Influenza A virus circulation in backyard animals in the Pacific coast of Guatemala, 2013-2014.


Journal

Zoonoses and public health
ISSN: 1863-2378
Titre abrégé: Zoonoses Public Health
Pays: Germany
ID NLM: 101300786

Informations de publication

Date de publication:
11 2022
Historique:
revised: 18 03 2022
received: 28 05 2021
accepted: 30 04 2022
pubmed: 26 5 2022
medline: 14 10 2022
entrez: 25 5 2022
Statut: ppublish

Résumé

Due to their documented epidemiological relevance as hosts for influenza A viruses (IAV), humans, poultry and pigs in backyard production systems (BPS) within wetlands could be key to the emergence of novel IAV variants able to transmit between humans or animals. To better understand the circulation of IAV at the human-animal interface of BPS within wetlands, we studied IAV in backyard duck flocks and pig herds in the Pacific Coast of Guatemala. From April 2013 to October 2014, we estimated the monthly IAV per cent seropositive and viral positive flocks and herds in two resource-limited communities. We detected antibodies in sera against the IAV nucleoprotein through ELISA. We also detected IAV viral RNA in respiratory (ducks and pigs) and cloacal (ducks) swabs through rRT-PCR directed at the matrix gene. We attempted viral isolation in eggs or MDCK cells followed by sequencing from swabs positive for IAV. During our study period, IAV seropositivity in duck flocks was 38%, and viral positivity was 23% (n = 86 BPS sampled). IAV seropositivity in pig herds was 42%, and viral positivity was 20% (n = 90 BPS sampled). Both flocks and herds had detectable antibodies against IAV mostly year-round, and IAV was detected in several months. We isolated an H3N2 virus from one pig sampled at the end of 2013. Standard nucleotide BLAST searches indicate that the isolated virus was similar to seasonal viruses circulating in humans, suggesting human-to-pig transmission. Our data show concurrent circulation of IAV in multiple species of poultry and pigs that were commingled in rudimentary conditions in proximity to humans, but no significant risk factors could be identified.

Identifiants

pubmed: 35611690
doi: 10.1111/zph.12972
doi:

Substances chimiques

Nucleoproteins 0
Nucleotides 0
RNA, Viral 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

826-834

Subventions

Organisme : CDC HHS
ID : 1U01GH000028
Pays : United States
Organisme : CDC HHS
ID : 5U01GH001003
Pays : United States
Organisme : NIAID NIH HHS
ID : HHSN266200700010C
Pays : United States
Organisme : NIAID NIH HHS
ID : HHSN272201400008C
Pays : United States

Informations de copyright

© 2022 Wiley-VCH GmbH.

