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Pathogens (Basel, Switzerland)2017; 6(1); 6; doi: 10.3390/pathogens6010006

Evolution and Divergence of H3N8 Equine Influenza Viruses Circulating in the United Kingdom from 2013 to 2015.

Abstract: Equine influenza viruses (EIV) are a major cause of acute respiratory disease in horses worldwide and occasionally also affect vaccinated animals. Like other influenza A viruses, they undergo antigenic drift, highlighting the importance of both surveillance and virus characterisation in order for vaccine strains to be kept up to date. The aim of the work reported here was to monitor the genetic and antigenic changes occurring in EIV circulating in the UK from 2013 to 2015 and to identify any evidence of vaccine breakdown in the field. Virus isolation, reverse transcription polymerase chain reaction (RT-PCR) and sequencing were performed on EIV-positive nasopharyngeal swab samples submitted to the Diagnostic Laboratory Services at the Animal Health Trust (AHT). Phylogenetic analyses were completed for the haemagglutinin-1 (HA1) and neuraminidase (NA) genes using PhyML and amino acid sequences compared against the current World Organisation for Animal Health (OIE)-recommended Florida clade 2 vaccine strain. Substitutions between the new isolates and the vaccine strain were mapped onto the three-dimensional structure protein structures using PyMol. Antigenic analyses were carried out by haemagglutination inhibition assay using a panel of post-infection ferret antisera. Sixty-nine outbreaks of equine influenza in the UK were reported by the AHT between January 2013 and December 2015. Forty-seven viruses were successfully isolated in eggs from 41 of the outbreaks. Only three cases of vaccine breakdown were identified and in each case the vaccine used contained a virus antigen not currently recommended for equine influenza vaccines. Nucleotide sequencing of the HA and NA genes revealed that all of the viruses belonged to the Florida clade 2 sub-lineage of H3N8 EIV. Phylogenetic and sequence analyses showed that the two sub-populations, previously identified within clade 2, continued to circulate and had accrued further amino acid substitutions. Antigenic characterisation using post-infection ferret antisera in haemagglutination inhibition assays however, failed to detect any marked antigenic differences between the isolates. These findings show that Florida clade 2 EIV continue to circulate in the UK and support the current OIE recommendation to include an example of Florida clade 2 in vaccines.
Publication Date: 2017-02-08 PubMed ID: 28208721PubMed Central: PMC5371894DOI: 10.3390/pathogens6010006Google Scholar: Lookup
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  • 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 focused on examining the evolution and divergence of the H3N8 Equine Influenza Viruses (EIV) in the UK from 2013 to 2015, aiming to identify any changes in these viruses and possible vaccine breakdowns.

Methodology

  • Virus isolation, reverse transcription polymerase chain reaction (RT-PCR), and sequencing were performed on EIV-positive nasopharyngeal swab samples submitted to the Diagnostic Laboratory Services at the Animal Health Trust (AHT).
  • Phylogenetic analyses were completed for the haemagglutinin-1 (HA1) and neuraminidase (NA) genes using PhyML, a tool for phylogenetic reconstruction, and amino acid sequences were compared against the current World Organisation for Animal Health (OIE)-recommended Florida clade 2 vaccine strain.
  • Substitutions between the new isolates and the vaccine strain were observed by mapping onto the three-dimensional structure protein structures using PyMol, a molecular visualization tool. Antigenic analyses were carried out by haemagglutination inhibition assay using a panel of post-infection ferret antisera.

Findings

  • Between January 2013 and December 2015, 69 outbreaks of equine influenza in the UK were reported by the AHT. From these, 47 viruses were successfully isolated in eggs from 41 of the outbreaks.
  • There were only three identified cases of vaccine breakdown, and in each case, the vaccine that was used contained a virus antigen not currently recommended for equine influenza vaccines.
  • The nucleotide sequencing of the HA and NA genes revealed that all of the viruses belonged to the Florida clade 2 sub-lineage of H3N8 EIV.
  • Phylogenetic and sequence analyses showed that the previously identified two sub-populations of the Florida clade 2 continued to circulate, with additional amino acid substitutions accrued over time.
  • Interestingly, no significant antigenic differences were observed between the isolates through antigenic characterisation using post-infection ferret antisera in haemagglutination inhibition assays.

