Isolation and characterization of influenza A virus (H6N2) from a temporary artificial pond in Mexico

Rodrigo Jesús Barrón-Rodríguez, Fernando Chávez-Maya, Elizabeth Loza-Rubio, Gary García-Espinosa

Abstract


Veterinaria México OA
ISSN: 2448-6760

Cite this as:

  • Barrón-Rodríguez RJ, Chávez-Maya F, Loza-Rubio E, García-Espinosa G. Isolation and characterization of influenza A virus (H6N2) from a temporary artificial pond in Mexico. Veterinaria México OA. 2018;5(2). doi: 10.21753/5.2.475..

Most epidemiological surveillance studies of the influenza A virus (IAV) have focused on the isolation and detection of the virus in wild birds. However, there are limited descriptions of both the wild duck population and the purpose and size of the aquatic habitats where viruses have been detected or isolated. The objective of this study was to determine if a pond of 16 hectares (39.536 acres), used for agricultural and fishing purposes and visited by approximately 9000 wild migratory ducks consisting of nine different species during the wintering stay, is suitable to support the isolation of IAV. One influenza A virus was isolated from Pekin ducks used as sentinels during the wintering stay season from September 2007 to March 2008. Only one IAV subtype was isolated from 9 of the 88 samples collected from the sentinel ducks over seven months, and the molecular characterization of this isolate revealed an H6N2 virus subtype. Based on this information, it is suggested that a pond such as the one in this study provides a suitable biological setting to support the presence of IAV, but the minimum biological environment to isolate the influenza A virus is still unknown.

Figure 1. Location of the artificial pond in the State of Mexico with 19°24’22” N, 99°41’36” W coordinates and the routes of migratory birds in America (Google Earth).

Keywords


Influenza in birds; wetland; ponds; ducks

Full Text:

PDF

References


Fan Z, Ci Y, Ma Y, Liu L, Wang D, Ma J, et al. Phylogenetic analysis of a novel H6N6 avian influenza virus isolated from a green peafowl in China and its pathogenic potential in mice. Infect Genet Evol. 2014;28:107-12. doi: https:// doi.org/10.1016/j.meegid.2014.09.008.

Hanson BA, Stallknecht DE, Swayne DE, Lewis LA, Senne DA. Avian influenza viruses in Minnesota ducks during 1998–2000. Avian Dis. 2003;47(s3):867- 71. doi: 10.1637/0005-2086-47.s3.867.

Krauss S, Walker D, Pryor SP, Niles L, Chenghong L, Hinshaw VS, et al. Influenza A viruses of migrating wild aquatic birds in North America. Vector Borne Zoonotic Dis. 2004;4(3):177-89. doi: 10.1089/vbz.2004.4.177

Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol Rev. 1992;56(1):152-79.

Stallknecht DE, Shane SM, Zwank PJ, Senne DA, Kearney MT. Avian influenza viruses from migratory and resident ducks of coastal Louisiana. Avian Dis. 1990;34(2):398-405.

Fouchier RA, Munster VJ. Epidemiology of low pathogenic avian influenza viruses in wild birds. Revue scientifique et technique (International Office of Epizootics). 2009;28(1):49-58.

Vandegrift KJ, Sokolow SH, Daszak P, Kilpatrick AM. Ecology of avian influenza viruses in a changing world. Annals of the New York Academy of Sciences. 2010;1195:113-28. doi: 10.1111/j.1749-6632.2010.05451.x.

Stallknecht DE, Goekjian VH, Wilcox BR, Poulson RL, Brown JD. Avian influenza virus in aquatic habitats: what do we need to learn? Avian Dis. 2010;54(1 Suppl):461-5. doi: 10.1637/8760-033109-Reg.1.

Gilbert M, Xiao X, Domenech J, Lubroth J, Martin V, Slingenbergh J. Anatidae migration in the western palearctic and spread of highly pathogenic avian influenza H5NI virus. Emerging infectious diseases. 2006;12(11):1650-6. doi: 10.3201/ eid1211.060223.