Références

Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., & Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Research, 25(17), 3389-3402.
Bailey-Leonardo, E. L. (2011). Analisis espacial del humedal Monterrico: Identificacion de areas criticas e indice de riesgo para brotes de influenza aviar altamente patogena. (DVM Thesis). Universidad San Carlos de Guatemala, Guatemala.
Bowman, A. S., Nelson, S. W., Page, S. L., Nolting, J. M., Killian, M. L., Sreevatsan, S., & Slemons, R. D. (2014). Swine-to-human transmission of influenza A(H3N2) virus at agricultural fairs, Ohio, USA, 2012. Emerging Infectious Diseases, 20(9), 1472-1480. https://doi.org/10.3201/eid2009.131082
Bravo-Vasquez, N., Di Pillo, F., Lazo, A., Jimenez-Bluhm, P., Schultz-Cherry, S., & Hamilton-West, C. (2016). Presence of influenza viruses in backyard poultry and swine in El Yali wetland, Chile. Preventive Veterinary Medicine, 134, 211-215. https://doi.org/10.1016/j.prevetmed.2016.10.004
Bravo-Vasquez, N., Baumberger, C., Jimenez-Bluhm, P., Di Pillo, F., Lazo, A., Sanhueza, J., Schultz-Cherry, S., & Hamilton-West, C. (2020). Risk factors and spatial relative risk assessment for influenza A virus in poultry and swine in backyard production systems of Central Chile. Veterinary Medicine and Science, 6(3), 518-526. https://doi.org/10.1002/vms3.254
Buscaglia, C., Espinosa, C., Terrera, M. V., & De Benedetti, R. (2007). Avian influenza surveillance in backyard poultry of Argentina. Avian Diseases, 51(1), 467-469. https://doi.org/10.1637/7542.1
Campollo, E. M. (2012). Determinación de la presencia del virus de la gripe aviar (virus H5N1), en la población de aves de traspatio que conviven con aves migratorias, en los humedales de alto riesgo en la Republica de Guatemala, durante los años 2006 al 2007. CONCYT, SENACYT, FONACYT, UMG.
Ceron, A., Ortiz, M. R., Alvarez, D., Palmer, G. H., & Cordon-Rosales, C. (2016). Local disease concepts relevant to the design of a community-based surveillance program for influenza in rural Guatemala. International Journal for Equity in Health, 15, 69. https://doi.org/10.1186/s12939-016-0359-z
Consejo Municipal, T., & SEGEPLAN. (2010). Plan de Desarrollo Taxisco, Santa Rosa: Consejo Municipal de Desarrollo del Municipio de Taxisco, Santa Rosa y Secretaria de Planificacion y Programacion de la Presidencia, Direccion de Planificacion Territorial.
Donatelli, I., Castrucci, M. R., s De Marco, M. A., Delogu, M., & Webster, R. G. (2017). Human-animal Interface: The case for influenza interspecies transmission. Advances in Experimental Medicine and Biology, 972, 17-33. https://doi.org/10.1007/5584_2016_136
Eiserman, K. (2006). Evaluation of waterbird populations and their conservation in Guatemala. Guatemalan Society of Ornithology.
Ellison, A. M. (2004). Wetlands of Central America. Wetlands Ecology and Management, 12, 3-55.
FAO. (2008a). Biosecurity for highly pathogenic avian influenza: Issues and options. Food and Agriculture Organization of the United Nations.
FAO. (2010). Good practices for biosecurity in the pig sector. Food and Agriculture Organization of the United Nations.
Gonzalez-Reiche, A. S., Morales-Betoulle, M. E., Alvarez, D., Betoulle, J. L., Müller, M. L., Sosa, S. M., & Perez, D. R. (2012). Influenza A viruses from wild birds in Guatemala belong to the north American lineage. PLoS One, 7(3), e32873. https://doi.org/10.1371/journal.pone.0032873
Gonzalez-Reiche, A. S., Muller, M. L., Ortiz, L., Cordon-Rosales, C., & Perez, D. R. (2016). Prevalence and diversity of low pathogenicity avian influenza viruses in wild birds in Guatemala, 2010-2013. Avian Diseases, 60(1 Suppl), 359-364. https://doi.org/10.1637/11130-050715-Reg