Implications

  • The findings support the current OIE recommendation to include an example of Florida clade 2 in vaccines as it continues to circulate in the UK.
  • This research enhances the understanding of EIV evolution, highlighting the need for continued monitoring of the virus to ensure the effectiveness of existing vaccines and inform the development of new ones.

Cite This Article

APA
Rash A, Morton R, Woodward A, Maes O, McCauley J, Bryant N, Elton D. (2017). Evolution and Divergence of H3N8 Equine Influenza Viruses Circulating in the United Kingdom from 2013 to 2015. Pathogens, 6(1), 6. https://doi.org/10.3390/pathogens6010006

Publication

ISSN: 2076-0817
NlmUniqueID: 101596317
Country: Switzerland
Language: English
Volume: 6
Issue: 1
PII: 6

Researcher Affiliations

Rash, Adam
  • Animal Health Trust, Lanwades Park, Kentford, Newmarket, CB8 7UU, UK. adam.rash@aht.org.uk.
Morton, Rachel
  • Animal Health Trust, Lanwades Park, Kentford, Newmarket, CB8 7UU, UK. Rachel.Morton@aht.org.uk.
Woodward, Alana
  • Animal Health Trust, Lanwades Park, Kentford, Newmarket, CB8 7UU, UK. Alana.Woodward@aht.org.uk.
Maes, Olivia
  • Animal Health Trust, Lanwades Park, Kentford, Newmarket, CB8 7UU, UK. Olivia.Maes@aht.org.uk.
McCauley, John
  • Crick Worldwide Influenza Centre, The Francis Crick Institute, 1 Midland Road, London, NW1 1AT, UK. John.McCauley@crick.ac.uk.
Bryant, Neil
  • Animal Health Trust, Lanwades Park, Kentford, Newmarket, CB8 7UU, UK. Neil.Bryant@aht.org.uk.
Elton, Debra
  • Animal Health Trust, Lanwades Park, Kentford, Newmarket, CB8 7UU, UK. Debra.Elton@aht.org.uk.

Grant Funding

  • Wellcome Trust
  • FC001030 / Arthritis Research UK
  • MC_U117512723 / Medical Research Council

Conflict of Interest Statement

The authors declare no conflict of interest. The founding sponsors had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, and in the decision to publish the results.

