{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T08:52:08Z","timestamp":1790671928498,"version":"4.1.0"},"reference-count":51,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2021,6,24]],"date-time":"2021-06-24T00:00:00Z","timestamp":1624492800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Vet. Sci."],"abstract":"<jats:p>The Yamal Peninsula in the Russian Federation experienced a massive outbreak of anthrax in reindeer (<jats:italic>Rangifer tarandus<\/jats:italic>) in July\u2013August 2016, with 2,650 (6.46% of the total susceptible population) animals infected, of which 2,350 died (case fatality rate of 88.67%). In our study, we analyzed climatic and epidemiological factors that could have triggered the outbreak. The cancelation of reindeer vaccination against anthrax in 2007 resulted in an increase in population susceptibility. In response to the outbreak, total vaccination of all susceptible animals was resumed. To assess the vaccination effectiveness, we tested 913 samples of blood serum taken from vaccinated reindeer using an antigenic erythrocyte diagnostic kit to detect specific anti-anthrax antibodies via an indirect hemagglutination assay (IHA) 9 months after vaccination. We found that 814 samples had sufficiently high levels of anti-anthrax antibodies to indicate a protection level of 89% (95% confidence interval: 87\u201391%) of the whole reindeer population. Abnormally high ambient temperature in the summer of 2016 contributed to the thawing of permafrost and viable <jats:italic>Bacillus anthracis<\/jats:italic> spores could have become exposed to the surface; the monthly average air temperatures in June, July, and August 2016 were 20\u2013100% higher than those of the previous 30-year period, while the maximum air temperatures were 16\u201375% higher. Using the projected climate data for 2081\u20132100 according to the \u201cworst case\u201d RCP8.5 scenario, we demonstrated that the yearly air temperature may average above 0\u00b0C across the entire Yamal Peninsula, while the yearly number of days with a mean temperature above 0\u00b0C may rise by 49 \u00b1 6 days, which would provide conditions for reactivation of soil anthrax reservoirs. Our results showed that the outbreak of anthrax occurred under conditions of a significant increase in air temperature in the study area, underlined the importance of vaccination for controlling the epidemic process, and demonstrated the effectiveness of monitoring studies using the IHA diagnostic kit for detecting erythrocyte anthrax antigens.<\/jats:p>","DOI":"10.3389\/fvets.2021.668420","type":"journal-article","created":{"date-parts":[[2021,6,24]],"date-time":"2021-06-24T05:12:05Z","timestamp":1624511525000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":21,"title":["Reindeer Anthrax in the Russian Arctic, 2016: Climatic Determinants of the Outbreak and Vaccination Effectiveness"],"prefix":"10.3389","volume":"8","author":[{"given":"Elena A.","family":"Liskova","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Irina Y.","family":"Egorova","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuri O.","family":"Selyaninov","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Irina V.","family":"Razheva","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nadezhda A.","family":"Gladkova","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nadezhda N.","family":"Toropova","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Olga I.","family":"Zakharova","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Olga A.","family":"Burova","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Galina V.","family":"Surkova","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Svetlana M.","family":"Malkhazova","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fedor I.","family":"Korennoy","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ivan V.","family":"Iashin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrei A.","family":"Blokhin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2021,6,24]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"e0208621","DOI":"10.1371\/journal.pone.0208621","article-title":"Decoupling environmental effects and host population dynamics for anthrax, a classic reservoir-driven disease","volume":"13","author":"Gomez","year":"2018","journal-title":"PLoS ONE."