{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,30]],"date-time":"2026-07-30T14:19:29Z","timestamp":1785421169386,"version":"3.56.0"},"reference-count":50,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2026,7,27]],"date-time":"2026-07-27T00:00:00Z","timestamp":1785110400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Ministry of Science and Higher Education of the Republic of Kazakhstan","award":["AP23489183"],"award-info":[{"award-number":["AP23489183"]}]},{"award":["AP23489183"],"award-info":[{"award-number":["AP23489183"]}],"id":[{"id":"https:\/\/ror.org\/05tyne317","id-type":"ROR","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>Highly pathogenic avian influenza (HPAI) is a transboundary disease of birds with zoonotic potential. Since 2021, H5 HPAI virus variants have spread globally, with migratory waterfowl playing a key role in transcontinental dissemination. Kazakhstan lies at the intersection of major flyways, creating a persistent risk of virus introduction into domestic poultry. While HPAI risk in wild birds has been explored in Kazakhstan, the spatial risk for poultry has remained underassessed. Here, we present a risk map for HPAI in poultry across 174 administrative districts of Kazakhstan, using a multi-criteria decision analysis (TOPSIS) that integrates five quantitative risk indicators that relate to wild bird habitat, virus survival in the environment and poultry farm census. The obtained district-level risk index agreed well with historical outbreak data (2005\u20132025), with an area under the receiver operating characteristic (ROC) curve of 0.899 (95% CI: 0.846\u20130.952). Most districts (56%) were at negligible risk, whereas medium- and high-risk clusters occurred in the north, central, and southern regions, and near the Caspian Sea. These findings provide an operational, spatially explicit tool for targeting surveillance and biosecurity measures to high-risk areas, ultimately helping to mitigate the impact of one of the most devastating transboundary poultry diseases in Central Asia.<\/jats:p>","DOI":"10.3390\/pathogens15080796","type":"journal-article","created":{"date-parts":[[2026,7,27]],"date-time":"2026-07-27T16:11:56Z","timestamp":1785168716000},"page":"796","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["District-Level Risk Mapping of Highly Pathogenic Avian Influenza in Poultry in Kazakhstan Using a Multi-Criteria Decision Model"],"prefix":"10.3390","volume":"15","author":[{"given":"Aizada A.","family":"Mukhanbetkaliyeva","sequence":"first","affiliation":[{"name":"Institute of Animal Science and Veterinary, Saken Seifullin Kazakh Agrotechnical University, Astana 010011, Kazakhstan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Irene","family":"Iglesias Martin","sequence":"additional","affiliation":[{"name":"Centro de Investigaci\u00f3n en Sanidad Animal (CISA), Instituto Nacional de Investigaci\u00f3n y Tecnolog\u00eda Agraria y Alimentaria (INIA), Consejo Superior de Investigaciones Cient\u00edficas (CSIC), 28130 Madrid, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7378-3531","authenticated-orcid":false,"given":"Fedor I.","family":"Korennoy","sequence":"additional","affiliation":[{"name":"Federal Centre for Animal Health (FGBI ARRIAH), Vladimir 600901, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alimzhan S.","family":"Kadyrov","sequence":"additional","affiliation":[{"name":"Institute of Animal Science and Veterinary, Saken Seifullin Kazakh Agrotechnical University, Astana 010011, Kazakhstan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yersyn Y.","family":"Mukhanbetkaliyev","sequence":"additional","affiliation":[{"name":"Institute of Animal Science and Veterinary, Saken Seifullin Kazakh Agrotechnical University, Astana 010011, Kazakhstan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2093-8667","authenticated-orcid":false,"given":"Saidulla I.","family":"Ruzmatov","sequence":"additional","affiliation":[{"name":"Institute