar: lookup
  19. Yondon M, Zayat B, Nelson MI, Heil GL, Anderson BD, Lin X, Halpin RA, McKenzie PP, White SK, Wentworth DE, Gray GC. Equine influenza A(H3N8) virus isolated from Bactrian camel, Mongolia.. Emerg Infect Dis 2014 Dec;20(12):2144-7.
    doi: 10.3201/eid2012.140435pmc: PMC4257804pubmed: 25418532google scholar: lookup
  20. SOVINOVA O, TUMOVA B, POUSKA F, NEMEC J. Isolation of a virus causing respiratory disease in horses.. Acta Virol 1958 Jan-Mar;2(1):52-61.
    pubmed: 13533033
  21. Guo Y, Wang M, Kawaoka Y, Gorman O, Ito T, Saito T, Webster RG. Characterization of a new avian-like influenza A virus from horses in China.. Virology 1992 May;188(1):245-55.
    pubmed: 1314452doi: 10.1016/0042-6822(92)90754-dgoogle scholar: lookup
  22. Guo Y, Wang M, Zheng GS, Li WK, Kawaoka Y, Webster RG. Seroepidemiological and molecular evidence for the presence of two H3N8 equine influenza viruses in China in 1993-94.. J Gen Virol 1995 Aug;76 ( Pt 8):2009-14.
    doi: 10.1099/0022-1317-76-8-2009pubmed: 7636481google scholar: lookup
  23. Hurt AC, Vijaykrishna D, Butler J, Baas C, Maurer-Stroh S, Silva-de-la-Fuente MC, Medina-Vogel G, Olsen B, Kelso A, Barr IG, González-Acuña D. Detection of evolutionarily distinct avian influenza a viruses in antarctica.. mBio 2014 May 6;5(3):e01098-14.
    doi: 10.1128/mBio.01098-14pmc: PMC4010832pubmed: 24803521google scholar: lookup
  24. Spackman E, McCracken KG, Winker K, Swayne DE. H7N3 avian influenza virus found in a South American wild duck is related to the Chilean 2002 poultry outbreak, contains genes from equine and North American wild bird lineages, and is adapted to domestic turkeys.. J Virol 2006 Aug;80(15):7760-4.
    doi: 10.1128/JVI.00445-06pmc: PMC1563721pubmed: 16840356google scholar: lookup
  25. Statistics AaPCoA. Livestock Statistics in Mongolia. 2016.
  26. Chan S. Important bird areas in Asia: key sites for conservation. BirdLife International; 2004.
  27. Sakoda Y, Sugar S, Batchluun D, Erdene-Ochir TO, Okamatsu M, Isoda N, Soda K, Takakuwa H, Tsuda Y, Yamamoto N, Kishida N, Matsuno K, Nakayama E, Kajihara M, Yokoyama A, Takada A, Sodnomdarjaa R, Kida H. Characterization of H5N1 highly pathogenic avian influenza virus strains isolated from migratory waterfowl in Mongolia on the way back from the southern Asia to their northern territory.. Virology 2010 Oct 10;406(1):88-94.
    doi: 10.1016/j.virol.2010.07.007pubmed: 20673942google scholar: lookup
  28. Yondon M, Heil GL, Burks JP, Zayat B, Waltzek TB, Jamiyan BO, McKenzie PP, Krueger WS, Friary JA, Gray GC. Isolation and characterization of H3N8 equine influenza A virus associated with the 2011 epizootic in Mongolia.. Influenza Other Respir Viruses 2013 Sep;7(5):659-65.
    doi: 10.1111/irv.12069pmc: PMC3626732pubmed: 23289427google scholar: lookup
  29. Kang HM, Kim MC, Choi JG, Batchuluun D, Erdene-Ochir TO, Paek MR, Sodnomdarjaa R, Kwon JH, Lee YJ. Genetic analyses of avian influenza viruses in Mongolia, 2007 to 2009, and their relationships with Korean isolates from domestic poultry and wild birds.. Poult Sci 2011 Oct;90(10):2229-42.