},{"key":"B2","unstructured":"Rovid SpicklerA\n          Anthrax2003"},{"key":"B3","doi-asserted-by":"publisher","first-page":"892","DOI":"10.1111\/tbed.12456","article-title":"Historical cases of anthrax in Sweden 1916\u20131961","volume":"64","author":"Elvander","year":"2017","journal-title":"Transbound Emerg Dis."},{"key":"B4","doi-asserted-by":"publisher","first-page":"815","DOI":"10.1056\/NEJM199909093411107","article-title":"Anthrax","volume":"341","author":"Dixon","year":"1999","journal-title":"N Engl J Med."},{"key":"B5","unstructured":"Anthrax in Humans and Animals"},{"key":"B6","doi-asserted-by":"publisher","first-page":"359","DOI":"10.20506\/rst.21.2.1336","article-title":"Anthrax and wildlife","volume":"21","author":"Hugh-Jones","year":"2002","journal-title":"Rev Sci Tech l'OIE"},{"key":"B7","doi-asserted-by":"publisher","first-page":"65","DOI":"10.21055\/0370-1069-2017-1-65-71","article-title":"The current situation on anthrax in Russia and in the world main trends and features","volume":"1","author":"Eremenko","year":"2017","journal-title":"Probl Part Danger Infect."},{"key":"B8","doi-asserted-by":"publisher","first-page":"8482","DOI":"10.3402\/gha.v4i0.8482","article-title":"Thawing of permafrost may disturb historic cattle burial grounds in East Siberia","volume":"4","author":"Revich","year":"2011","journal-title":"Glob Health Action."},{"key":"B9","unstructured":"Anthrax in Yamal: re-emergence causes and diagnostic issues37\n            SelyaninovYO\n            EgorovaIY\n            KolbasovDV\n            ListishenkoAA\n          Veterinariya.102016"},{"key":"B10","doi-asserted-by":"publisher","first-page":"e0209140","DOI":"10.1371\/journal.pone.0209140","article-title":"Insights from Bacillus anthracis strains isolated from permafrost in the tundra zone of Russia","volume":"14","author":"Timofeev","year":"2019","journal-title":"PLoS ONE."},{"key":"B11","doi-asserted-by":"publisher","first-page":"130","DOI":"10.7589\/0090-3558-29.1.130","article-title":"An enzyme-linked immunosorbent assay for detecting anthrax antibody in white-tailed deer (Odocoileus virginianus): evaluation of anthrax vaccination and sera from free-ranging deer","volume":"29","author":"Peterson","year":"1993","journal-title":"J Wildl Dis."},{"key":"B12","doi-asserted-by":"publisher","first-page":"44","DOI":"10.30766\/2072-9081.2017.59.4.44-48","article-title":"Veterinary problems of northern reindeer breeding and improvement of technology of carrying out of mass treatment-and-prophylactic actions","volume":"59","author":"Kazanovskiy","year":"2017","journal-title":"Agric Sci Euro-North-East."},{"key":"B13","doi-asserted-by":"publisher","first-page":"42","DOI":"10.21055\/0370-1069-2010-3(105)-42-45","article-title":"Detection of antibodies to protective antigen of bacillus anthracis using indirect hemagglutination test and enzime-linked immunosorbent assay","volume":"52","author":"Barkov","year":"2010","journal-title":"Probl Part Danger Infect."},{"key":"B14","unstructured":"VasinaNK\n            SelyaninovYO\n            EgorovaIY\n          Serological Monitoring of the Efficiency of Specific Prevention of the Siberian Ulcer in the Cfd Rf2012"},{"key":"B15","doi-asserted-by":"publisher","first-page":"131","DOI":"10.25283\/2223-4594-2017-2-131-137","article-title":"Northern reindeer breeding in the twenty-first century: genetic resource, cultural heritage and business","volume":"4","author":"Yuzhakov","year":"2017","journal-title":"Arct Ecol Econ."},{"key":"B16","unstructured":"A Report on Climate Features on the Territory of the Russian Federation in 20182019"},{"key":"B17","unstructured":"BulyginaON\n            RazuvaevVN\n            AleksandrovaTM\n          Description of the Data Array of Daily Air Temperature and the Quantity of Precipitation at Meteorological Stations in Russia and the FORMER USSR (TTTR) \"Certificate of State Registration of the Database No. 2014620942"},{"key":"B18","doi-asserted-by":"publisher","first-page":"313","DOI":"10.1080\/02693799008941549","article-title":"Kriging: a method of interpolation for geographical information systems","volume":"4","author":"Oliver","year":"1990","journal-title":"Int J Geographic Inform Syst."