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Influenza and other respiratory viruses2010; 4(6); 345-351; doi: 10.1111/j.1750-2659.2010.00157.x

Infectivity and pathogenicity of canine H3N8 influenza A virus in horses.

Abstract: Equine H3N8 influenza A viruses (EIVs) cause respiratory disease in horses and circulate among horses worldwide. In 2004, an outbreak of canine H3N8 influenza A virus (CIV) occurred among dogs in Florida and has spread among dogs in the United States (US). Genetic analyses revealed that this CIV is closely related to the recent EIVs. Although CIV-infected dogs could be the source of H3N8 influenza A virus for horses, it remains unclear whether the CIV circulating in the United States still maintains its infectivity and/or pathogenicity in horses. To address this, we investigated the infectivity and pathogenicity of CIV in horses and the receptor binding specificity of CIV. Methods: Three horses were inoculated with A/canine/Colorado/30604/2006 (CO06, H3N8). Clinical signs and nasal swabs were recorded or collected every day. We also evaluated the virus binding to α2-3-linked 5-N-acetylneuraminic acid (NeuAcα2-3Gal) and 5-N-glycolylneuraminic acid (NeuGcα2-3Gal) receptor analogues. Results: Although all the three horses inoculated with CO06 seroconverted, they showed only mild clinical signs and two of them showed no virus shedding. CO06 had reduced binding to NeuGcα2-3Gal. Conclusions: Our results demonstrated that CO06 had reduced proliferation ability and pathogenicity in horses. As the recognition of NeuGcα2-3Gal by EIV is known to be essential for binding to the equine respiratory system, the decreased binding of CO06 to NeuGcα2-3Gal may be one of the important factors that reduces the proliferation ability and pathogenicity of CO06 in horses.
Publication Date: 2010-10-21 PubMed ID: 20958928PubMed Central: PMC4634615DOI: 10.1111/j.1750-2659.2010.00157.xGoogle Scholar: Lookup
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  • Journal Article

Summary

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This research investigates the ability of a canine version of the H3N8 influenza A virus to infect and cause disease in horses. The study concludes that the specific strain of the virus used in this experiment was less able to multiply and cause disease in horses, possibly due to its diminished binding capability with a key element in the equine respiratory system.

Background and Objectives

  • The research was based on a previous occurrence in 2004 where an outbreak of the H3N8 influenza A virus among dogs was observed in Florida and has since spread among dogs in the United States.
  • Genetic analyses showed that the canine version of this virus is closely related to the equine version, causing respiratory disease in horses.
  • The research aim was to determine whether this canine version still maintains its ability to infect and cause disease in horses.
  • Methods

    • Three horses were inoculated with a particular strain of the virus, known as A/canine/Colorado/30604/2006 (abbreviated to CO06).
    • Observations were taken daily on clinical signs and nasal swabs were collected.
    • The virus’s ability to bind to two types of receptor analogues was also evaluated.
    • Results

      • All three horses presented an immune response to the virus, but only showed mild symptoms of illness.
      • Two of the three horses did not shed the virus, indicating that it did not multiply effectively in their systems.
      • The CO06 strain was less effective at binding to one of the receptor analogues.
      • Conclusions

        • The results suggest that the CO06 strain was less effective in both multiplying and causing disease in horses, likely due to its reduced ability to bind to the NeuGcα2-3Gal receptor analogue.
        • This receptor analogue is critical for the equine version of H3N8 influenza A to bind to the respiratory system of the horse.
        • Therefore, this reduction in binding ability is likely a key reason for the diminished infectivity and pathogenicity of CO06 in horses.