    doi: 10.3382/ps.2011-01524pubmed: 21934005google scholar: lookup
  30. Tamuri AU, Dos Reis M, Hay AJ, Goldstein RA. Identifying changes in selective constraints: host shifts in influenza.. PLoS Comput Biol 2009 Nov;5(11):e1000564.
    doi: 10.1371/journal.pcbi.1000564pmc: PMC2770840pubmed: 19911053google scholar: lookup
  31. Gabriel G, Dauber B, Wolff T, Planz O, Klenk HD, Stech J. The viral polymerase mediates adaptation of an avian influenza virus to a mammalian host.. Proc Natl Acad Sci U S A 2005 Dec 20;102(51):18590-5.
    doi: 10.1073/pnas.0507415102pmc: PMC1317936pubmed: 16339318google scholar: lookup
  32. Herfst S, Schrauwen EJ, Linster M, Chutinimitkul S, de Wit E, Munster VJ, Sorrell EM, Bestebroer TM, Burke DF, Smith DJ, Rimmelzwaan GF, Osterhaus AD, Fouchier RA. Airborne transmission of influenza A/H5N1 virus between ferrets.. Science 2012 Jun 22;336(6088):1534-41.
    doi: 10.1126/science.1213362pmc: PMC4810786pubmed: 22723413google scholar: lookup
  33. Murcia PR, Baillie GJ, Daly J, Elton D, Jervis C, Mumford JA, Newton R, Parrish CR, Hoelzer K, Dougan G, Parkhill J, Lennard N, Ormond D, Moule S, Whitwham A, McCauley JW, McKinley TJ, Holmes EC, Grenfell BT, Wood JL. Intra- and interhost evolutionary dynamics of equine influenza virus.. J Virol 2010 Jul;84(14):6943-54.
    doi: 10.1128/JVI.00112-10pmc: PMC2898244pubmed: 20444896google scholar: lookup
  34. Muranaka M, Yamanaka T, Katayama Y, Niwa H, Oku K, Matsumura T, Oyamada T. Time-related Pathological Changes in Horses Experimentally Inoculated with Equine Influenza A Virus.. J Equine Sci 2012;23(2):17-26.
    doi: 10.1294/jes.23.17pmc: PMC4013977pubmed: 24833992google scholar: lookup
  35. Parrish CR, Holmes EC, Morens DM, Park EC, Burke DS, Calisher CH, Laughlin CA, Saif LJ, Daszak P. Cross-species virus transmission and the emergence of new epidemic diseases.. Microbiol Mol Biol Rev 2008 Sep;72(3):457-70.
    doi: 10.1128/MMBR.00004-08pmc: PMC2546865pubmed: 18772285google scholar: lookup
  36. Cowling BJ, Jin L, Lau EH, Liao Q, Wu P, Jiang H, Tsang TK, Zheng J, Fang VJ, Chang Z, Ni MY, Zhang Q, Ip DK, Yu J, Li Y, Wang L, Tu W, Meng L, Wu JT, Luo H, Li Q, Shu Y, Li Z, Feng Z, Yang W, Wang Y, Leung GM, Yu H. Comparative epidemiology of human infections with avian influenza A H7N9 and H5N1 viruses in China: a population-based study of laboratory-confirmed cases.. Lancet 2013 Jul 13;382(9887):129-37.
    doi: 10.1016/S0140-6736(13)61171-Xpmc: PMC3777567pubmed: 23803488google scholar: lookup
  37. Chen H, Yuan H, Gao R, Zhang J, Wang D, Xiong Y, Fan G, Yang F, Li X, Zhou J, Zou S, Yang L, Chen T, Dong L, Bo H, Zhao X, Zhang Y, Lan Y, Bai T, Dong J, Li Q, Wang S, Zhang Y, Li H, Gong T, Shi Y, Ni X, Li J, Zhou J, Fan J, Wu J, Zhou X, Hu M, Wan J, Yang W, Li D, Wu G, Feng Z, Gao GF, Wang Y, Jin Q, Liu M, Shu Y. Clinical and epidemiological characteristics of a fatal case of avian influenza A H10N8 virus infection: a descriptive study.. Lancet 2014 Feb 22;383(9918):714-21.