Gonzalez-Reiche, A. S., Nelson, M. I., Angel, M., Muller, M. L., Ortiz, L., Dutta, J., van Bakel, H., Cordon-Rosales, C., & Perez, D. R. (2017a). Evidence of intercontinental spread and uncommon variants of low-pathogenicity avian influenza viruses in ducks overwintering in Guatemala. mSphere, 2(2), e00362. https://doi.org/10.1128/mSphere.00362-16
Gonzalez-Reiche, A. S., Ramirez, A. L., Muller, M. L., Orellana, D., Sosa, S. M., Ola, P., Paniagua, J., Ortíz, L., Hernandez, J., Cordón-Rosales, C., & Perez, D. R. (2017b). Origin, distribution, and potential risk factors associated with influenza A virus in swine in two production systems in Guatemala. Influenza and Other Respiratory Viruses, 11(2), 182-192. https://doi.org/10.1111/irv.12437
Gregory, C. G., Troy, M., Ana, W. C., Sharon, F. S., Christopher, W. O., Michael, C. A., & Charles, F. L. (2007). Swine workers and swine influenza virus infections. Emerging Infectious Disease journal, 13(12), 1871-1878. https://doi.org/10.3201/eid1312.061323
Gu, M., Xu, L., Wang, X., & Liu, X. (2017). Current situation of H9N2 subtype avian influenza in China. Veterinary Research, 48(1), 49. https://doi.org/10.1186/s13567-017-0453-2
Hernandez-Divers, S. M., Villegas, P., Prieto, F., Unda, J. C., Stedman, N., Ritchie, B., Carroll, R., & Hernandez-Divers, S. J. (2006). A survey of selected avian pathogens of backyard poultry in northwestern Ecuador. Journal of Avian Medicine and Surgery, 20(3), 147-158. https://doi.org/10.1647/2005-015r.1
Hernandez-Divers, S. M., Villegas, P., Jimenez, C., Hernandez-Divers, S. J., Garcia, M., Riblet, S. M., Carroll, C. R., O'Connor, B. M., Webb, J. L., Yabsley, M. J., Williams, S. M., & Sanchez, S. (2008). Backyard chicken flocks pose a disease risk for Neotropic birds in Costa Rica. Avian Diseases, 52(4), 558-566. https://doi.org/10.1637/8298-032808-Reg.1
Iqbal, M. (2009). Controlling avian influenza infections: The challenge of the backyard poultry. Journal of Molecular and Genetic Medicine, 3(1), 119-120. https://doi.org/10.4172/1747-0862.1000022
Jimenez-Bluhm, P., Di Pillo, F., Bahl, J., Osorio, J., Schultz-Cherry, S., & Hamilton-West, C. (2018). Circulation of influenza in backyard productive systems in Central Chile and evidence of spillover from wild birds. Preventive Veterinary Medicine, 153, 1-6. https://doi.org/10.1016/j.prevetmed.2018.02.018
Kile, J. C., Ren, R., Liu, L., Greene, C. M., Roguski, K., Iuliano, A. D., Jang, Y., Jones, J., Thor, S., Song, Y., Zhou, S., Trock, S. C., Dugan, V., Wentworth, D. E., Levine, M. Z., Uyeki, T. M., Katz, J. M., Jernigan, D. B., Olsen, S. J., … Davis, C. T. (2017). Update: Increase in human infections with novel Asian lineage avian influenza A(H7N9) viruses during the fifth epidemic - China, October 1, 2016-august 7, 2017. MMWR. Morbidity and Mortality Weekly Report, 66(35), 928-932. https://doi.org/10.15585/mmwr.mm6635a2
Lai, S., Qin, Y., Cowling, B. J., Ren, X., Wardrop, N. A., Gilbert, M., Tsang, T. K., Wu, P., Feng, L., Jiang, H., Peng, Z., Zheng, J., Liao, Q., Li, S., Horby, P. W., Farrar, J. J., Gao, G. F., Tatem, A. J., & Yu, H. (2016). Global epidemiology of avian influenza A H5N1 virus infection in humans, 1997-2015: A systematic review of individual case data. The Lancet Infectious Diseases, 16(7), 153-155.
Lowen, A. C. (2017). Constraints, drivers, and implications of influenza A virus reassortment. Annu Rev Virol, 4(1), 105-121. https://doi.org/10.1146/annurev-virology-101416-041726
Ma, W., Kahn, R. E., & Richt, J. A. (2008). The pig as a mixing vessel for influenza viruses: Human and veterinary implications. Journal of Molecular and Genetic Medicine, 3(1), 158-166.