of Animal Science and Veterinary, Saken Seifullin Kazakh Agrotechnical University, Astana 010011, Kazakhstan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8360-1527","authenticated-orcid":false,"given":"Asem Zh.","family":"Abenova","sequence":"additional","affiliation":[{"name":"Institute of Animal Science and Veterinary, Saken Seifullin Kazakh Agrotechnical University, Astana 010011, Kazakhstan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Temirlan G.","family":"Bakishev","sequence":"additional","affiliation":[{"name":"Institute of Animal Science and Veterinary, Saken Seifullin Kazakh Agrotechnical University, Astana 010011, Kazakhstan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andres M.","family":"Perez","sequence":"additional","affiliation":[{"name":"Center for Animal Health and Food Safety, College of Veterinary Medicine, University of Minnesota, St. Paul Campus, St. Paul, MN 55108, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3707-3767","authenticated-orcid":false,"given":"Sarsenbay K.","family":"Abdrakhmanov","sequence":"additional","affiliation":[{"name":"Institute of Animal Science and Veterinary, Saken Seifullin Kazakh Agrotechnical University, Astana 010011, Kazakhstan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,7,27]]},"reference":[{"key":"ref_1","unstructured":"Alexander, D.J. (2009). Avian Influenza and Newcastle Disease: A Field and Laboratory Guide, Springer."},{"key":"ref_2","first-page":"36","article-title":"Highly pathogenic avian influenza: A new pandemic threat and possibilities to resist it","volume":"12","author":"Onischenko","year":"2006","journal-title":"Vestn. Ross. Akad. Meditsinskikh Nauk."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"De Bruin, A.C.M., Funk, M., Spronken, M.I., Gultyaev, A.P., Fouchier, R.A.M., and Richard, M. (2022). Hemagglutinin Subtype Specificity and Mechanisms of Highly Pathogenic Avian Influenza Virus Genesis. Viruses, 14.","DOI":"10.3390\/v14071566"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"2155072","DOI":"10.1080\/22221751.2022.2155072","article-title":"Alarming situation of emerging H5 and H7 avian influenza and effective control strategies","volume":"12","author":"Shi","year":"2023","journal-title":"Emerg. Microbes Infect."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Guo, F., Li, Y., Yu, S., Liu, L., Luo, T., Pu, Z., Xiang, D., Shen, X., Irwin, D.M., and Liao, M. (2019). Adaptive evolution of human-isolated H5Nx avian influenza a virus. Front. Microbiol., 10.","DOI":"10.3389\/fmicb.2019.01328"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1335","DOI":"10.3201\/eid3007.240508","article-title":"Highly Pathogenic Avian Influenza A(H5N1) Clade 2.3.4.4b Virus Infection in Domestic Dairy Cattle and Cats, United States, 2024","volume":"30","author":"Burrough","year":"2024","journal-title":"Emerg. Infect. Dis."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"533","DOI":"10.1093\/infdis\/jiae379","article-title":"An Update on Highly Pathogenic Avian Influenza A(H5N1) Virus, Clade 2.3.4.4b","volume":"230","author":"Webby","year":"2024","journal-title":"J. Infect. Dis."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"e02209-24","DOI":"10.1128\/jvi.02209-24","article-title":"Highly pathogenic avian influenza H5N1: History, current situation, and outlook","volume":"99","author":"Krammer","year":"2025","journal-title":"J. Virol."},{"key":"ref_9","unstructured":"The World Organization for Animal Health (WOAH) (2026, May 25). Avian Influenza. Available online: https:\/\/www.woah.org\/en\/disease\/avian-influenza\/."},{"key":"ref_10","unstructured":"World Health Organization (2026, June 05). Assessment of Risk Associated with Recent Influenza A(H5N1) Clade 2.3.4.4b Viruses. Available online: https:\/\/www.who.int\/publications\/m\/item\/assessment-of-risk-associated-with-recent-influenza-a(h5n1)-clade-2.3.4.4b-viruses."