epidemiology; influenza A virus; mammals; public health; risk assessment; transmission
Abstract :
[en] [en] AIMS: The world experienced a huge number of outbreaks of highly pathogenic avian influenza (HPAI) in birds, which could represent one of the largest registered epidemics of infectious disease in food-producing animals. Therefore, mammals, including humans, are continuously exposed to HPAI viruses leading to sporadic and sometimes unusual mammal infections. The aim of this paper is to assess the risk of crossing the avian/mammalian species barrier by the currently circulating HPAI viruses, focusing on the epidemiological situation of Belgium, a representative country for Western Europe.
METHODS AND RESULTS: Information on transmission pathways and species susceptibility, based on the experimental and epidemiological data, was reviewed and weighted to assess the risk of mammal infection with HPAI A(H5N1) viruses of the circulating clade 2.3.4.4b. This risk is defined as the likelihood of mammal infection by birds crossed by the clinical consequences of this infection for this animal. From the Belgian perspective, it is concluded that this risk remains 'low' to 'moderate' for captive/domestic mammal species. However, this risk was categorised as 'high' for certain species, i.e. mammals that have the opportunity to have frequent direct or indirect close contacts with infected (dead) birds, such as wild felids, wild mustelids, foxes and wild marine carnivore mammals. For some mammal species, the uncertainty associated with the assessment remains high due to an ever-changing situation.
CONCLUSIONS: The longer the virus will continue to circulate in wildlife/the environment the stronger the probability of contact between infected birds and mammals will become. This will increase the related risk of viral adaptation for efficient transmission between mammal, posing concerns for public health. Regular reassessments based on the field and experimental data are therefore necessary to implement and adapt risk-based mitigation measures. This will require continuous monitoring of avian influenza viruses in both birds and mammals as well as sharing of sequence data.
Disciplines :
Veterinary medicine & animal health
Author, co-author :
Van Leeuw, Virginie; Federal Agency for the Safety of the Food Chain, Brussels, Belgium
Depoorter, Pieter; Federal Agency for the Safety of the Food Chain, Brussels, Belgium
Mauroy, Axel ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires (DMI) > Virologie vétérinaire et maladies virales animales ; Federal Agency for the Safety of the Food Chain, Brussels, Belgium
Rettigner, Chantal; Federal Agency for the Safety of the Food Chain, Brussels, Belgium
Rouffaer, Lieze; Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium
Stassijns, Jorgen; Sciensano, Brussels, Belgium
Steensels, Mieke; Sciensano, Brussels, Belgium
Van Gucht, Steven; Sciensano, Brussels, Belgium
Van Reeth, Kristien; Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium
Vermeersch, Katie; Federal Public Service Health, Food Chain Safety and Environment, Brussels, Belgium
Vervaeke, Muriel; Policy Department-Wildlife Disease Management, Agency for Nature and Forests, Brussels, Belgium
Saegerman, Claude ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires (DMI) > Epidémiologie et analyse des risques appliqués aux sciences vétérinaires
Abdelwhab, E. M., and T. C. Mettenleiter. 2023. “Zoonotic Animal Influenza Virus and Potential Mixing Vessel Hosts.” Viruses 15: 980. https://doi.org/10.3390/v15040980.
Agüero, M., I. Monne, O. Azucena Sánchez, et al. 2023. “Highly Pathogenic Avian Influenza A(H5N1) Virus Infection in Farmed Minks, Spain, October 2022.” Eurosurveillance 28: 2300001. https://doi.org/10.2807/1560-7917.ES.2023.28.3.2300001.
Animal and Plant Health Inspection Service (APHIS). 2024. “Highly Pathogenic Avian Influenza (HPAI) Detections in Livestock.” https://www.aphis.usda.gov/livestock-poultry-disease/avian/avian-influenza/hpai-detections/livestock.
Animal and Plant Health Inspection Service—U.S. Department of Agriculture (USDA). 2024. “Highly Pathogenic Avian Influenza (HPAI) H5N1 Detections in Alpacas.” https://www.aphis.usda.gov/livestock-poultry-disease/avian/avian-influenza/hpai-detections/mammals/highly-pathogenic-avian.
Antigua, K. J. C., W. S. Choi, Y. H. Baek, and M. S. Song. 2019. “The Emergence and Decennary Distribution of Clade 2.3.4.4 HPAI H5NX.” Microorganisms 7: 156. https://doi.org/10.3390/microorganisms7060156.