Cite This Article

APA
Yamanaka T, Tsujimura K, Kondo T, Matsumura T, Ishida H, Kiso M, Hidari KI, Suzuki T. (2010). Infectivity and pathogenicity of canine H3N8 influenza A virus in horses. Influenza Other Respir Viruses, 4(6), 345-351. https://doi.org/10.1111/j.1750-2659.2010.00157.x

Publication

ISSN: 1750-2659
NlmUniqueID: 101304007
Country: England
Language: English
Volume: 4
Issue: 6
Pages: 345-351

Researcher Affiliations

Yamanaka, Takashi
  • Epizootic Research Center, Equine Research Institute, Japan Racing Association, Shimotsukeshi, Tochigi, Japan. yamanaka@epizoo.equinst.go.jp
Tsujimura, Koji
    Kondo, Takashi
      Matsumura, Tomio
        Ishida, Hideharu
          Kiso, Makoto
            Hidari, Kazuya I P J
              Suzuki, Takashi

                MeSH Terms

                • Animals
                • Antibodies, Viral / blood
                • Disease Models, Animal
                • Dog Diseases / virology
                • Dogs
                • Horse Diseases / pathology
                • Horse Diseases / virology
                • Horses
                • Influenza A Virus, H3N8 Subtype / isolation & purification
                • Influenza A Virus, H3N8 Subtype / pathogenicity
                • Nasal Mucosa / virology
                • Orthomyxoviridae Infections / pathology
                • Orthomyxoviridae Infections / veterinary
                • Orthomyxoviridae Infections / virology
                • Receptors, Virus / analysis
                • United States
                • Virus Attachment
                • Virus Shedding