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Islam, A., Hossain, M.E., Amin, E., Islam, S., Islam, M., Sayeed, M.A., Hasan, M.M., Miah, M., Hassan, M.M., and Rahman, M.Z. (2023). Epidemiology and Phylodynamics of Multiple Clades of H5N1 Circulating in Domestic Duck Farms in Different Production Systems in Bangladesh. Front. Public Health, 11.","DOI":"10.3389\/fpubh.2023.1168613"},{"key":"ref_12","unstructured":"(2026, June 09). Updated Joint FAO\/WHO\/WOAH Public Health Assessment of Recent High Pathogenicity Avian Influenza A(H5) Virus Events in Animals and People. Available online: https:\/\/www.woah.org\/app\/uploads\/2026\/05\/2026-05-18-fao-woah-who-h5-assessment.pdf."},{"key":"ref_13","unstructured":"Organizaci\u00f3n Mundial de Sanidad Animal (2023). Distribution of HPAI New Outbreaks in Poultry, and Corresponding Subtypes, OMSA. Available online: https:\/\/www.woah.org\/app\/uploads\/2023\/02\/hpai-situation-report-20230216.pdf."},{"key":"ref_14","unstructured":"Organizaci\u00f3n Mundial de Sanidad Animal (2023). Influenza Aviar\u2014WOAH\u2014Organizaci\u00f3n Mundial de Sanidad Animal, OMSA. Available online: https:\/\/www.woah.org\/en\/disease\/avian-influenza\/#ui-id-2."},{"key":"ref_15","first-page":"2300001","article-title":"Highly pathogenic avian influenza A(H5N1) virus infection in farmed minks, Spain, October 2022","volume":"28","author":"Monne","year":"2023","journal-title":"Eurosurveillance"},{"key":"ref_16","unstructured":"United Nations (2026, May 28). Avian Flu Reported in 108 Countries Across Five Continents, Says UN Health Agency. Available online: https:\/\/news.un.org\/en\/story\/2024\/12\/1158286."},{"key":"ref_17","first-page":"17","article-title":"Review of the Epizootic and Epidemic Situation regarding Highly Pathogenic Avian Influenza in Russia and Globally in 2025","volume":"1","author":"Enikeeva","year":"2026","journal-title":"Probl. Part. Danger. Infect."},{"key":"ref_18","unstructured":"Nagy, S., and Langendoen, T. (2020). Flyway Trend Analyses Based on Data from the African-Eurasian Waterbird Census from the Period of 1967\u20132018, Wetlands International. Available online: http:\/\/iwc.wetlands.org\/index.php\/aewatrends8."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"65","DOI":"10.4081\/gh.2009.211","article-title":"Spatio-temporal dynamics of global H5N1 outbreaks match bird migration patterns","volume":"4","author":"Si","year":"2009","journal-title":"Geospat. Health"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1007\/s00705-016-3076-4","article-title":"Monitoring of Influenza A Viruses in Wild Bird Populations in Kazakhstan in 2002\u20132009","volume":"162","author":"Kydyrmanov","year":"2017","journal-title":"Arch. Virol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1017\/S0959270908000087","article-title":"Waterbird population estimates for a key staging site in Kazakhstan: A contribution to wetland conservation on the Central Asian flyway","volume":"18","author":"Schielzeth","year":"2008","journal-title":"Bird Conserv. Int."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1016\/j.sste.2012.01.002","article-title":"Risk factor modelling of the spatio-temporal patterns of highly pathogenic avian influenza (HPAIV) H5N1: A review","volume":"3","author":"Gilbert","year":"2012","journal-title":"Spat. Spatiotemporal Epidemiol."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Si, Y., de Boer, W.F., and Gong, P. (2013). Different Environmental Drivers of Highly Pathogenic Avian Influenza H5N1 Outbreaks in Poultry and Wild Birds. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0053362"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"76","DOI":"10.1111\/tbed.13595","article-title":"Association of Wild Bird Densities around Poultry Farms with the Risk of Highly Pathogenic Avian Influenza Virus Subtype H5N8 Outbreaks in the Netherlands, 2016","volume":"68","author":"Velkers","year":"2021","journal-title":"Transbound. Emerg. Dis."