Abstract
Influenza constitutes a challenge to animal and human health. It is a highly contagious disease with wildlife reservoirs and considered as endemic among swine populations. Pigs are crucial in the disease dynamics due to their capacity to generate new reassortant viruses. The risk of informal animal trade in the spread of zoonotic diseases is well recognized worldwide. Nevertheless, the contribution of the backyard pig trade network in the transmission of influenza in a wildlife/livestock interface area is unknown. This study provides the first simulation of influenza transmission based on backyard farm connections in Mexico. A susceptible-infectious-recovered (SIR) model was implemented using the Epimodel software package in R, and 260 backyard farms were considered as nodes. Three different scenarios of connectivity (low, medium, and high) mediated by trade were generated and compared. Our results suggest that half of the pig population were infected within 5 days in the high connectivity scenario and the number of infected farms was approximately 65-fold higher compared to the low connected one. The consequence of connectivity variations directly influenced both time and duration of influenza virus transmission. Therefore, high connectivity driven by informal trade constitutes a significant risk to animal health. Trade patterns of animal movements are complex. This approach emphasizes the importance of pig movements and spatial dynamics among backyard production, live animal markets, and wildlife.
This is a preview of subscription content, access via your institution.



References
Büttner, K., Krieter, J., Traulsen, A. and Traulsen, I., 2013. Static network analysis of a pork supply chain in Northern Germany—Characterisation of the potential spread of infectious diseases via animal movements Preventive Veterinary Medicine, 110, 418–428
Cappelle, J., Gaidet, N., Iverson, S.A., Takekawa, J.Y., Newman, S.H., Fofana, B. and Gilbert, M., 2011. Characterizing the interface between wild ducks and poultry to evaluate the potential of transmission of avian pathogens International Journal of Health Geographics, 10, 60
Cisneros, L.F., Valdivia, A.G., Waldrup, K., Díaz-Aparicio, E., Martínez-de-Anda, A., Cruz-Vázquez, C.R. and Ortiz, R., 2012. Surveillance for Mycobacterium bovis transmission from domestic cattle to wild ruminants in a Mexican wildlife-livestock interface area American Journal of Veterinary Research, 73, 1617–1625
De la Rosa, M. del P., 2007. Aspectos socioculturales, económicos, sanitarios y bienestar animal que influyen en la conducta de las personas que comercializan équidos en el mercado de San Bernabé, Almoloya de Juárez, Estado de México (Universidad Nacional Autónoma de México: Ciudad de México)
Dorjee, S., Poljak, Z., Revie, C.W., Bridgland, J., McNab, B., Leger, E. and Sanchez, J., 2013. A Review of Simulation Modelling Approaches Used for the Spread of Zoonotic Influenza Viruses in Animal and Human Populations: Approaches to Modelling Influenza Zoonoses and Public Health, 60, 383–411
Fasina, F.O., Mokoele, J.M., Spencer, B.T., Van Leengoed, L.A.M.L., Bevis, Y. and Booysen, I., 2015. Spatio-temporal patterns and movement analysis of pigs from smallholder farms and implications for African swine fever spread, Limpopo province, South Africa Onderstepoort J Vet Res, 82
Févre, E.M., Bronsvoort, B.M. de C., Hamilton, K.A. and Cleaveland, S., 2006. Animal movements and the spread of infectious diseases Trends in Microbiology, 14, 125–131
Gutiérrez-Ruiz EJ, Aranda-Cirerol FJ, Rodríguez-Vivas RI, Bolio-González ME, Ramírez González S and Estrella-Tec J, 2012. Factores sociales de la crianza de animales de traspatio en Yucatán, México Bioagrociencias, 5, 20–28
Kukielka, E.A., Martínez-López, B. and Beltrán-Alcrudo, D., 2017. Modeling the live-pig trade network in Georgia: Implications for disease prevention and control PLOS ONE, 12, e0178904