Krauss S, Stallknecht DE, Slemons RD, Bowman AS, Poulson RL, Nolting JM, et al. The enigma of the apparent disappearance of Eurasian highly pathogenic H5 clade 2.3.4.4 influenza A viruses in North American waterfowl. Proceedings of the National Academy of Sciences of the United States of America. 2016;113(32):9033-8. doi: 10.1073/pnas.1608853113.

Paul MC, Gilbert M, Desvaux S, Rasamoelina Andriamanivo H, Peyre M, Khong NV, et al. Agro-environmental determinants of avian influenza circulation: A multisite study in Thailand, Vietnam and Madagascar. PLOS ONE. 2014;9(7):e101958. doi: 10.1371/journal.pone.0101958.

Alexander DJ. An overview of the epidemiology of avian influenza. Vaccine. 2007;25(30):5637-44. doi: 10.1016/j.vaccine.2006.10.051.

Cecchi G, Ilemobade A, Le Brun Y, Hogerwerf L, Slingenbergh J. Agro-ecological features of the introduction and spread of the highly pathogenic avian influenza (HPAI) H5N1 in northern Nigeria. Geospatial health. 2008;3(1):7-16. doi: 10.4081/gh.2008.227.

Reeber S. Waterfowl of North America, Europe & Asia, An Identification Guide. [Internet]2015. Available from: https://press.princeton.edu/titles/10714.html.

Spivey TJ, Lindberg MS, Meixell BW, Smith KR, Puryear WB, Davis KR, et al. Maintenance of influenza A viruses and antibody response in mallards (Anas platyrhynchos) sampled during the non-breeding season in Alaska. PLOS ONE. 2017;12(8):e0183505. doi: 10.1371/journal.pone.0183505.

Secretaría del Medio Ambiente y Recursos Naturales. Estrategia para la conservación, manejo y aprovechamiento sustentable de las aves acuáticas y su hábitat en México. [Internet]2008. Available from: http://www.dumac.org/dumac/ habitat/esp/pdf/AvesAcuaticas.pdf.

Vázquez Rivera H. Preferencia de hábitat por la avifauna presente en la laguna Chimaliapan, Ciénagas de Lerma, Lerma, Estado de México [Master’s degree]. DF(MX): Universidad Nacional Autónoma de México; 2004.

van Perlo B. Birds of Mexico and Central America. New Jersey (US): Princeton University Press; 2006. 336 p.

Bibby CJ. Bird census techniques. 2nd ed. London (UK): Academic Press; 2000.

Dufour-Zavala L, American Association of Avian P. A laboratory manual for the isolation, identification and characterization of avian pathogens. Jacksonville, Fl.: American Association of Avian Pathologists; 2008.

Hoffmann E, Stech J, Guan Y, Webster RG, Perez DR. Universal primer set for the full-length amplification of all influenza A viruses. Archives of virology. 2001;146(12):2275-89.

Rozen S, Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods in molecular biology (Clifton, NJ). 2000;132:365-86.

Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular biology and evolution. 2013;30(12):2725-9. doi: 10.1093/molbev/mst197.

Reeves AB, Pearce JM, Ramey AM, Ely CR, Schmutz JA, Flint PL, et al. Genomic analysis of avian influenza viruses from waterfowl in western Alaska, USA. Jour¬nal of wildlife diseases. 2013;49(3):600-10. doi: 10.7589/2012-04-108.

Pedersen K, Swafford SR, DeLiberto TJ. Low pathogenicity avian influenza subtypes isolated from wild birds in the United States, 2006-2008. Avian Dis. 2010;54(1 Suppl):405-10. doi: 10.1637/8693-031309-Reg.1.

Runstadler JA, Happ GM, Slemons RD, Sheng ZM, Gundlach N, Petrula M, et al. Using RRT-PCR analysis and virus isolation to determine the prevalence of avian influenza virus infections in ducks at Minto Flats State Game Refuge, Alaska, during August 2005. Archives of virology. 2007;152(10):1901-10. doi: 10.1007/s00705-007-0994-1.