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Sultankulova, K., Argimbayeva, T., Aubakir, N., Bopi, A., Omarova, Z., Melisbek, A., Karamendin, K., Kydyrmanov, A., Chervyakova, O., and Kerimbayev, A. (2024). Reassortants of the Highly Pathogenic Influenza Virus A\/H5N1 Causing Mass Swan Mortality in Kazakhstan from 2023 to 2024. Animals, 14.","DOI":"10.3390\/ani14223211"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Kydyrmanov, A., Karamendin, K., Kassymbekov, Y., Daulbayeva, K., Sabyrzhan, T., Khan, Y., Nuralibekov, S., Baikara, B., and Fereidouni, S. (2024). Mass Mortality in Terns and Gulls Associated with Highly Pathogenic Avian Influenza Viruses in Caspian Sea, Kazakhstan. Viruses, 16.","DOI":"10.3390\/v16111661"},{"key":"ref_27","unstructured":"Sputnik Kazakhstan (2026, May 29). Avian Flu in Kazakhstan: About 2 Million Birds Died in 2020. Available online: https:\/\/ru.sputnik.kz\/20210106\/ptichiy-gripp-v-kazakhstan-okolo-2-millionov-ptits-pogiblo-v-2020-godu-15935875.html."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"e13038","DOI":"10.7717\/peerj.13038","article-title":"Highly Pathogenic Avian Influenza Virus of the A\/H5N8 Subtype, Clade 2.3.4.4b, Caused Outbreaks in Kazakhstan in 2020","volume":"10","author":"Amirgazin","year":"2022","journal-title":"PeerJ"},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Abenova, A., Mukhanbetkaliyev, Y.Y., Kadyrov, A., Sytnik, I.I., Shevtsov, A., Korennoy, F.I., Martin, I.I., Perez, A.M., and Abdrakhmanov, S.K. (2025). Environmental Suitability of Kazakhstan to Highly Pathogenic Avian Influenza Using Data on Eurasian Outbreaks, 2020\u20132024. Viruses, 17.","DOI":"10.20944\/preprints202501.2135.v1"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"76","DOI":"10.51585\/gjvr.2025.3.0149","article-title":"Risk assessment of highly pathogenic Avian Influenza (HPAI) in wild bird species in Kazakhstan","volume":"5","author":"Iglesias","year":"2025","journal-title":"Ger. J. Vet. Res."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Bekshin, Z., Temirbekova, A., Nurbekova, Z., Amirkhanova, N., Satenova, A., Askarov, A., Zakarya, K., Abduraimov, Y., and Rsaliyev, A. (2025). Epidemiology, Virology, and Control of Highly Pathogenic Avian Influenza in Kazakhstan. Pathogens, 14.","DOI":"10.3390\/pathogens14111084"},{"key":"ref_32","unstructured":"(2026, June 20). Annual Reporting Meeting of the Members of the Union of Poultry Farmers of Kazakhstan. Available online: https:\/\/ptica.kz\/news\/otchetnoe-godovoe-sobranie-chlenov-ojufl-sojuz-pticevodov-kazahstana?lang=en."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1080\/13658810600661508","article-title":"GIS-Based Multicriteria Decision Analysis: A Survey of the Literature","volume":"20","author":"Malczewski","year":"2006","journal-title":"Int. J. Geogr. Inf. Sci."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"2282","DOI":"10.1016\/j.biocon.2009.05.006","article-title":"EBird: A citizen-based bird observation network in the biological sciences","volume":"142","author":"Sullivan","year":"2009","journal-title":"Biol. Conserv."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Central Veterinary Institute, and Wageningen University (2017). Risk factors of primary introduction of highly pathogenic and low pathogenic avian influenza virus into European poultry holdings, considering at least material contaminated by wild birds and contact with wild birds. EFSA Support. Publ., 14, 1282.","DOI":"10.2903\/sp.efsa.2017.EN-1282"},{"key":"ref_36","unstructured":"(2026, May 12). Kazakhstan Waterways (OpenStreetMap Export). Available online: https:\/\/data.humdata.org\/dataset\/hotosm_kaz_waterways."},{"key":"ref_37","unstructured":"(2026, May 12). JRC Global Surface Water Mapping Layers, v1.4. Available online: https:\/\/developers.google.com\/earth-engine\/datasets\/catalog\/JRC_GSW1_4_GlobalSurfaceWater."