Lebl, K., Lentz, H.H.K., Pinior, B. and Selhorst, T., 2016. Impact of Network Activity on the Spread of Infectious Diseases through the German Pig Trade Network Frontiers in Veterinary Science, 3
Leslie, E.E.C., Geong, M., Abdurrahman, M., Ward, M.P. and Toribio, J.-A.L.M.L., 2016. Live pig markets in eastern Indonesia: Trader characteristics, biosecurity and implications for disease spread Acta Tropica, 155, 95–103
Miguel, E., Grosbois, V., Caron, A., Boulinier, T., Fritz, H., Cornélis, D., Foggin, C., Makaya, P.V., Tshabalala, P.T. and de Garine-Wichatitsky, M., 2013. Contacts and foot and mouth disease transmission from wild to domestic bovines in Africa Ecosphere, 4, art51
Miller, R.S., Farnsworth, M.L. and Malmberg, J.L., 2013. Diseases at the livestock–wildlife interface: Status, challenges, and opportunities in the United States Preventive Veterinary Medicine, 110, 119–132
National Institute of Statistics and Geography (INEGI), 2007. Censo Agrícola, Ganadero y Forestal, (México)
Pohlmann, A., Starick, E., Harder, T., Grund, C., Höper, D., Globig, A., Staubach, C., Dietze, K., Strebelow, G., Ulrich, R.G., Schinköthe, J., Teifke, J.P., Conraths, F.J., Mettenleiter, T.C. and Beer, M., 2017. Outbreaks among Wild Birds and Domestic Poultry Caused by Reassorted Influenza A(H5N8) Clade 2.3.4.4 Viruses, Germany, 2016 Emerging Infectious Diseases, 23, 633–636
R Development Core Team, 2017. R: A language and environment for statistical computing. R Foundation for Statistical Computing, (Vienna, Austria)
Reynolds, J.J.H., Torremorell, M. and Craft, M.E., 2014. Mathematical Modeling of Influenza A Virus Dynamics within Swine Farms and the Effects of Vaccination PLoS ONE, 9, e106177
Romagosa, A., Allerson, M., Gramer, M., Joo, H., Deen, J., Detmer, S. and Torremorell, M., 2011. Vaccination of influenza a virus decreases transmission rates in pigs Veterinary Research, 42, 120
Schulz, J., Boklund, A., Halasa, T.H.B., Toft, N. and Lentz, H.H.K., 2017. Network analysis of pig movements: Loyalty patterns and contact chains of different holding types in Denmark PLOS ONE, 12, e0179915
Short, K.R., Richard, M., Verhagen, J.H., van Riel, D., Schrauwen, E.J.A., van den Brand, J.M.A., Mänz, B., Bodewes, R. and Herfst, S., 2015. One health, multiple challenges: The inter-species transmission of influenza A virus One Health, 1, 1–13
Torremorell, M., Allerson, M., Corzo, C., Diaz, A. and Gramer, M., 2012. Transmission of Influenza A Virus in Pigs: Transmission of Influenza Virus in Pigs Transboundary and Emerging Diseases, 59, 68–84
Tufiño, C., 2013. Caracterización molecular de los virus de influenza A que circulan en cerdos en la región del Bajío Mexicano (Universidad Nacional Autónoma de México: Ciudad de México)
Wiethoelter, A.K., Beltrán-Alcrudo, D., Kock, R. and Mor, S.M., 2015. Global trends in infectious diseases at the wildlife–livestock interface Proceedings of the National Academy of Sciences, 112, 9662–9667
Zepeda–Gómez, C., Lot–Helgueras, A., Nemiga, X.A. and Madrigal–Uribe, D., 2012. Floristics and diversity of the Lerma river wetlands in the State of Mexico 23–49
Acknowledgments
The authors are grateful to the National Institute of Statistics and Geography (INEGI) for the information obtained in the “Censo Agrícola, Ganadero y Forestal 2007” and the facilities for data processing in the Microdata Laboratory. We also acknowledge the help provided by the Academic Writing Team at Universidad Nacional Autónoma de México for the text edition.
Funding
The study received financial support from the PAPIIT project IA-205916.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Ethical standards
The manuscript does not contain clinical studies or patient data.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Mateus-Anzola, J., Wiratsudakul, A., Rico-Chávez, O. et al. Simulation modeling of influenza transmission through backyard pig trade networks in a wildlife/livestock interface area. Trop Anim Health Prod 51, 2019–2024 (2019). https://doi.org/10.1007/s11250-019-01892-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11250-019-01892-4