},{"key":"B19","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1007\/978-3-642-03647-7_17","article-title":"The variogram and kriging","volume-title":"Handbook of Applied Spatial Analysis","author":"Oliver","year":"2010"},{"key":"B20","doi-asserted-by":"publisher","first-page":"D21110","DOI":"10.1029\/2008JD010100","article-title":"Comparison of six methods for the interpolation of daily, European climate data","volume":"113","author":"Hofstra","year":"2008","journal-title":"J Geophys Res Atmos."},{"key":"B21","doi-asserted-by":"publisher","first-page":"485","DOI":"10.1175\/BAMS-D-11-00094.1","article-title":"An overview of CMIP5 and the experiment design","volume":"93","author":"Taylor","year":"2012","journal-title":"Bull Am Meteorol Soc."},{"key":"B22","unstructured":"Towards New Scenarios for Analysis of Emissions Climate Change Impacts and Response Strategies. Technical Summary"},{"key":"B23","article-title":"VNIIVViM (Pocrov)","year":"1979"},{"key":"B24","author":"Bakulov","year":"2001","journal-title":"Anthrax. New Pages in the Study of the \u201cold disease.\u201d Posad"},{"key":"B25","doi-asserted-by":"publisher","first-page":"25","DOI":"10.30896\/0042-4846.2019.22.11.25-29","article-title":"The use of erythrocyte diagnostic in assessing the effectiveness of cattle immunoprophylaxis against anthrax","volume":"11","author":"Ivanova","year":"2019","journal-title":"Veterinariya."},{"key":"B26","first-page":"133","volume-title":"Handbook of Microbiological and Virological Research Methods","author":"Birger","year":"1982"},{"key":"B27","first-page":"729","volume-title":"Risk Anaysis - A Quantitative Guide","author":"Vose","year":"2008"},{"key":"B28","doi-asserted-by":"publisher","first-page":"63","DOI":"10.21055\/0370-1069-2018-1-63-65","article-title":"Epidemiological and epizootiological situation on anthrax in 2017, Forecast for 2018","volume":"1","author":"Ryazanova","year":"2018","journal-title":"Probl Part Danger Infect."},{"key":"B29","doi-asserted-by":"publisher","first-page":"1813","DOI":"10.1111\/brv.12420","article-title":"Spores and soil from six sides: interdisciplinarity and the environmental biology of anthrax (Bacillus anthracis)","volume":"93","author":"Carlson","year":"2018","journal-title":"Biol Rev."},{"key":"B30","doi-asserted-by":"publisher","first-page":"10","DOI":"10.1016\/j.micinf.2018.06.001","article-title":"Zoonoses under our noses","volume":"21","author":"Cross","year":"2019","journal-title":"Microbes Infect."},{"key":"B31","doi-asserted-by":"publisher","first-page":"1610","DOI":"10.1128\/AEM.71.3.1610-1615.2005","article-title":"Natural dissemination of Bacillus anthracis spores in Northern Canada","volume":"71","author":"Dragon","year":"2005","journal-title":"Appl Environ Microbiol."},{"key":"B32","first-page":"256","article-title":"Investigation, control and epizootiology of anthrax in a geographically isolated, free-roaming bison population in northern Canada","volume":"59","author":"Gates","year":"1995","journal-title":"Can J Vet Res."},{"key":"B33","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1186\/1751-0147-52-7","article-title":"Anthrax outbreak in a Swedish beef cattle herd - 1st case in 27 years: case report","volume":"52","author":"Lewerin","year":"2010","journal-title":"Acta Vet Scand."},{"key":"B34","doi-asserted-by":"publisher","first-page":"174","DOI":"10.1007\/s10393-020-01474-z","article-title":"Factors contributing to anthrax outbreaks in the circumpolar North","volume":"17","author":"Hueffer","year":"2020","journal-title":"Ecohealth."},{"key":"B35","doi-asserted-by":"publisher","first-page":"1009","DOI":"10.3389\/fmicb.2015.01009","article-title":"Anthrax prophylaxis: Recent advances and future directions","volume":"6","author":"Williamson","year":"2015","journal-title":"Front Microbiol."},{"key":"B36","unstructured":"Anthrax in Humans and Animals. Fourth Edition Food and Agriculture Organization of the United Nations World Organisation for Animal Health2008"},{"key":"B37","first-page":"83","article-title":"Severe anthrax outbreaks in Italy in 2004: considerations on factors involved in the spread of infection","volume":"33","author":"Fasanella","year":"2010","journal-title":"New Microbiol."