                References

                This article includes 30 references
                1. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. Evolution and ecology of influenza A viruses.. Microbiol Rev 1992 Mar;56(1):152-79.
                  pmc: PMC372859pubmed: 1579108doi: 10.1128/mr.56.1.152-179.1992google scholar: lookup
                2. van Maanen C, Cullinane A. Equine influenza virus infections: an update.. Vet Q 2002 Jun;24(2):79-94.
                  pubmed: 12095083doi: 10.1080/01652176.2002.9695127google scholar: lookup
                3. Webster RG. Are equine 1 influenza viruses still present in horses?. Equine Vet J 1993 Nov;25(6):537-8.
                4. Daly JM, Lai AC, Binns MM, Chambers TM, Barrandeguy M, Mumford JA. Antigenic and genetic evolution of equine H3N8 influenza A viruses.. J Gen Virol 1996 Apr;77 ( Pt 4):661-71.
                  pubmed: 8627254doi: 10.1099/0022-1317-77-4-661google scholar: lookup
                5. Lai AC, Rogers KM, Glaser A, Tudor L, Chambers T. Alternate circulation of recent equine-2 influenza viruses (H3N8) from two distinct lineages in the United States.. Virus Res 2004 Mar 15;100(2):159-64.
                6. 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.
                  pubmed: 18632226doi: 10.1016/j.vetmic.2008.06.009google scholar: lookup
                7. Damiani AM, Scicluna MT, Ciabatti I, Cardeti G, Sala M, Vulcano G, Cordioli P, Martella V, Amaddeo D, Autorino GL. Genetic characterization of equine influenza viruses isolated in Italy between 1999 and 2005.. Virus Res 2008 Jan;131(1):100-5.
                8. 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.
                  pubmed: 18840963doi: 10.1292/jvms.70.899google scholar: lookup
                9. Martella V, Elia G, Decaro N, Di Trani L, Lorusso E, Campolo M, Desario C, Parisi A, Cavaliere N, Buonavoglia C. An outbreak of equine influenza virus in vaccinated horses in Italy is due to an H3N8 strain closely related to recent North American representatives of the Florida sub-lineage.. Vet Microbiol 2007 Mar 31;121(1-2):56-63.
                  pubmed: 17197135doi: 10.1016/j.vetmic.2006.11.017google scholar: lookup
                10. 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.
                  pubmed: 16474051doi: 10.1136/vr.158.6.185google scholar: lookup
                11. 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.
                  pubmed: 18628606doi: 10.1292/jvms.70.623google scholar: lookup
                12. 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.
                13. 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.
                  pubmed: 19346084doi: 10.1016/j.vetmic.2009.03.004google scholar: lookup
                14. 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.
                  pubmed: 16186182doi: 10.1126/science.1117950google scholar: lookup
                15. Dubovi EJ, Njaa BL. Canine influenza.. Vet Clin North Am Small Anim Pract 2008 Jul;38(4):827-35, viii.
                  pubmed: 18501281doi: 10.1016/j.cvsm.2008.03.004google scholar: lookup
                16. Yoon KJ, Cooper VL, Schwartz KJ, Harmon KM, Kim WI, Janke BH, Strohbehn J, Butts D, Troutman J. Influenza virus infection in racing greyhounds.. Emerg Infect Dis 2005 Dec;11(12):1974-6.
                  pmc: PMC3367648pubmed: 16485496doi: 10.3201/eid1112.050810google scholar: lookup
                17. Payungporn S, Crawford PC, Kouo TS, Chen LM, Pompey J, Castleman WL, Dubovi EJ, Katz JM, Donis RO. Influenza A virus (H3N8) in dogs with respiratory disease, Florida.. Emerg Infect Dis 2008 Jun;14(6):902-8.
                  pmc: PMC2600298pubmed: 18507900doi: 10.3201/eid1406.071270google scholar: lookup
                18. Rogers GN, Pritchett TJ, Lane JL, Paulson JC. Differential sensitivity of human, avian, and equine influenza A viruses to a glycoprotein inhibitor of infection: selection of receptor specific variants.. Virology 1983 Dec;131(2):394-408.
                  pubmed: 6197808doi: 10.1016/0042-6822(83)90507-xgoogle scholar: lookup
                19. Ito T, Kawaoka Y. Host-range barrier of influenza A viruses.. Vet Microbiol 2000 May 22;74(1-2):71-5.
                  pubmed: 10799779doi: 10.1016/s0378-1135(00)00167-xgoogle scholar: lookup
                20. Suzuki Y, Ito T, Suzuki T, Holland RE Jr, Chambers TM, Kiso M, Ishida H, Kawaoka Y. Sialic acid species as a determinant of the host range of influenza A viruses.. J Virol 2000 Dec;74(24):11825-31.
                21. Imagawa H, Fukunaga Y, Kamada M, Nanbu M, Kitamura M. Distribution of HI antibody against 3 vaccine strains of equine influenza in light‐breed horses in Japan. J Equine Sci 1993; 4:31–38.
                22. Yamanaka T, Nemoto M, Tsujimura K, Kondo T, Matsumura T. Interspecies transmission of equine influenza virus (H3N8) to dogs by close contact with experimentally infected horses.. Vet Microbiol 2009 Nov 18;139(3-4):351-5.
                  pubmed: 19596528doi: 10.1016/j.vetmic.2009.06.015google scholar: lookup
                23. Reed LJ, Müench H. A simple method of estimating fifty per cent of endpoint. AM J Hyg 1938; 27:493.
                24. Tanahashi E, Fukunaga K, Ozawa Y. Synthesis of Sialyl‐α‐(2→3)‐Neolactotetraose Derivatives Containing Different Sialic Acids: Molecular Probes for Elucidation of Substrate Specificity of Human α1,3‐Fucosyltransferases. J Carbohydr Chem 2000; 19:747–768.
                25. Masuda H, Suzuki T, Sugiyama Y, Horiike G, Murakami K, Miyamoto D, Jwa Hidari KI, Ito T, Kida H, Kiso M, Fukunaga K, Ohuchi M, Toyoda T, Ishihama A, Kawaoka Y, Suzuki Y. Substitution of amino acid residue in influenza A virus hemagglutinin affects recognition of sialyl-oligosaccharides containing N-glycolylneuraminic acid.. FEBS Lett 1999 Dec 24;464(1-2):71-4.
                  pubmed: 10611486doi: 10.1016/s0014-5793(99)01575-6google scholar: lookup
                26. Hidari KI, Murata T, Yoshida K, Takahashi Y, Minamijima YH, Miwa Y, Adachi S, Ogata M, Usui T, Suzuki Y, Suzuki T. Chemoenzymatic synthesis, characterization, and application of glycopolymers carrying lactosamine repeats as entry inhibitors against influenza virus infection.. Glycobiology 2008 Oct;18(10):779-88.
                  pubmed: 18621993doi: 10.1093/glycob/cwn067google scholar: lookup
                27. Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0.. Mol Biol Evol 2007 Aug;24(8):1596-9.
                  pubmed: 17488738doi: 10.1093/molbev/msm092google scholar: lookup
                28. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees.. Mol Biol Evol 1987 Jul;4(4):406-25.
                29. 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.
                  pmc: PMC2570814pubmed: 18325262doi: 10.3201/eid1403.070643google scholar: lookup
                30. Song D, Kang B, Lee C, Jung K, Ha G, Kang D, Park S, Park B, Oh J. Transmission of avian influenza virus (H3N2) to dogs.. Emerg Infect Dis 2008 May;14(5):741-6.
                  pmc: PMC2600237pubmed: 18439355doi: 10.3201/eid1405.071471google scholar: lookup