Parmley EJ, Bastien N, Booth TF, Bowes V, Buck PA, Breault A, et al. Wild bird influenza survey, Canada, 2005. Emerging infectious diseases. 2008;14(1):84- 7. doi: 10.3201/eid1401.061562.

Goekjian VH, Smith JT, Howell DL, Senne DA, Swayne DE, Stallknecht DE. Avian influenza viruses and avian paramyxoviruses in wintering and breeding waterfowl populations in North Carolina, USA. Journal of wildlife diseases. 2011;47(1):240-5. doi: 10.7589/0090-3558-47.1.240.

Rollo SN, Ferro PJ, Peterson MJ, Ward MP, Ballard BM, Lupiani B. Role of nonmigratory mottled ducks (Anas fulvigula) as sentinels for avian influenza surveillance. Journal of zoo and wildlife medicine : official publication of the American Association of Zoo Veterinarians. 2012;43(1):168-70. doi: 10.1638/2011-0038.1.

Ferro PJ, El-Attrache J, Fang X, Rollo SN, Jester A, Merendino T, et al. Avian influenza surveillance in hunter-harvested waterfowl from the Gulf Coast of Texas (November 2005-January 2006). Journal of wildlife diseases. 2008;44(2):434- 9. doi: 10.7589/0090-3558-44.2.434.

Berlanga H, Calderón Parra R, Héctor Gómez de S, Ortega Álvarez R, Rodríguez Contreras V, Sánchez González LA, et al. Aves de México : lista actualizada de especies y nombres comunes 2015. México :: Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (CONABIO); 2015.

Jourdain E, Gunnarsson G, Wahlgren J, Latorre-Margalef N, Bröjer C, Sahlin S, et al. Influenza virus in a natural host, the mallard: Experimental infection data. PLOS ONE. 2010;5(1):e8935. doi: 10.1371/journal.pone.0008935.

Boonyapisitsopa S, Chaiyawong S, Nonthabenjawan N, Jairak W, Prakairungnamthip D, Bunpapong N, et al. Sentinel model for influenza A virus monitoring in free-grazing ducks in Thailand. Veterinary microbiology. 2016;182:35-43. doi: 10.1016/j.vetmic.2015.10.023.

Coman A, Maftei DN, Chereches RM, Zavrotchi E, Bria P, Dragnea C, et al. Avian influenza surveillance in the danube delta using sentinel geese and ducks. Influenza research and treatment. 2014;2014:965749. doi: 10.1155/2014/965749.

Globig A, Baumer A, Revilla-Fernández S, Beer M, Wodak E, Fink M, et al. Ducks as Sentinels for Avian Influenza in Wild Birds. Emerging infectious diseases. 2009;15(10):1633-6. doi: 10.3201/eid1510.090439.

Wille M, Lindqvist K, Muradrasoli S, Olsen B, Järhult JD. Urbanization and the dynamics of RNA viruses in mallards (Anas platyrhynchos). Infect Genet Evol. 2017;51:89-97. doi: https://doi.org/10.1016/j.meegid.2017.03.019.

Ito T, Okazaki K, Kawaoka Y, Takada A, Webster RG, Kida H. Perpetuation of influenza A viruses in Alaskan waterfowl reservoirs. Archives of virology. 1995;140(7):1163-72.

Ornelas-Eusebio E, Obregon-Ascencio A, Chavez-Maya F, Garcia-Espinosa G. Molecular characterization of an influenza A virus (H4N2) isolated from waterfowl habitats in the State of Mexico. The Journal of veterinary medical science. 2015;77(3):365-9. doi: 10.1292/jvms.14-0267.

Lang AS, Kelly A, Runstadler JA. Prevalence and diversity of avian influenza viruses in environmental reservoirs. The Journal of general virology. 2008;89(Pt 2):509-19. doi: 10.1099/vir.0.83369-0.