References

This article includes 43 references
  1. Weis W, Brown JH, Cusack S, Paulson JC, Skehel JJ, Wiley DC. Structure of the influenza virus haemagglutinin complexed with its receptor, sialic acid.. Nature 1988 Jun 2;333(6172):426-31.
    doi: 10.1038/333426a0pubmed: 3374584google scholar: lookup
  2. Skehel JJ, Wiley DC. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin.. Annu Rev Biochem 2000;69:531-69.
  3. Matrosovich MN, Matrosovich TY, Gray T, Roberts NA, Klenk HD. Neuraminidase is important for the initiation of influenza virus infection in human airway epithelium.. J Virol 2004 Nov;78(22):12665-7.
  4. Halbherr SJ, Ludersdorfer TH, Ricklin M, Locher S, Berger Rentsch M, Summerfield A, Zimmer G. Biological and protective properties of immune sera directed to the influenza virus neuraminidase.. J Virol 2015 Feb;89(3):1550-63.
    doi: 10.1128/JVI.02949-14pmc: PMC4300740pubmed: 25392225google scholar: lookup
  5. Yamanaka T, Tsujimura K, Kondo T, Hobo S, Matsumura T. Efficacy of oseltamivir phosphate to horses inoculated with equine influenza A virus.. J Vet Med Sci 2006 Sep;68(9):923-8.
    doi: 10.1292/jvms.68.923pubmed: 17019060google scholar: lookup
  6. Yamanaka T, Bannai H, Nemoto M, Tsujimura K, Kondo T, Muranaka M, Hobo S, Minamijima YH, Yamada M, Matsumura T. Efficacy of a single intravenous dose of the neuraminidase inhibitor peramivir in the treatment of equine influenza.. Vet J 2012 Aug;193(2):358-62.
    doi: 10.1016/j.tvjl.2012.01.005pubmed: 22326934google scholar: lookup
  7. 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
  8. Bryant NA, Rash AS, Russell CA, Ross J, Cooke A, Bowman S, MacRae S, Lewis NS, Paillot R, Zanoni R, Meier H, Griffiths LA, Daly JM, Tiwari A, Chambers TM, Newton JR, Elton DM. Antigenic and genetic variations in European and North American equine influenza virus strains (H3N8) isolated from 2006 to 2007.. Vet Microbiol 2009 Jul 2;138(1-2):41-52.
    doi: 10.1016/j.vetmic.2009.03.004pubmed: 19346084google scholar: lookup
  9. Woodward AL, Rash AS, Blinman D, Bowman S, Chambers TM, Daly JM, Damiani A, Joseph S, Lewis N, McCauley JW, Medcalf L, Mumford J, Newton JR, Tiwari A, Bryant NA, Elton DM. Development of a surveillance scheme for equine influenza in the UK and characterisation of viruses isolated in Europe, Dubai and the USA from 2010-2012.. Vet Microbiol 2014 Mar 14;169(3-4):113-27.
    doi: 10.1016/j.vetmic.2013.11.039pubmed: 24480583google scholar: lookup
  10. Burrows R, Denyer M, Goodridge D, Hamilton F. Field and laboratory studies of equine influenza viruses isolated in 1979.. Vet Rec 1981 Oct 17;109(16):353-6.
    doi: 10.1136/vr.109.16.353pubmed: 6275599google scholar: lookup
  11. Cowled B, Ward MP, Hamilton S, Garner G. The equine influenza epidemic in Australia: spatial and temporal descriptive analyses of a large propagating epidemic.. Prev Vet Med 2009 Nov 1;92(1-2):60-70.
  12. Livesay GJ, O'Neill T, Hannant D, Yadav MP, Mumford JA. The outbreak of equine influenza (H3N8) in the United Kingdom in 1989: diagnostic use of an antigen capture ELISA.. Vet Rec 1993 Nov 20;133(21):515-9.
    doi: 10.1136/vr.133.21.515pubmed: 8310627google scholar: lookup
  13. Ito M, Nagai M, Hayakawa Y, Komae H, Murakami N, Yotsuya S, Asakura S, Sakoda Y, Kida H. Genetic Analyses of an H3N8 Influenza Virus Isolate, Causative Strain of the Outbreak of Equine Influenza at the Kanazawa Racecourse in Japan in 2007.. J Vet Med Sci 2008 Sep;70(9):899-906.
    doi: 10.1292/jvms.70.899pubmed: 18840963google scholar: lookup
  14. Newton JR, Daly JM, Spencer L, Mumford JA. Description of the outbreak of equine influenza (H3N8) in the United Kingdom in 2003, during which recently vaccinated horses in Newmarket developed respiratory disease.. Vet Rec 2006 Feb 11;158(6):185-92.