    doi: 10.1016/S0140-6736(14)60111-2pubmed: 24507376google scholar: lookup
  38. Van Hoeven N, Pappas C, Belser JA, Maines TR, Zeng H, García-Sastre A, Sasisekharan R, Katz JM, Tumpey TM. Human HA and polymerase subunit PB2 proteins confer transmission of an avian influenza virus through the air.. Proc Natl Acad Sci U S A 2009 Mar 3;106(9):3366-71.
    doi: 10.1073/pnas.0813172106pmc: PMC2651239pubmed: 19211790google scholar: lookup
  39. Cauldwell AV, Long JS, Moncorgé O, Barclay WS. Viral determinants of influenza A virus host range.. J Gen Virol 2014 Jun;95(Pt 6):1193-1210.
    doi: 10.1099/vir.0.062836-0pubmed: 24584475google scholar: lookup
  40. Newton R, Cooke A, Elton D, Bryant N, Rash A, Bowman S, Blunden T, Miller J, Hammond TA, Camm I, Day M. Canine influenza virus: cross-species transmission from horses.. Vet Rec 2007 Jul 28;161(4):142-3.
    pubmed: 17660470doi: 10.1136/vr.161.4.142-agoogle scholar: lookup
  41. Anderson TC, Bromfield CR, Crawford PC, Dodds WJ, Gibbs EP, Hernandez JA. Serological evidence of H3N8 canine influenza-like virus circulation in USA dogs prior to 2004.. Vet J 2012 Mar;191(3):312-6.
    doi: 10.1016/j.tvjl.2011.11.010pubmed: 22178358google scholar: lookup
  42. Sack A, Daramragchaa U, Chuluunbaatar M, Gonchigoo B, Bazartseren B, Tsogbadrakh N, Gray GC. Low Prevalence of Enzootic Equine Influenza Virus among Horses in Mongolia.. Pathogens 2017 Nov 30;6(4).
    doi: 10.3390/pathogens6040061pmc: PMC5750585pubmed: 29189713google scholar: lookup
  43. Kuiken T, Holmes EC, McCauley J, Rimmelzwaan GF, Williams CS, Grenfell BT. Host species barriers to influenza virus infections.. Science 2006 Apr 21;312(5772):394-7.
    doi: 10.1126/science.1122818pubmed: 16627737google scholar: lookup
  44. Abdel-Moneim AS, Abdel-Ghany AE, Shany SA. Isolation and characterization of highly pathogenic avian influenza virus subtype H5N1 from donkeys.. J Biomed Sci 2010 Apr 14;17(1):25.
    doi: 10.1186/1423-0127-17-25pmc: PMC2867947pubmed: 20398268google scholar: lookup
  45. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P. Global trends in emerging infectious diseases.. Nature 2008 Feb 21;451(7181):990-3.
    doi: 10.1038/nature06536pmc: PMC5960580pubmed: 18288193google scholar: lookup
  46. Gilbert M, Jambal L, Karesh WB, Fine A, Shiilegdamba E, Dulam P, Sodnomdarjaa R, Ganzorig K, Batchuluun D, Tseveenmyadag N, Bolortuya P, Cardona CJ, Leung CY, Peiris JS, Spackman E, Swayne DE, Joly DO. Highly pathogenic avian influenza virus among wild birds in Mongolia.. PLoS One 2012;7(9):e44097.
    doi: 10.1371/journal.pone.0044097pmc: PMC3439473pubmed: 22984464google scholar: lookup
  47. INFL WA, MA NU U. WHO manual on animal influenza diagnosis and surveillance. Geneva: World Health Organization; 2002.
  48. Baillie GJ, Galiano M, Agapow PM, Myers R, Chiam R, Gall A, Palser AL, Watson SJ, Hedge J, Underwood A, Platt S, McLean E, Pebody RG, Rambaut A, Green J, Daniels R, Pybus OG, Kellam P, Zambon M. Evolutionary dynamics of local pandemic H1N1/2009 influenza virus lineages revealed by whole-genome analysis.. J Virol 2012 Jan;86(1):11-8.
    doi: 10.1128/JVI.05347-11pmc: PMC3255882pubmed: 22013031google scholar: lookup
  49. Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs.. Genome Res 2008 May;18(5):821-9.