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"2910","DOI":"10.1128\/AEM.03790-13","article-title":"Abiotic factors affecting the persistence of avian influenza virus in surface waters of waterfowl habitats","volume":"80","author":"Keeler","year":"2014","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_39","unstructured":"(2026, July 20). ERA5-Land Daily Aggregated\u2014ECMWF Climate Reanalysis. Available online: https:\/\/developers.google.com\/earth-engine\/datasets\/catalog\/ECMWF_ERA5_LAND_DAILY_AGGR."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"31","DOI":"10.51585\/gjvr.2024.4.0107","article-title":"DiFLUsion: A Novel Space-Time Alert System for HPAI","volume":"4","author":"Iglesias","year":"2024","journal-title":"Ger. J. Vet. Res."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"3160","DOI":"10.1111\/tbed.14722","article-title":"Two Major Epidemics of Highly Pathogenic Avian Influenza Virus H5N8 and H5N1 in Domestic Poultry in France, 2020\u20132022","volume":"69","author":"Lambert","year":"2022","journal-title":"Transbound. Emerg. Dis."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"EFSA (European Food Safety Authority), ECDC (European Centre for Disease Prevention and Control), Alexakis, L., Buczkowski, H., Ducatez, M., Fusaro, A., Gonzales, J.L., Kuiken, T., and St\u00e5hl, K. (2025). Avian Influenza Overview September\u2013December 2024. EFSA J., 23, 9204.","DOI":"10.2903\/j.efsa.2025.9204"},{"key":"ref_43","unstructured":"Bureau of National Statistics of the Agency for Strategic Planning and Reforms of the Republic of Kazakhstan (2026, June 20). Animal Husbandry of the Republic of Kazakhstan: 2025; Bureau of National Statistics: Astana, Kazakhstan, 2025, Available online: https:\/\/stat.gov.kz\/."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Hwang, C.L., and Yoon, K. (1981). Multiple Attribute Decision Making: Methods and Applications. Lecture Notes in Economics and Mathematical Systems, Springer.","DOI":"10.1007\/978-3-642-48318-9"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1016\/j.prevetmed.2019.02.006","article-title":"A Modified TOPSIS (Technique for Order of Preference by Similarity to Ideal Solution) Applied to Choosing Appropriate Selection Methods in Ongoing Surveillance for Avian Influenza in Canada","volume":"165","author":"Christensen","year":"2019","journal-title":"Prev. Vet. Med."},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Saaty, T.L. (1980). The Analytic Hierarchy Process: Planning, Priority Setting, Resource Allocation, McGraw-Hill.","DOI":"10.21236\/ADA214804"},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Robin, X., Turck, N., Hainard, A., Tiberti, N., Lisacek, F., Sanchez, J.-C., and M\u00fcller, M. (2011). PROC: An Open-Source Package for R and S+ to Analyze and Compare ROC Curves. BMC Bioinform., 12.","DOI":"10.1186\/1471-2105-12-77"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1002\/1097-0142(1950)3:1<32::AID-CNCR2820030106>3.0.CO;2-3","article-title":"Index for rating diagnostic tests","volume":"3","author":"Youden","year":"1950","journal-title":"Cancer"},{"key":"ref_49","first-page":"186","article-title":"The Data Model Concept in Statistical Mapping","volume":"7","author":"Jenks","year":"1967","journal-title":"Int. Yearb. Cartogr."},{"key":"ref_50","unstructured":"(2026, July 22). What Is the Jenks Optimization Method? (ArcGIS Knowledge Base). Available online: https:\/\/support.esri.com\/en-us\/knowledge-base\/what-is-the-jenks-optimization-method-1462479759617-000006743."}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/15\/8\/796\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,7,30]],"date-time":"2026-07-30T04:21:11Z","timestamp":1785385271000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/15\/8\/796"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,7,27]]},"references-count":50,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2026,8]]}},"alternative-id":["pathogens15080796"],"URL":"https:\/\/doi.org\/10.3390\/pathogens15080796","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,7,27]]}}}