    doi: 10.1136/vr.158.6.185pubmed: 16474051google scholar: lookup
  15. Virmani N, Bera BC, Singh BK, Shanmugasundaram K, Gulati BR, Barua S, Vaid RK, Gupta AK, Singh RK. Equine influenza outbreak in India (2008-09): virus isolation, sero-epidemiology and phylogenetic analysis of HA gene.. Vet Microbiol 2010 Jul 14;143(2-4):224-37.
    doi: 10.1016/j.vetmic.2009.12.007pubmed: 20053509google scholar: lookup
  16. Alves Beuttemmüller E, Woodward A, Rash A, Dos Santos Ferraz LE, Fernandes Alfieri A, Alfieri AA, Elton D. Characterisation of the epidemic strain of H3N8 equine influenza virus responsible for outbreaks in South America in 2012.. Virol J 2016 Mar 19;13:45.
    doi: 10.1186/s12985-016-0503-9pmc: PMC4799594pubmed: 26993620google scholar: lookup
  17. Perglione CO, Gildea S, Rimondi A, Miño S, Vissani A, Carossino M, Cullinane A, Barrandeguy M. Epidemiological and virological findings during multiple outbreaks of equine influenza in South America in 2012.. Influenza Other Respir Viruses 2016 Jan;10(1):37-46.
    doi: 10.1111/irv.12349pmc: PMC4687505pubmed: 26406274google scholar: lookup
  18. Yamanaka T, Niwa H, Tsujimura K, Kondo T, Matsumura T. Epidemic of equine influenza among vaccinated racehorses in Japan in 2007.. J Vet Med Sci 2008 Jun;70(6):623-5.
    doi: 10.1292/jvms.70.623pubmed: 18628606google scholar: lookup
  19. Worobey M, Han GZ, Rambaut A. A synchronized global sweep of the internal genes of modern avian influenza virus.. Nature 2014 Apr 10;508(7495):254-7.
    doi: 10.1038/nature13016pmc: PMC4098125pubmed: 24531761google scholar: lookup
  20. Lai AC, Chambers TM, Holland RE Jr, Morley PS, Haines DM, Townsend HG, Barrandeguy M. Diverged evolution of recent equine-2 influenza (H3N8) viruses in the Western Hemisphere.. Arch Virol 2001;146(6):1063-74.
    doi: 10.1007/s007050170106pubmed: 11504416google scholar: lookup
  21. Bernardino PN, Mapes SM, Corbin R, Pusterla N. Pyrosequencing as a fast and reliable tool to determine clade affiliation for equine Influenza A virus.. J Vet Diagn Invest 2016 May 1;28(3):323-326.
    doi: 10.1177/1040638716638123pubmed: 26961323google scholar: lookup
  22. Gildea S, Quinlivan M, Arkins S, Cullinane A. The molecular epidemiology of equine influenza in Ireland from 2007-2010 and its international significance.. Equine Vet J 2012 Jul;44(4):387-92.
  23. Gildea S, Fitzpatrick DA, Cullinane A. Epidemiological and virological investigations of equine influenza outbreaks in Ireland (2010-2012).. Influenza Other Respir Viruses 2013 Dec;7 Suppl 4(Suppl 4):61-72.
    doi: 10.1111/irv.12192pmc: PMC5655889pubmed: 24224821google scholar: lookup
  24. Legrand LJ, Pitel PH, Cullinane AA, Fortier GD, Pronost SL. Genetic evolution of equine influenza strains isolated in France from 2005 to 2010.. Equine Vet J 2015 Mar;47(2):207-11.
    doi: 10.1111/evj.12244pubmed: 25763436google scholar: lookup
  25. Qi T, Guo W, Huang WQ, Li HM, Zhao LP, Dai LL, He N, Hao XF, Xiang WH. Genetic evolution of equine influenza viruses isolated in China.. Arch Virol 2010 Sep;155(9):1425-32.
    doi: 10.1007/s00705-010-0724-ypubmed: 20559670google scholar: lookup
  26. 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
  27. Binns MM, Daly JM, Chirnside ED, Mumford JA, Wood JM, Richards CM, Daniels RS. Genetic and antigenic analysis of an equine influenza H 3 isolate from the 1989 epidemic.. Arch Virol 1993;130(1-2):33-43.
    doi: 10.1007/BF01318994pubmed: 8503788google scholar: lookup
  28. Barbic L, Madic J, Turk N, Daly J. Vaccine failure caused an outbreak of equine influenza in Croatia.. Vet Microbiol 2009 Jan 1;133(1-2):164-71.
    doi: 10.1016/j.vetmic.2008.06.009pubmed: 18632226google scholar: lookup
  29. Cullinane A, Elton D, Mumford J. Equine influenza - surveillance and control.. Influenza Other Respir Viruses 2010 Nov;4(6):339-44.