},{"key":"B38","doi-asserted-by":"publisher","first-page":"e0192031","DOI":"10.1371\/journal.pone.0192031","article-title":"Rates and risk factors for human cutaneous anthrax in the country of Georgia: National surveillance data, 2008\u20132015","volume":"13","author":"Kasradze","year":"2018","journal-title":"PLoS ONE."},{"key":"B39","doi-asserted-by":"publisher","first-page":"e2985","DOI":"10.1371\/journal.pntd.0002985","article-title":"Changing patterns of human anthrax in azerbaijan during the post-soviet and preemptive livestock vaccination eras","volume":"8","author":"Kracalik","year":"2014","journal-title":"PLoS Negl Trop Dis."},{"key":"B40","doi-asserted-by":"publisher","first-page":"18792","DOI":"10.3402\/ijch.v71i0.18792","article-title":"Climate change and zoonotic infections in the Russian arctic","volume":"71","author":"Revich","year":"2012","journal-title":"Int J Circumpolar Health."},{"key":"B41","first-page":"27","article-title":"Experience in the prevention of anthrax in animals in Russia","volume":"5","author":"Ipatenko","year":"1995","journal-title":"Veterinary"},{"key":"B42","first-page":"757","volume-title":"Infectious Diseases of Humans: Dynamics and Control","author":"Anderson","year":"1992"},{"key":"B43","doi-asserted-by":"publisher","first-page":"288","DOI":"10.1016\/j.idm.2017.06.002","article-title":"Reproduction numbers of infectious disease models","volume":"2","author":"van den Driessche","year":"2017","journal-title":"Infect Dis Model."},{"key":"B44","doi-asserted-by":"publisher","first-page":"303","DOI":"10.1007\/s11538-016-0238-1","article-title":"A mathematical model of anthrax transmission in animal populations","volume":"79","author":"Saad-Roy","year":"2017","journal-title":"Bull Math Biol."},{"key":"B45","doi-asserted-by":"publisher","first-page":"104864","DOI":"10.1016\/j.atmosres.2020.104864","article-title":"Is the cold region in Northeast China still getting warmer under climate change impact?","volume":"237","author":"Zhou","year":"2020","journal-title":"Atmos Res."},{"key":"B46","doi-asserted-by":"publisher","first-page":"14","DOI":"10.1016\/j.coesh.2018.03.007","article-title":"Permafrost degradation on a warmer Earth: Challenges and perspectives","volume":"5","author":"Oliva","year":"2018","journal-title":"Curr Opin Environ Sci Heal."},{"key":"B47","doi-asserted-by":"publisher","first-page":"264","DOI":"10.1038\/s41467-018-08240-4","article-title":"Permafrost is warming at a global scale","volume":"10","author":"Biskaborn","year":"2019","journal-title":"Nat Commun."},{"key":"B48","doi-asserted-by":"publisher","first-page":"1859","DOI":"10.1128\/IAI.55.8.1859-1861.1987","article-title":"mechanical transmission of Bacillus anthracis by stable flies (Stomoxys calcitrans) and Mosquitoes (Aedes aegypti and Aedes taeniorhynchus)","volume":"55","author":"Turell","year":"1987","journal-title":"Infect Immun"},{"key":"B49","doi-asserted-by":"publisher","first-page":"064026","DOI":"10.1088\/1748-9326\/9\/6\/064026","article-title":"An observation-based assessment of the influences of air temperature and snow depth on soil temperature in Russia","volume":"9","author":"Park","year":"2014","journal-title":"Environ Res Lett."},{"key":"B50","unstructured":"Elimination of the Outbreak of Anthrax in the Yamal Region"},{"key":"B51","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1134\/S1067413617020059","article-title":"Anthrax in Yamal: an ecological look at traditional reindeer husbandry","volume":"2","author":"Bogdanov","year":"2017","journal-title":"Ecology."}],"container-title":["Frontiers in Veterinary Science"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fvets.2021.668420\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,6,24]],"date-time":"2021-06-24T05:12:17Z","timestamp":1624511537000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fvets.2021.668420\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,6,24]]},"references-count":51,"alternative-id":["10.3389\/fvets.2021.668420"],"URL":"https:\/\/doi.org\/10.3389\/fvets.2021.668420","relation":{},"ISSN":["2297-1769"],"issn-type":[{"value":"2297-1769","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,6,24]]},"article-number":"668420"}}