                Citations

                This article has been cited 13 times.
                1. Klivleyeva NG, Glebova TI, Shamenova MG, Saktaganov NT. Influenza A viruses circulating in dogs: A review of the scientific literature. Open Vet J 2022 Sep-Oct;12(5):676-687.
                  doi: 10.5455/OVJ.2022.v12.i5.12pubmed: 36589407google scholar: lookup
                2. Wasik BR, Voorhees IEH, Parrish CR. Canine and Feline Influenza. Cold Spring Harb Perspect Med 2021 Jan 4;11(1).
                  doi: 10.1101/cshperspect.a038562pubmed: 31871238google scholar: lookup
                3. 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
                4. 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.00521-15pubmed: 25903329google scholar: lookup
                5. Parrish CR, Murcia PR, Holmes EC. Influenza virus reservoirs and intermediate hosts: dogs, horses, and new possibilities for influenza virus exposure of humans. J Virol 2015 Mar;89(6):2990-4.
                  doi: 10.1128/JVI.03146-14pubmed: 25540375google scholar: lookup
                6. Pecoraro HL, Bennett S, Spindel ME, Landolt GA. Evolution of the hemagglutinin gene of H3N8 canine influenza virus in dogs. Virus Genes 2014 Dec;49(3):393-9.
                  doi: 10.1007/s11262-014-1102-8pubmed: 25056577google scholar: lookup
                7. 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.23.17pubmed: 24833992google scholar: lookup
                8. Takahashi T, Takano M, Kurebayashi Y, Masuda M, Kawagishi S, Takaguchi M, Yamanaka T, Minami A, Otsubo T, Ikeda K, Suzuki T. N-glycolylneuraminic acid on human epithelial cells prevents entry of influenza A viruses that possess N-glycolylneuraminic acid binding ability. J Virol 2014 Aug;88(15):8445-56.
                  doi: 10.1128/JVI.00716-14pubmed: 24829344google scholar: lookup
                9. Pecoraro HL, Bennett S, Garretson K, Quintana AM, Lunn KF, Landolt GA. Comparison of the Infectivity and Transmission of Contemporary Canine and Equine H3N8 Influenza Viruses in Dogs. Vet Med Int 2013;2013:874521.
                  doi: 10.1155/2013/874521pubmed: 24198997google scholar: lookup
                10. Anderson TC, Crawford PC, Katz JM, Dubovi EJ, Landolt G, Gibbs EP. Diagnostic performance of the canine influenza A virus subtype H3N8 hemagglutination inhibition assay. J Vet Diagn Invest 2012 May;24(3):499-508.
                  doi: 10.1177/1040638712440992pubmed: 22529116google scholar: lookup
                11. Yamanaka T, Nemoto M, Bannai H, Tsujimura K, Kondo T, Matsumura T, Muranaka M, Ueno T, Kinoshita Y, Niwa H, Hidari KI, Suzuki T. No evidence of horizontal infection in horses kept in close contact with dogs experimentally infected with canine influenza A virus (H3N8). Acta Vet Scand 2012 Apr 16;54(1):25.
                  doi: 10.1186/1751-0147-54-25pubmed: 22506984google scholar: lookup
                12. Branda F, Yon DK, Albanese M, Binetti E, Giovanetti M, Ciccozzi A, Ciccozzi M, Scarpa F, Ceccarelli G. Equine Influenza: Epidemiology, Pathogenesis, and Strategies for Prevention and Control. Viruses 2025 Feb 21;17(3).
                  doi: 10.3390/v17030302pubmed: 40143233google 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