    doi: 10.1101/gr.074492.107pmc: PMC2336801pubmed: 18349386google scholar: lookup
  50. Lunter G, Goodson M. Stampy: a statistical algorithm for sensitive and fast mapping of Illumina sequence reads.. Genome Res 2011 Jun;21(6):936-9.
    doi: 10.1101/gr.111120.110pmc: PMC3106326pubmed: 20980556google scholar: lookup
  51. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput.. Nucleic Acids Res 2004;32(5):1792-7.
    doi: 10.1093/nar/gkh340pmc: PMC390337pubmed: 15034147google scholar: lookup
  52. Suyama M, Torrents D, Bork P. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments.. Nucleic Acids Res 2006 Jul 1;34(Web Server issue):W609-12.
    doi: 10.1093/nar/gkl315pmc: PMC1538804pubmed: 16845082google scholar: lookup
  53. Gouy M, Guindon S, Gascuel O. SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building.. Mol Biol Evol 2010 Feb;27(2):221-4.
    doi: 10.1093/molbev/msp259pubmed: 19854763google scholar: lookup
  54. Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences.. Bioinformatics 2006 Jul 1;22(13):1658-9.
    doi: 10.1093/bioinformatics/btl158pubmed: 16731699google scholar: lookup
  55. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies.. Bioinformatics 2014 May 1;30(9):1312-3.
    doi: 10.1093/bioinformatics/btu033pmc: PMC3998144pubmed: 24451623google scholar: lookup
  56. Gonzalez G, Marshall JF, Morrell J, Robb D, McCauley JW, Perez DR, Parrish CR, Murcia PR. Infection and pathogenesis of canine, equine, and human influenza viruses in canine tracheas.. J Virol 2014 Aug;88(16):9208-19.
    doi: 10.1128/JVI.00887-14pmc: PMC4136294pubmed: 24899186google scholar: lookup
  57. Patrono LV, Bonfante F, Zanardello C, Terregino C, Capua I, Murcia PR. Phylogenetically distinct equine influenza viruses show different tropism for the swine respiratory tract.. J Gen Virol 2015 May;96(Pt 5):969-974.
    doi: 10.1099/vir.0.000049pmc: PMC4631061pubmed: 25593159google scholar: lookup
  58. Feng KH, Gonzalez G, Deng L, Yu H, Tse VL, Huang L, Huang K, Wasik BR, Zhou B, Wentworth DE, Holmes EC, Chen X, Varki A, Murcia PR, Parrish CR. Equine and Canine Influenza H3N8 Viruses Show Minimal Biological Differences Despite Phylogenetic Divergence.. J Virol 2015 Jul;89(13):6860-73.
    doi: 10.1128/JVI.00521-15pmc: PMC4468500pubmed: 25903329google scholar: lookup

Citations

This article has been cited 13 times.
  1. Wasik BR, Rothschild E, Voorhees IEH, Reedy SE, Murcia PR, Pusterla N, Chambers TM, Goodman LB, Holmes EC, Kile JC, Parrish CR. Understanding the divergent evolution and epidemiology of H3N8 influenza viruses in dogs and horses. Virus Evol 2023;9(2):vead052.
    doi: 10.1093/ve/vead052pubmed: 37692894google scholar: lookup
  2. He Z, Wang X, Lin Y, Feng S, Huang X, Zhao L, Zhang J, Ding Y, Li W, Yuan R, Jiao P. Genetic characteristics of waterfowl-origin H5N6 highly pathogenic avian influenza viruses and their pathogenesis in ducks and chickens. Front Microbiol 2023;14:1211355.
    doi: 10.3389/fmicb.2023.1211355pubmed: 37405154google scholar: lookup
  3. Guo X, Zhang Z, Lin C, Ren H, Li Y, Zhang Y, Qu Y, Li H, Ma S, Xia H, Sun R, Zu H, Lin Y, Wang X. A/(H1N1) pdm09 NS1 promotes viral replication by enhancing autophagy through hijacking the IAV negative regulatory factor LRPPRC. Autophagy 2023 May;19(5):1533-1550.