Arruda, B., A. L. V. Baker, A. Buckley, et al. 2024. “Divergent Pathogenesis and Transmission of Highly Pathogenic Avian Influenza A(H5N1) in Swine.” Emerging Infectious Disease 30, no. 4: 738–751. https://doi.org/10.3201/eid3004.231141.
Avian Flu Data Portal, and EURL for Avian Influenza and Newcastle Disease. 2024. “General Situation.” https://eurlaidata.izsvenezie.it/epidemio.php.
Briand, F. X., F. Souchaud, I. Pierre, et al. 2023. “Highly Pathogenic Avian Influenza A(H5N1) Clade 2.3.4.4b Virus in Domestic Cat, France, 2022.” Emerging Infectious Disease 29: 1696–1698. https://doi.org/10.3201/eid2908.230188.
Burrough, E. R., D. R. Magstadt, B. Petersen, et al. 2024. “Highly Pathogenic Avian Influenza A(H5N1) Clade 2.3.4.4b Virus Infection in Domestic Dairy Cattle and Cats, United States, 2024.” Emerging Infectious Diseases 30, no. 7: 1335–1343. https://doi.org/10.3201/eid3007.240508.
Byrd-Leotis, L., R. D. Cummings, and D. A. Steinhauer. 2017. “The Interplay Between the Host Receptor and Influenza Virus Hemagglutinin and Neuraminidase.” International Journal of Molecular Sciences 18: 1541. https://doi.org/10.3390/ijms18071541.
Caserta, L. C., E. A. Frye, S. L. Butt, et al. 2024. “From Birds to Mammals: Spillover of Highly Pathogenic Avian Influenza H5N1 Virus to Dairy Cattle Led to Efficient Intra- and Interspecies Transmission.” bioRxiv. https://doi.org/10.1101/2024.05.22.595317.
Center for Disease Contral and Prevention (CDC). 2024a. “CDC Confirms Human H5 Bird Flu Case in Missouri.” https://www.cdc.gov/media/releases/2024/s0906-birdflu-case-missouri.html.
Center for Disease Control and Prevention (CDC). 2024b. “Prevention and Antiviral Treatment of Bird Flu Viruses in People.” https://www.cdc.gov/bird-flu/prevention/index.html.
Chen, Y., G. Zhong, G. Wang, et al. 2010. “Dogs Are Highly Susceptible to H5N1 Avian Influenza Virus.” Virology 405: 15–19. https://doi.org/10.1016/j.virol.2010.05.024.
Chestakova, I. V., A. Van Der Linden, B. B. Martin, et al. 2023. “High Number of HPAI H5 Virus Infections and Antibodies in Wild Carnivores in the Netherlands, 2020–2022.” Emerging Microbes & Infections 12: 2270068. https://doi.org/10.1101/2023.05.12.540493.
Convention on the Conservation of Migratory Species (CMS), and Food and Agriculture Organization of the United Nations (FAO) Co-convened Scientific Task Force on Avian Influenza and Wild Birds. 2023. “Statement-July 2023.” https://www.fao.org/3/cc6936en/cc6936en.pdf.
Cronk, B. D., L. C. Caserta, M. Laverack, et al. 2023. “Infection and Tissue Distribution of Highly Pathogenic Avian Influenza A Type H5N1 (Clade 2.3.4.4b) in Red Fox Kits (Vulpes vulpes).” Emerging Microbes & Infections 12: 2249554. https://doi.org/10.1080/22221751.2023.2249554.
Domańska-Blicharz, K., E. Świȩtoń, A. Świątalska, et al. 2023. “Outbreak of Highly Pathogenic Avian Influenza A(H5N1) Clade 2.3.4.4b Virus in Cats, Poland, June to July 2023.” Eurosurveillance 28: 2300366. https://doi.org/10.2807/1560-7917.ES.2023.28.31.2300366.
Du, W., M. Dai, Z. Li, et al. 2018. “Substrate Binding by the Second Sialic Acid-Binding Site of Influenza A Virus N1 Neuraminidase Contributes to Enzymatic Activity.” Journal of Virology 92: e01243-18. https://doi.org/10.1128/JVI.01243-18.