Mena, I., Nelson, M. I., Quezada-Monroy, F., Dutta, J., Cortes-Fernandez, R., Lara-Puente, J. H., Castro-Peralta, F., Cunha, L. F., Trovão, N. S., Lozano-Dubernard, B., Rambaut, A., van Bakel, H., & Garcia-Sastre, A. (2016). Origins of the 2009 H1N1 influenza pandemic in swine in Mexico. eLife, 5, e16777. https://doi.org/10.7554/eLife.16777
Munoz, O., De Nardi, M., van der Meulen, K., van Reeth, K., Koopmans, M., Harris, K., von Dobschuetz, S., Freidl, G., Meijer, A., Breed, A., Hill, A., Kosmider, R., Banks, J., Stärk, K. D., Wieland, B., Stevens, K., van der Werf, S., Enouf, V., Dauphin, G., & FLURISK Consortium. (2016). Genetic adaptation of influenza A viruses in domestic animals and their potential role in interspecies transmission: A literature review (vol 13, pg 171, 2016). EcoHealth, 13(1), 199. https://doi.org/10.1007/s10393-015-1031-6
Nasreen, S., Khan, S. U., Luby, S. P., Gurley, E. S., Abedin, J., Zaman, R. U., Sohel, B. M., Rahman, M., Hancock, K., Levine, M. Z., Veguilla, V., Wang, D., Holiday, C., Gillis, E., Sturm-Ramirez, K., Bresee, J. S., Rahman, M., Uyeki, T. M., Katz, J. M., & Azziz-Baumgartner, E. (2015). Highly pathogenic avian influenza A(H5N1) virus infection among Workers at Live Bird Markets, Bangladesh, 2009-2010. Emerging Infectious Disease journal, 21(4), 629-637. https://doi.org/10.3201/eid2104.141281
Nelson, M. I., Gramer, M. R., Vincent, A. L., & Holmes, E. C. (2012). Global transmission of influenza viruses from humans to swine. The Journal of General Virology, 93(Pt 10), 2195-2203. https://doi.org/10.1099/vir.0.044974-0
Neumann, G., Noda, T., & Kawaoka, Y. (2009). Emergence and pandemic potential of swine-origin H1N1 influenza virus. Nature, 459(7249), 931-939. https://doi.org/10.1038/nature08157
OIRSA. (2016). Northern Guatemala is officially declared free of low pathogenicity avian influenza virus subtype H5N2 (report in Spanish). https://www.orisa.org/noticia-detalle.aspx?id=1313
Renshaw, H. W. (1975). Influence of antibody-mediated immune suppression on clinical, viral, and immune responses to swine influenza infection. American Journal of Veterinary Research, 36(1), 5-13.
Saavedra-Montanez, M., Carrera-Aguirre, V., Castillo-Juarez, H., Rivera-Benitez, F., Rosas-Estrada, K., Pulido-Camarillo, E., Mercado-García, C., Carreón-Nápoles, R., Haro-Tirado, M., Rosete, D. P., Cabello, C., Manjarrez, M. E., Sánchez-Betancourt, I., & Ramirez-Mendoza, H. (2013). Retrospective serological survey of influenza viruses in backyard pigs from Mexico City. Influenza and Other Respiratory Viruses, 7(5), 827-832. https://doi.org/10.1111/irv.12063
Samir, R., Eduardo, A.-B., Marwa Mohamed, A., Manal, F., Katherine, R., Elaziz, H. A., Iuliano, A. D., Salah, N., Uyeki, T. M., Lindstrom, S., Davis, C. T., Eid, A., & Genedy, M. (2015). Increased number of human cases of influenza virus a(H5N1) infection, Egypt, 2014-15. Emerging Infectious Disease journal, 21(12), 2171-2173. https://doi.org/10.3201/eid2112.150885
Senne, D. A. (2003). Avian influenza in the Western hemisphere including the Pacific Islands and Australia. Avian Diseases, 47(3 Suppl), 798-805.
Sigüenza De Micheo, R. (2007). Duck counts in Guatemala, final report 2006/2007 season (in Spanish): Fundacion Defensores de la Naturaleza, Ducks Unlimited, USAC.
Slomka, M. J., Densham, A. L., Coward, V. J., Essen, S., Brookes, S. M., Irvine, R. M., Spackman, E., Ridgeon, J., Gardner, R., Hanna, A., Suarez, D. L., & Brown, I. H. (2010). Real time reverse transcription (RRT)-polymerase chain reaction (PCR) methods for detection of pandemic (H1N1) 2009 influenza virus and European swine influenza A virus infections in pigs. Influenza and Other Respiratory Viruses, 4(5), 277-293. https://doi.org/10.1111/j.1750-2659.2010.00149.x