  30. . The World Organisation for Animal Health (OIE) Expert surveillance panel on equine influenza vaccine composition—Conclusions and recommendations.. Off. Int. Epizoot. Bull. 2016;2:61–63.
  31. . GISAID EpiFlu Database Editorial: Action stations: The time for sitting on flu data is over.. Nature 2006;441:1028.
    pubmed: 0
  32. Collins PJ, Vachieri SG, Haire LF, Ogrodowicz RW, Martin SR, Walker PA, Xiong X, Gamblin SJ, Skehel JJ. Recent evolution of equine influenza and the origin of canine influenza.. Proc Natl Acad Sci U S A 2014 Jul 29;111(30):11175-80.
    doi: 10.1073/pnas.1406606111pmc: PMC4121831pubmed: 25024224google scholar: lookup
  33. Russell RJ, Haire LF, Stevens DJ, Collins PJ, Lin YP, Blackburn GM, Hay AJ, Gamblin SJ, Skehel JJ. The structure of H5N1 avian influenza neuraminidase suggests new opportunities for drug design.. Nature 2006 Sep 7;443(7107):45-9.
    doi: 10.1038/nature05114pubmed: 16915235google scholar: lookup
  34. . The World Organisation for Animal Health (OIE) Expert surveillance panel on equine influenza vaccine composition—Conclusions and recommendations.. Off. Int. Epizoot. Bull. 2010;2:44–45.
  35. Bryant NA, Rash AS, Woodward AL, Medcalf E, Helwegen M, Wohlfender F, Cruz F, Herrmann C, Borchers K, Tiwari A, Chambers TM, Newton JR, Mumford JA, Elton DM. Isolation and characterisation of equine influenza viruses (H3N8) from Europe and North America from 2008 to 2009.. Vet Microbiol 2011 Jan 10;147(1-2):19-27.
    doi: 10.1016/j.vetmic.2010.05.040pubmed: 20580170google scholar: lookup
  36. Corti D, Suguitan AL Jr, Pinna D, Silacci C, Fernandez-Rodriguez BM, Vanzetta F, Santos C, Luke CJ, Torres-Velez FJ, Temperton NJ, Weiss RA, Sallusto F, Subbarao K, Lanzavecchia A. Heterosubtypic neutralizing antibodies are produced by individuals immunized with a seasonal influenza vaccine.. J Clin Invest 2010 May;120(5):1663-73.
    doi: 10.1172/JCI41902pmc: PMC2860935pubmed: 20389023google scholar: lookup
  37. Dreyfus C, Ekiert DC, Wilson IA. Structure of a classical broadly neutralizing stem antibody in complex with a pandemic H2 influenza virus hemagglutinin.. J Virol 2013 Jun;87(12):7149-54.
    doi: 10.1128/JVI.02975-12pmc: PMC3676097pubmed: 23552413google scholar: lookup
  38. Yamanaka T, Cullinane A, Gildea S, Bannai H, Nemoto M, Tsujimura K, Kondo T, Matsumura T. The potential impact of a single amino-acid substitution on the efficacy of equine influenza vaccines.. Equine Vet J 2015 Jul;47(4):456-62.
    doi: 10.1111/evj.12290pubmed: 24773030google scholar: lookup
  39. Yamanaka T, Nemoto M, Bannai H, Tsujimura K, Kondo T, Matsumura T, Gildea S, Cullinane A. Assessment of antigenic difference of equine influenza virus strains by challenge study in horses.. Influenza Other Respir Viruses 2016 Nov;10(6):536-539.
    doi: 10.1111/irv.12418pmc: PMC5059955pubmed: 27465864google scholar: lookup
  40. Cook RF, Sinclair R, Mumford JA. Detection of influenza nucleoprotein antigen in nasal secretions from horses infected with A/equine influenza (H3N8) viruses.. J Virol Methods 1988 May;20(1):1-12.
    doi: 10.1016/0166-0934(88)90034-1pubmed: 2840448google scholar: lookup
  41. . Manual of Diagnostic Tests and Vaccines for Terrestrial Animals. Chapter 2.5.7 Equine influenza. OIE 2016;pp. 1–16.
  42. Rash A, Woodward A, Bryant N, McCauley J, Elton D. An efficient genome sequencing method for equine influenza [H3N8] virus reveals a new polymorphism in the PA-X protein.. Virol J 2014 Sep 2;11:159.
    doi: 10.1186/1743-422X-11-159pmc: PMC4161859pubmed: 25183201google scholar: lookup
  43. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0.. Syst Biol 2010 May;59(3):307-21.
    doi: 10.1093/sysbio/syq010pubmed: 20525638google scholar: lookup