Dufour, B., L. Plée, F. Moutou, et al. 2011. “A Qualitative Risk Assessment Methodology for Scientific Expert Panels.” Revue Scientifique et Technique (International Office of Epizootics) 30: 673–681. https://doi.org/10.20506/rst.30.3.2063.
Edenborough, K. M., S. Lowther, K. Laurie, et al. 2016. “Predicting Disease Severity and Viral Spread of H5N1 Influenza Virus in Ferrets in the Context of Natural Exposure Routes.” Journal of Virology 90: 1888–1897. https://doi.org/10.1128/jvi.01878-15.
European Centre for Disease Prevention and Control (ECDC). 2024a. “Public Health Situation for Avian Influenza A(H5) Viruses.” https://www.ecdc.europa.eu/en/infectious-disease-topics/z-disease-list/avian-influenza/threats-and-outbreaks/situation-ah5.
European Centre for Disease Prevention and Control (ECDC). 2024b. “Risk Assessment H5 Clade 2.3.4.4b Viruses.” https://www.ecdc.europa.eu/en/infectious-disease-topics/z-disease-list/avian-influenza/threats-and-outbreaks/risk-assessment-h5.
European Food Safety Authority (EFSA), European Centre for Disease Prevention and Control (ECDC), European Union Reference Laboratory for Avian Influenza (EURL), et al. 2023a. “Scientific Report: Avian Influenza Overview December 2022–March 2023.” EFSA Journal 21: 7917. https://doi.org/10.2903/j.efsa.2023.7917.
European Food Safety Authority (EFSA), European Centre for Disease Prevention and Control (ECDC), European Union Reference Laboratory for Avian Influenza (EURL), et al. 2023b. “Scientific Report: Avian Influenza Overview September–December 2023.” EFSA Journal 21: 8539–8562. https://doi.org/10.2903/j.efsa.2023.8539.
European Food Safety Authority (EFSA), European Centre for Disease Prevention and Control (ECDC), European Union Reference Laboratory for Avian Influenza (EURL), et al. 2024. “Scientific Report: Avian Influenza Overview December 2023–March 2024.” EFSA Journal 22: 8754–8769. https://doi.org/10.2903/j.efsa.2024.8754.
Food and Agriculture Organization of the United Nations (FAO). 2024. “Global Avian Influenza Viruses With Zoonotic Potential Situation Update, Bird Species Affected by H5Nx HPAI.” https://www.fao.org/animal-health/situation-updates/global-aiv-with-zoonotic-potential/bird-species-affected-by-h5nx-hpai/en.
Frymus, T., S. Belák, H. Egberink, et al. 2021. “Influenza Virus Infections in Cats.” Viruses 13: 1435. https://doi.org/10.3390/v13081435.
Gamarra-Toledo, V., P. I. Plaza, R. Gutiérrez, et al. 2023. “Mass Mortality of Marine Mammals Associated to Highly Pathogenic Influenza Virus (H5N1) in South America.” Emerging Infectious Diseases 29: 2553–2556. https://doi.org/10.3201/eid2912.230192.
Garg, S., C. Reed, C. T. Davis, et al. 2024. “Outbreak of Highly Pathogenic Avian Influenza A(H5N1) Viruses in U.S. Dairy Cattle and Detection of Two Human Cases—United States, 2024.” MMWR. Morbidity and Mortality Weekly Report 73, no. 21: 501–505. https://doi.org/10.15585/mmwr.mm7321e1.
Giese, M., T. C. Harder, J. P. Teifke, et al. 2008. “Experimental Infection and Natural Contact Exposure of Dogs With Avian Influenza Virus (H5N1).” Emerging Infectious Diseases 14: 308–310. https://doi.org/10.3201/eid1402.070864.
Govorkova, E. A., J. E. Rehg, S. Krauss, et al. 2005. “Lethality to Ferrets of H5N1 Influenza Viruses Isolated From Humans and Poultry in 2004.” Journal of Virology 79: 2191–2198. https://doi.org/10.1128/jvi.79.4.2191-2198.2005.
Guan, L., A. J. Eisfeld, D. Pattinson, et al. 2024. “Cow's Milk Containing Avian Influenza A(H5N1) Virus—Heat Inactivation and Infectivity in Mice.” New England Journal of Medicine 391, no. 1: 87–90. https://doi.org/10.1056/NEJMc2405495.