Spackman, E., Senne, D. A., Myers, T. J., Bulaga, L. L., Garber, L. P., Perdue, M. L., Lohman, K., Daum, L. T., & Suarez, D. L. (2002). Development of a real-time reverse transcriptase PCR assay for type a influenza virus and the avian H5 and H7 hemagglutinin subtypes. Journal of Clinical Microbiology, 40(9), 3256-3260.
Spackman, E., Ip, H. S., Suarez, D. L., Slemons, R. D., & Stallknecht, D. E. (2008). Analytical validation of a real-time reverse transcription polymerase chain reaction test for pan-American lineage H7 subtype avian influenza viruses. Journal of Veterinary Diagnostic Investigation, 20(5), 612-616. https://doi.org/10.1177/104063870802000512
Tinoco, Y. O., Montgomery, J. M., Kasper, M. R., Nelson, M. I., Azziz-Baumgartner, E., Gilman, R. H., Azziz-Baumgartner, E., Widdowson, M. A., Barnes, J., Gilman, R. H., Bausch, D. G., & Gonzalez, A. E. (2015). Transmission dynamics of pandemic influenza A(H1N1)pdm09 virus in humans and swine in backyard farms in Tumbes, Peru. Influenza and Other Respiratory Viruses 10(1), 47-56. https://doi.org/10.1111/irv.12329
Tolf, C., Latorre-Margalef, N., Wille, M., Bengtsson, D., Gunnarsson, G., Grosbois, V., Hasselquist, D., Olsen, B., Elmberg, J., & Waldenstrom, J. (2013). Individual variation in influenza A virus infection histories and long-term immune responses in mallards. PLoS One, 8(4), e61201. https://doi.org/10.1371/journal.pone.0061201
Tse, M., Kim, M., Chan, C. H., Ho, P. L., Ma, S. K., Guan, Y., & Peiris, J. S. (2012). Evaluation of three commercially available influenza A type-specific blocking enzyme-linked immunosorbent assays for seroepidemiological studies of influenza A virus infection in pigs. Clinical and Vaccine Immunology, 19(3), 334-337. https://doi.org/10.1128/CVI.05358-11
Webster, R. G., Bean, W. J., Gorman, O. T., Chambers, T. M., & Kawaoka, Y. (1992). Evolution and ecology of influenza A viruses. Microbiological Reviews, 56(1), 152-179.
WHO. (2011). Manual for the laboratory diagnosis and virological surveillance of influenza. WHO.
WHO/FluNet. (2021). Influenza laboratory surveillance information: Guatemala 2013-2014. www.who.int/flunet
Wong, J. T., de Bruyn, J., Bagnol, B., Grieve, H., Li, M., Pym, R., & Alders, R. G. (2017). Small-scale poultry and food security in resource-poor settings: A review. Global Food Security, 15, 43-52.
Zhou, B., & Wentworth, D. E. (2012). Influenza A virus molecular virology techniques. Methods in Molecular Biology, 865, 175-192. https://doi.org/10.1007/978-1-61779-621-0_11

Auteurs

Maria L Müller-Theissen (ML)

Centro de Estudios en Salud, Universidad del Valle de Guatemala, Guatemala, Guatemala.

Eduardo Azziz-Baumgartner (E)

Influenza Division, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, USA.

Lucia Ortiz (L)

Centro de Estudios en Salud, Universidad del Valle de Guatemala, Guatemala, Guatemala.

Christine M Szablewski (CM)

Influenza Division, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, USA.

Danilo Alvarez (D)

Centro de Estudios en Salud, Universidad del Valle de Guatemala, Guatemala, Guatemala.

Ana S Gonzalez-Reiche (AS)

Centro de Estudios en Salud, Universidad del Valle de Guatemala, Guatemala, Guatemala.

Jorge Jara (J)

Centro de Estudios en Salud, Universidad del Valle de Guatemala, Guatemala, Guatemala.

C Todd Davis (CT)

Influenza Division, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, USA.

Celia Cordon-Rosales (C)

Centro de Estudios en Salud, Universidad del Valle de Guatemala, Guatemala, Guatemala.

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