Citations

This article has been cited 21 times.
  1. Ahmed BM, Bayoumi MM, Farrag MA, Elgamal MA, Daly JM, Amer HM. Emergence of equine influenza virus H3Nx Florida clade 2 in Arabian racehorses in Egypt.. Virol J 2022 Nov 12;19(1):185.
    doi: 10.1186/s12985-022-01917-9pubmed: 36371185google scholar: lookup
  2. Burashev Y, Orynbayev M, Zakarya K, Abduraimov Y, Kassenov M, Strochkov V, Kozhabergenov N, Usserbayev B, Melisbek A, Shirinbekov M, Sypatay N, Sultankulova K. Complete Coding Genome Sequence of an Influenza A/H3N8 Equine Virus Isolated in Kazakhstan in 2007.. Microbiol Resour Announc 2022 Oct 20;11(10):e0114721.
    doi: 10.1128/mra.01147-21pubmed: 36094178google scholar: lookup
  3. Rozario C, Martínez-Sobrido L, McSorley HJ, Chauché C. Could Interleukin-33 (IL-33) Govern the Outcome of an Equine Influenza Virus Infection? Learning from Other Species.. Viruses 2021 Dec 15;13(12).
    doi: 10.3390/v13122519pubmed: 34960788google scholar: lookup
  4. Amat JAR, Patton V, Chauché C, Goldfarb D, Crispell J, Gu Q, Coburn AM, Gonzalez G, Mair D, Tong L, Martinez-Sobrido L, Marshall JF, Marchesi F, Murcia PR. Long-term adaptation following influenza A virus host shifts results in increased within-host viral fitness due to higher replication rates, broader dissemination within the respiratory epithelium and reduced tissue damage.. PLoS Pathog 2021 Dec;17(12):e1010174.
    doi: 10.1371/journal.ppat.1010174pubmed: 34919598google scholar: lookup
  5. Olguin-Perglione C, Barrandeguy ME. An Overview of Equine Influenza in South America.. Viruses 2021 May 12;13(5).
    doi: 10.3390/v13050888pubmed: 34065839google scholar: lookup
  6. Karam B, Wilson WD, Chambers TM, Reedy S, Pusterla N. Hemagglutinin inhibition antibody responses to commercial equine influenza vaccines in vaccinated horses.. Can Vet J 2021 Mar;62(3):266-272.
    pubmed: 33692582
  7. Pavulraj S, Bergmann T, Trombetta CM, Marchi S, Montomoli E, Alami SSE, Ragni-Alunni R, Osterrieder N, Azab W. Immunogenicity of Calvenza-03 EIV/EHV(®) Vaccine in Horses: Comparative In Vivo Study.. Vaccines (Basel) 2021 Feb 17;9(2).
    doi: 10.3390/vaccines9020166pubmed: 33671378google scholar: lookup
  8. Oli AN, Obialor WO, Ifeanyichukwu MO, Odimegwu DC, Okoyeh JN, Emechebe GO, Adejumo SA, Ibeanu GC. Immunoinformatics and Vaccine Development: An Overview.. Immunotargets Ther 2020;9:13-30.
    doi: 10.2147/ITT.S241064pubmed: 32161726google scholar: lookup
  9. Fougerolle S, Fortier C, Legrand L, Jourdan M, Marcillaud-Pitel C, Pronost S, Paillot R. Success and Limitation of Equine Influenza Vaccination: The First Incursion in a Decade of a Florida Clade 1 Equine Influenza Virus that Shakes Protection Despite High Vaccine Coverage.. Vaccines (Basel) 2019 Nov 2;7(4).
    doi: 10.3390/vaccines7040174pubmed: 31684097google scholar: lookup
  10. Blanco-Lobo P, Rodriguez L, Reedy S, Oladunni FS, Nogales A, Murcia PR, Chambers TM, Martinez-Sobrido L. A Bivalent Live-Attenuated Vaccine for the Prevention of Equine Influenza Virus.. Viruses 2019 Oct 11;11(10).
    doi: 10.3390/v11100933pubmed: 31614538google scholar: lookup
  11. Toh X, Soh ML, Ng MK, Yap SC, Harith N, Fernandez CJ, Huangfu T. Isolation and characterization of equine influenza virus (H3N8) from an equine influenza outbreak in Malaysia in 2015.. Transbound Emerg Dis 2019 Sep;66(5):1884-1893.