Halwe, N. J., K. Cool, A. Breithaupt, et al. 2024. “Outcome of H5N1 Clade 2.3.4.4b Virus Infection in Calves and Lactating Cows.” bioRxiv. https://doi.org/10.1101/2024.08.09.607272.
Hu, T., H. Zhao, Y. Zhang, et al. 2016. “Fatal Influenza A(H5N1) Virus Infection in Zoo-Housed Tigers in Yunnan Province, China.” Scientific Reports 6: 25845. https://doi.org/10.1038/srep25845.
Imperia, E., L. Bazzani, F. Scarpa, et al. 2023. “Avian Influenza: Could the H5N1 Virus Be a Potential Next Threat?” Microbiology Research 14: 635–645. https://doi.org/10.3390/microbiolres14020045.
Kalthoff, D., B. Hoffmann, T. Harder, M. Durban, and M. Beer. 2008. “Experimental Infection of Cattle With Highly Pathogenic Avian Influenza Virus (H5N1).” Emerging Infectious Diseases 14, no. 7: 1132–1134. https://doi.org/10.3201/eid1407.071468.
Kaplan, B. S., M. K. Torchetti, K. M. Lager, R. J. Webby, and A. L. Vincent. 2017. “Absence of Clinical Disease and Contact Transmission of HPAI H5NX Clade 2.3.4.4 From North America in Experimentally Infected Pigs.” Influenza and Other Respiratory Viruses 11: 464–470. https://doi.org/10.1111/irv.12463.
Kareinen, L., N. Tammiranta, A. Kauppinen, et al. 2024. “Highly Pathogenic Avian Influenza A(H5N1) Virus Infections on Fur Farms Connected to Mass Mortalities of Black-Headed Gulls, Finland, July to October 2023.” European Communicable Disease Bulletin 29, no. 25: 2400063. https://doi.org/10.2807/1560-7917.ES.2024.29.25.2400063.
Kimble, B., G. R. Nieto, and D. R. Perez. 2010. “Characterization of Influenza Virus Sialic Acid Receptors in Minor Poultry Species.” Virology Journal 7: 365. https://doi.org/10.1186/1743-422X-7-365.
Kintz, E., E. Pegg, W. Perry, and W. Trzaska. 2023. “A Qualitative Assessment of the Risk of Acquiring Avian Influenza From Poultry and Game Bird Meat Poultry Products.” https://www.food.gov.uk/research/risk-assessment-of-acquiring-avian-influenza-from-poultry-products-executive-summary.
Kuiken, T., G. Rimmelzwaan, D. Van Riel, et al. 2004. “Avian H5N1 Influenza in Cats.” Science 306: 241. https://doi.org/10.1126/science.1102287.
Le Sage, V., A. J. Campbell, D. S. Reed, W. P. Duprex, and S. S. Lakdawala. 2024. “Influenza H5N1 and H1N1 Viruses Remain Infectious in Unpasteurized Milk on Milking Machinery Surfaces.” medRxiv. https://doi.org/10.1101/2024.05.22.24307745.
Lee, C. W., and Y. M. Saif. 2009. “Avian Influenza Virus.” Comparative Immunology, Microbiology and Infectious Diseases 32: 301–310. https://doi.org/10.1016/j.cimid.2008.01.007.
Leguia, M., A. Garcia-Glaessner, B. Muñoz-Saavedra, et al. 2023. “Highly Pathogenic Avian Influenza A(H5N1) in Marine Mammals and Seabirds in Peru.” Nature Communications 14: 5489. https://doi.org/10.1038/s41467-023-41182-0.
Lindh, E., H. Lounela, N. Ikonen, et al. 2023. “Highly Pathogenic Avian Influenza A(H5N1) Virus Infection on Multiple Fur Farms in the South and Central Ostrobothnia Regions of Finland, July 2023.” Eurosurveillance 28: 2300400. https://doi.org/10.2807/1560-7917.ES.2023.28.31.2300400.
Lipatov, A. S., Y. K. Kwon, M. J. Pantin-Jackwood, and D. E. Swayne. 2009. “Pathogenesis of H5N1 Influenza Virus Infections in Mice and Ferret Models Differs According to Respiratory Tract or Digestive System Exposure.” Journal of Infectious Diseases 199: 717–725. https://doi.org/10.1086/596740.