    doi: 10.1080/15548627.2022.2139922pubmed: 36300799google scholar: lookup
  4. Gonzalez-Obando J, Forero JE, Zuluaga-Cabrera AM, Ruiz-Saenz J. Equine Influenza Virus: An Old Known Enemy in the Americas. Vaccines (Basel) 2022 Oct 14;10(10).
    doi: 10.3390/vaccines10101718pubmed: 36298583google scholar: lookup
  5. Whitlock F, Murcia PR, Newton JR. A Review on Equine Influenza from a Human Influenza Perspective. Viruses 2022 Jun 15;14(6).
    doi: 10.3390/v14061312pubmed: 35746783google scholar: lookup
  6. Zhang X, Li Y, Jin S, Zhang Y, Sun L, Hu X, Zhao M, Li F, Wang T, Sun W, Feng N, Wang H, He H, Zhao Y, Yang S, Xia X, Gao Y. PB1 S524G mutation of wild bird-origin H3N8 influenza A virus enhances virulence and fitness for transmission in mammals. Emerg Microbes Infect 2021 Dec;10(1):1038-1051.
    doi: 10.1080/22221751.2021.1912644pubmed: 33840358google scholar: lookup
  7. Bravo-Vasquez N, Yao J, Jimenez-Bluhm P, Meliopoulos V, Freiden P, Sharp B, Estrada L, Davis A, Cherry S, Livingston B, Danner A, Schultz-Cherry S, Hamilton-West C. Equine-Like H3 Avian Influenza Viruses in Wild Birds, Chile. Emerg Infect Dis 2020 Dec;26(12):2887-2898.
    doi: 10.3201/eid2612.202063pubmed: 33219648google scholar: lookup
  8. Badra R, Zhang W, Tam JSL, Webby R, van der Werf S, Nikisins S, Cullinane A, Gharaibeh S, Njouom R, Peiris M, Kayali G, Heraud JM. Transmission Pathways of Zoonotic Influenza Viruses and Influencing Factors: A Systematic Review of Recent Findings. Viruses 2025 Jun 17;17(6).
    doi: 10.3390/v17060857pubmed: 40573448google scholar: lookup
  9. Rather MA, Hassan A, Aman M, Gul I, Mir AH, Potdar V, Koul PA, Ahmad SM, Ganai NA, Shah RA, Chikan NA, Abdul-Careem MF, Shabir N. Molecular and ecological determinants of mammalian adaptability in avian influenza virus. Infection 2025 Oct;53(5):1575-1601.
    doi: 10.1007/s15010-025-02529-5pubmed: 40257536google scholar: lookup
  10. Verhoeven D, Sponseller BA, Crowe JE Jr, Bangaru S, Webby RJ, Lee BM. Use of equine H3N8 hemagglutinin as a broadly protective influenza vaccine immunogen. NPJ Vaccines 2024 Dec 19;9(1):247.
    doi: 10.1038/s41541-024-01037-1pubmed: 39702334google scholar: lookup
  11. Damdinjav B, Raveendran S, Mojsiejczuk L, Ankhanbaatar U, Yang J, Sadeyen JR, Iqbal M, Perez DR, Rajao DS, Park A, Viana M, Murcia PR. Evidence of Influenza A(H5N1) Spillover Infections in Horses, Mongolia. Emerg Infect Dis 2025 Jan;31(1):183-185.
    doi: 10.3201/eid3101.241266pubmed: 39661025google scholar: lookup
  12. Gonzalez-Obando J, Zuluaga-Cabrera A, Moreno I, Úsuga J, Ciuderis K, Forero JE, Diaz A, Rojas-Arbeláez C, Hernández-Ortiz JP, Ruiz-Saenz J. First Molecular Detection and Epidemiological Analysis of Equine Influenza Virus in Two Regions of Colombia, 2020-2023. Viruses 2024 May 24;16(6).
    doi: 10.3390/v16060839pubmed: 38932133google scholar: lookup
  13. Chambers TM. Equine Influenza. Cold Spring Harb Perspect Med 2022 Jan 4;12(1).
    doi: 10.1101/cshperspect.a038331pubmed: 32152243google scholar: lookup
Subscribe to our newsletter
Join 99,344 horse owners like you who receive our email updates on horse health and nutrition.