    doi: 10.1111/tbed.13218pubmed: 31059176google scholar: lookup
  12. Brister H, Barnum SM, Reedy S, Chambers TM, Pusterla N. Validation of two multiplex real-time PCR assays based on single nucleotide polymorphisms of the HA1 gene of equine influenza A virus in order to differentiate between clade 1 and clade 2 Florida sublineage isolates.. J Vet Diagn Invest 2019 Jan;31(1):137-141.
    doi: 10.1177/1040638718822693pubmed: 30803412google scholar: lookup
  13. Kwaśnik M, Góra IM, Żmudziński JF, Rola J, Polak MP, Rożek W. Genetic Analysis of the M Gene of Equine Influenza Virus Strains Isolated in Poland, in the Context of the Asian-like Group Formation.. J Vet Res 2018 Dec;62(4):405-412.
    doi: 10.2478/jvetres-2018-0057pubmed: 30729195google scholar: lookup
  14. Singh RK, Dhama K, Karthik K, Khandia R, Munjal A, Khurana SK, Chakraborty S, Malik YS, Virmani N, Singh R, Tripathi BN, Munir M, van der Kolk JH. A Comprehensive Review on Equine Influenza Virus: Etiology, Epidemiology, Pathobiology, Advances in Developing Diagnostics, Vaccines, and Control Strategies.. Front Microbiol 2018;9:1941.
    doi: 10.3389/fmicb.2018.01941pubmed: 30237788google scholar: lookup
  15. Paillot R, Garrett D, Lopez-Alvarez MR, Birand I, Montesso F, Horspool L. The Immunity Gap Challenge: Protection against a Recent Florida Clade 2 Equine Influenza Strain.. Vaccines (Basel) 2018 Jul 2;6(3).
    doi: 10.3390/vaccines6030038pubmed: 30004410google scholar: lookup
  16. Gildea S, Garvey M, Lyons P, Lyons R, Gahan J, Walsh C, Cullinane A. Multifocal Equine Influenza Outbreak with Vaccination Breakdown in Thoroughbred Racehorses.. Pathogens 2018 Apr 17;7(2).
    doi: 10.3390/pathogens7020043pubmed: 29673169google scholar: lookup
  17. Nemoto M, Yamanaka T, Bannai H, Tsujimura K, Kokado H. Complete Genomic Sequences of H3N8 Equine Influenza Virus Strains Used as Vaccine Strains in Japan.. Genome Announc 2018 Mar 22;6(12).
    doi: 10.1128/genomeA.00172-18pubmed: 29567739google scholar: lookup
  18. Rodriguez L, Reedy S, Nogales A, Murcia PR, Chambers TM, Martinez-Sobrido L. Development of a novel equine influenza virus live-attenuated vaccine.. Virology 2018 Mar;516:76-85.
    doi: 10.1016/j.virol.2018.01.005pubmed: 29331866google scholar: lookup
  19. Sreenivasan CC, Jandhyala SS, Luo S, Hause BM, Thomas M, Knudsen DEB, Leslie-Steen P, Clement T, Reedy SE, Chambers TM, Christopher-Hennings J, Nelson E, Wang D, Kaushik RS, Li F. Phylogenetic Analysis and Characterization of a Sporadic Isolate of Equine Influenza A H3N8 from an Unvaccinated Horse in 2015.. Viruses 2018 Jan 11;10(1).
    doi: 10.3390/v10010031pubmed: 29324680google scholar: lookup
  20. Yamanaka T, Nemoto M, Bannai H, Tsujimura K, Matsumura T, Kokado H, Gildea S, Cullinane A. Neutralization antibody response to booster/priming immunization with new equine influenza vaccine in Japan.. J Vet Med Sci 2018 Mar 2;80(2):382-386.
    doi: 10.1292/jvms.17-0538pubmed: 29237998google scholar: lookup
  21. Paillot R, Marcillaud Pitel C, D'Ablon X, Pronost S. Equine Vaccines: How, When and Why? Report of the Vaccinology Session, French Equine Veterinarians Association, 2016, Reims.. Vaccines (Basel) 2017 Dec 4;5(4).
    doi: 10.3390/vaccines5040046pubmed: 29207516google scholar: lookup