Logeot, M., A. Mauroy, E. Thiry, et al. 2022. “Risk Assessment of SARS-CoV-2 Infection in Free-Ranging Wild Animals in Belgium.” Transboundary and Emerging Diseases 69: 986–996. https://doi.org/10.1111/tbed.14131.
Lowen, A. C. 2017. “Constraints, Drivers, and Implications of Influenza A Virus Reassortment.” Annual Review of Virology 4: 105–121. https://doi.org/10.1146/annurev-virology-101416-041726.
Ma, W., R. E. Kahn, and J. A. Richt. 2008. “The Pig as a Mixing Vessel for Influenza Viruses: Human and Veterinary Implications.” Journal of Molecular and Genetic Medicine 27: 158–166. https://doi.org/10.4172/1747-0862.1000028.
Maas, R., M. Tacken, L. Ruuls, G. Koch, E. Van Rooij, and N. Stockhofe-Zurwieden. 2007. “Avian Influenza (H5N1) Susceptibility and Receptors in Dogs.” Emerging Infectious Diseases 13: 1219–1221. https://doi.org/10.3201/eid1308.070393.
Mänz, B., D. Dornfeld, V. Götz, et al. 2013. “Pandemic Influenza A Viruses Escape From Restriction by Human MxA Through Adaptive Mutations in the Nucleoprotein.” PLoS Pathogens 9: e1003279. https://doi.org/10.1371/journal.ppat.1003279.
Mänz, B., M. Schwemmle, and L. Brunotte. 2013. “Adaptation of Avian Influenza A Virus Polymerase in Mammals to Overcome the Host Species Barrier.” Journal of Virology 87: 7200–7209. https://doi.org/10.1128/jvi.00980-13.
Moreno, A., F. Bonfante, A. Bortolami, et al. 2023. “Asymptomatic Infection With Clade 2.3.4.4b Highly Pathogenic Avian Influenza A(H5N1) in Carnivore Pets, Italy, April 2023.” Eurosurveillance 28: 2300441. https://doi.org/10.2807/1560-7917.ES.2023.28.35.2300441.
Nguyen, T.-Q., C. Hutter, A. Markin, et al. 2024. “Emergence and Interstate Spread of Highly Pathogenic Avian Influenza A(H5N1) in Dairy Cattle.” bioRxiv. https://doi.org/10.1101/2024.05.01.591751.
Nicholls, J. M., R. W. Y. Chan, R. J. Russel, G. M. Air, and J. S. M. Peiris. 2008. “Evolving Complexities of Influenza Virus and Its Receptors.” Trends in Microbiology 16: 149–157. https://doi.org/10.1016/j.tim.2008.01.008.
Pan American Health Organization (PAHO). 2023. “Avian Influenza A (H5N1) Risk Assessment: Implications for the Region of the Americas.” https://www.paho.org/en/documents/risk-assessment-public-health-related-outbreaks-caused-highly-pathogenic-avian-influenza.
Pinto, R. M., S. Bakshi, S. Lytras, et al. 2023. “BTN3A3 Evasion Promotes the Zoonotic Potential of Influenza A Viruses.” Nature 619, no. 7969: 338–347. https://doi.org/10.1038/s41586-023-06261-8.
Plaza, P. I., V. Gamarra-Toledo, J. Euguí, and S. A. Lambertucci. 2024. “Recent Changes in Patterns of Mammal Infection With Highly Pathogenic Avian Influenza A(H5N1) Virus Worldwide.” Emerging Infectious Diseases 30, no. 3: 444–452. https://doi.org/10.3201/eid3003.231098.
Pulit-Penaloza, J. A., N. Brock, J. A. Belser, et al. 2024. “Highly Pathogenic Avian Influenza A(H5N1) Virus of Clade 2.3.4.4b Isolated From a Human Case in Chile Causes Fatal Disease and Transmits Between co-Housed Ferrets.” Emerging Microbes & Infections 13, no. 1: 2332667. https://doi.org/10.1080/22221751.2024.2332667.
Puryear, W., K. Sawatzki, N. Hill, et al. 2023. “Highly Pathogenic Avian Influenza A(H5N1) Virus Outbreak in New England Seals, United States.” Emerging Infectious Diseases 29: 786–791. https://doi.org/10.3201/eid2904.221538.
Puryear, W. B., M. Keogh, N. Hill, et al. 2016. “Prevalence of Influenza A Virus in Live-Captured North Atlantic Gray Seals: A Possible Wild Reservoir.” Emerging Microbes & Infections 5: e81. https://doi.org/10.1038/emi.2016.77.