Markwell DD, Shortridge KF. Possible waterborne transmission and maintenance of influenza viruses in domestic ducks. Applied and environmental microbiology. 1982;43(1):110-5.

Ramey AM, Pearce JM, Reeves AB, Franson JC, Petersen MR, Ip HS. Evidence for limited exchange of avian influenza viruses between seaducks and dabbling ducks at Alaska Peninsula coastal lagoons. Archives of virology. 2011;156(10):1813-21. doi: 10.1007/s00705-011-1059-z.

Fan Z, Ci Y, Ma Y, Liu L, Ma J, Li DY, et al. Phylogenetic and pathogenic analysis of a novel H6N2 avian influenza virus isolated from a green peafowl in a wildlife park. Avian Dis. 2014;58(4):632-7. doi: 10.1637/10899-071114-ResNote.1.

Jiao P, Yuan R, Wei L, Jia B, Cao L, Song Y, et al. Complete genomic sequence of a novel natural recombinant H6N2 influenza virus from chickens in Guangdong, Southern China. Journal of virology. 2012;86(14):7717-8. doi: 10.1128/ jvi.00963-12.

Chin PS, Hoffmann E, Webby R, Webster RG, Guan Y, Peiris M, et al. Molecular evolution of H6 influenza viruses from poultry in southeastern China: Prevalence of H6N1 influenza viruses possessing seven A/Hong Kong/156/97 (H5N1)- like genes in poultry. Journal of virology. 2002;76(2):507-16. doi: 10.1128/ JVI.76.2.507-516.2002.

Ni F, Kondrashkina E, Wang Q. Structural and functional studies of influenza virus A/H6 hemagglutinin. PLOS ONE. 2015;10(7):e0134576. doi: 10.1371/journal. pone.0134576.

Matrosovich M, Zhou N, Kawaoka Y, Webster R. The surface glycoproteins of H5 influenza viruses isolated from humans, chickens, and wild aquatic birds have distinguishable properties. Journal of virology. 1999;73(2):1146-55.

Brookes DW, Miah S, Lackenby A, Hartgroves L, Barclay WS. Pandemic H1N1 2009 influenza virus with the H275Y oseltamivir resistance neuraminidase mutation shows a small compromise in enzyme activity and viral fitness. The Journal of antimicrobial chemotherapy. 2011;66(3):466-70. doi: 10.1093/jac/ dkq486.

To KK, Chan JF, Chen H, Li L, Yuen KY. The emergence of influenza A H7N9 in human beings 16 years after influenza A H5N1: a tale of two cities. The Lancet Infectious diseases. 2013;13(9):809-21. doi: 10.1016/s1473-3099(13)70167-1.

Li Z, Chen H, Jiao P, Deng G, Tian G, Li Y, et al. Molecular basis of replication of duck H5N1 influenza viruses in a mammalian mouse model. Journal of virology. 2005;79(18):12058-64. doi: 10.1128/jvi.79.18.12058-12064.2005.

Jiao P, Tian G, Li Y, Deng G, Jiang Y, Liu C, et al. A single-amino-acid substitution in the NS1 protein changes the pathogenicity of H5N1 avian influenza viruses in mice. Journal of virology. 2008;82(3):1146-54. doi: 10.1128/jvi.01698-07.

Jackwood MW, Suarez DL, Hilt D, Pantin-Jackwood MJ, Spackman E, Woolcock P, et al. Biologic characterization of chicken-derived H6N2 low pathogenic avian influenza viruses in chickens and ducks. Avian Dis. 2010;54(1):120-5. doi: 10.1637/8987-070909-ResNote.1.

Ozaki H, Guan Y, Peiris M, Webster R, Takada A, Webby R. Effect of the PB2 and M Genes on the replication of H6 influenza virus in chickens. Influenza research and treatment. 2014;2014:547839. doi: 10.1155/2014/547839.




DOI: http://dx.doi.org/10.21753/vmoa.5.2.475

Refbacks

  • There are currently no refbacks.