Rabalski, L., A. Milewska, A. Pohlmann, et al. 2023. “Emergence and Potential Transmission Route of Avian Influenza A(H5N1) Virus in Domestic Cats in Poland, June 2023.” Eurosurveillance 28: 2300390. https://doi.org/10.2807/1560-7917.ES.2023.28.31.2300390.
Reperant, L. A., G. Van Amerongen, M. W. G. Van De Bildt, et al. 2008. “Highly Pathogenic Avian Influenza Virus (H5N1) Infection in Red Foxes Fed Infected Bird Carcasses.” Emerging Infectious Diseases 14: 1835–1841. https://doi.org/10.3201/eid1412.080470.
Rimmelzwaan, G. F., D. Van Riel, M. Baars, et al. 2006. “Influenza A Virus (H5N1) Infection in Cats Causes Systemic Disease With Potential Novel Routes of Virus Spread Within and Between Hosts.” American Journal of Pathology 168: 176–183. https://doi.org/10.2353/ajpath.2006.050466.
Rimondi, A., R. Vanstreels, V. Olivera, A. Donini, M. Lauriente, and M. M. Uhart. 2024. “Highly Pathogenic Avian Influenza A(H5N1) Viruses From Multispecies Outbreak, Argentina, August 2023.” Emerging Infectious Diseases 30, no. 4: 812–814. https://doi.org/10.3201/eid3004.231725.
Rivetti, A. V., D. Reischak, C. H. S. de Oliveira, et al. 2024. “Phylodynamics of Avian Influenza A(H5N1) Viruses From Outbreaks in Brazil.” Virus Research 347: 199415. https://doi.org/10.1016/j.virusres.2024.199415.
Rosone, F., F. Bonfante, M. G. Sala, et al. 2023. “Seroconversion of a Swine Herd in a Free-Range Rural Multi-Species Farm Against HPAI H5N1 2.3.4.4b Clade Virus.” Microorganisms 11: 1162. https://doi.org/10.3390/microorganisms11051162.
Scharff-Olsen, C. H., A. Galatius, J. Teilmann, et al. 2019. “Diet of Seals in the Baltic Sea Region: A Synthesis of Published and New Data From 1968 to 2013.” ICES Journal of Marine Science 76: 284–297. https://doi.org/10.1093/icesjms/fsy159.
Schülein, A., M. Ritzmann, J. Christian, K. Schneider, and A. Neubauer-Juric. 2021. “Exposure of Wild Boar to Influenza A Viruses in Bavaria: Analysis of Seroprevalences and Antibody Subtype Specificity Before and After the Panzootic of Highly Pathogenic Avian Influenza Viruses A(H5N8).” Zoonoses and Public Health 68: 503–515. https://doi.org/10.1111/zph.12841.
Sciensano Institute, NRL Avian Influenza and Coordination of Veterinary Activities/Veterinary Epidemiology Service. 2024. https://moriskin.sciensano.be/shiny/avianinfluenza/.
Shelton, H., G. Ayora-Talavera, J. Ren, et al. 2011. “Receptor Binding Profiles of Avian Influenza Virus Hemagglutinin Subtypes on Human Cells as a Predictor of Pandemic Potential.” Journal of Virology 85: 1875–1880. https://doi.org/10.1128/jvi.01822-10.
Shinya, K., M. Ebina, S. Yamada, M. Ono, N. Kasai, and Y. Kawaoka. 2006. “Avian Flu: Influenza Virus Receptors in the Human Airway.” Nature 440: 435–436. https://doi.org/10.1038/440435a.
Shinya, K., A. Makino, H. Tanaka, et al. 2011. “Systemic Dissemination of H5N1 Influenza A Viruses in Ferrets and Hamsters After Direct Intragastric Inoculation.” Journal of Virology 85: 4673–4678. https://doi.org/10.1128/jvi.00148-11.
Songserm, T., A. Amonsin, R. Jam-On, et al. 2006. “Fatal Avian Influenza A H5N1 in a Dog.” Emerging Infectious Diseases 12: 1744–1747. https://doi.org/10.3201/eid1211.060542.
Spackman, E., N. Anderson, S. Walker, et al. 2024. “Inactivation of Highly Pathogenic Avian Influenza Virus With High Temperature Short Time Continuous Flow Pasteurization and Virus Detection in Bulk Milk Tanks.” medRxiv. https://doi.org/10.1101/2024.07.01.24309766.
Sreenivasan, C. C., F. Li, and D. Wang. 2024. “Cross-Species Transmission of Highly Pathogenic Avian Influenza (HPAI) H5N1 Virus in the U.S. Dairy Cattle: A Comprehensive Review.” Preprints.org. https://doi.org/10.20944/preprints202405.2137.v1.
Sreenivasan, C. C., M. Thomas, R. S. Kaushik, D. Wang, and F. Li. 2019. “Influenza A in Bovine Species: A Narrative Literature Review.” Viruses 11, no. 6: 561. https://doi.org/10.3390/v11060561.
Suttie, A., Y. M. Deng, A. R. Greenhill, P. Dussart, P. F. Horwood, and E. A. Karlsson. 2019. “Inventory of Molecular Markers Affecting Biological Characteristics of Avian Influenza A Viruses.” Virus Genes 55: 739–768. https://doi.org/10.1007/s11262-019-01700-z.
Thanawongnuwech, R., A. Amonsin, R. Tantilertcharoen, et al. 2005. “Probable Tiger-to-Tiger Transmission of Avian Influenza H5N1.” Emerging Infectious Diseases 11: 976. https://doi.org/10.3201/eid1105.050007.
Thiry, E., A. Zicola, D. Addie, et al. 2007. “Highly Pathogenic Avian Influenza H5N1 Virus in Cats and Other Carnivores.” Veterinary Microbiology 122: 25–31. https://doi.org/10.1016/j.vetmic.2006.12.021.
Tomás, G., A. Marandino, Y. Panzera, et al. 2024. “Highly Pathogenic Avian Influenza H5N1 Virus Infections in Pinnipeds and Seabirds in Uruguay: Implications for Bird-Mammal Transmission in South America.” Virus Evolution 10, no. 1: veae031. https://doi.org/10.1093/ve/veae031.
Uhart, M., R. E. T. Vanstreels, M. I. Nelson, et al. 2024. “Massive Outbreak of Influenza A H5N1 in Elephant Seals at Península Valdés, Argentina: Increased Evidence for Mammal-to-Mammal Transmission.” bioRxiv. https://doi.org/10.1101/2024.05.31.596774.
Vreman, S., M. Kik, E. Germeraad, et al. 2023. “Zoonotic Mutation of Highly Pathogenic Avian Influenza H5N1 Virus Identified in the Brain of Multiple Wild Carnivore Species.” Pathogens 12: 168. https://doi.org/10.3390/pathogens12020168.
Wan, H., and D. R. Perez. 2006. “Quail Carry Sialic Acid Receptors Compatible With Binding of Avian and Human Influenza Viruses.” Virology 15: 278–286. https://doi.org/10.1016/j.virol.2005.10.035.
WHO/OIE/FAO. 2012. “Continued Evolution of Highly Pathogenic Avian Influenza A(H5N1): Updated Nomenclature.” Influenza and Other Respiratory Viruses 6, no. 1: 1–5. https://doi.org/10.1111/j.1750-2659.2011.00298.x.
World Animal Health Information System (WAHIS). 2024. “Events Management.” https://wahis.woah.org/#/event-management.
World Health Organization (WHO). 2023. “Influenza A(H5N1) in Cats—Poland.” https://www.who.int/emergencies/disease-outbreak-news/item/2023-DON476.
World Organization for Animal Health (WOAH). 2024. “Avian Influenza.” https://www.woah.org/en/disease/avian-influenza/.
World Health Organization (WHO) Western Pacific Region. 2024. “Avian Influenza Weekly Update Number 970.” https://cdn.who.int/media/docs/default-source/wpro---documents/emergency/surveillance/avian-influenza/ai_20241025.pdf?sfvrsn=5f006f99_143.
World Health Organization (WHO). 2024. “Cumulative Number of Confirmed Human Cases for Avian Influenza A(H5N1) Reported to WHO, 2003–2024.” https://cdn.who.int/media/docs/default-source/influenza/h5n1-human-case-cumulative-table/2024_july_tableh5n1226acba9-e195-4ecf-8ef7-f00a93a06420.pdf?sfvrsn=5bb6bb97_3&download=true.
