{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,13]],"date-time":"2026-07-13T06:21:00Z","timestamp":1783923660953,"version":"3.55.0"},"reference-count":43,"publisher":"Public Library of Science (PLoS)","issue":"7","license":[{"start":{"date-parts":[[2022,7,20]],"date-time":"2022-07-20T00:00:00Z","timestamp":1658275200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100002341","name":"Academy of Finland","doi-asserted-by":"crossref","award":["334792"],"award-info":[{"award-number":["334792"]}],"id":[{"id":"10.13039\/501100002341","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100007601","name":"Horizon 2020","doi-asserted-by":"publisher","award":["856612"],"award-info":[{"award-number":["856612"]}],"id":[{"id":"10.13039\/501100007601","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Academy of Finland Centre of Excellence","award":["307331"],"award-info":[{"award-number":["307331"]}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:p>Tick-borne diseases are among the challenges associated with warming climate. Many studies predict, and already note, expansion of ticks\u2019 habitats to the north, bringing previously non-endemic diseases, such as borreliosis and encephalitis, to the new areas. In addition, higher temperatures accelerate phases of ticks\u2019 development in areas where ticks have established populations. Earlier works have shown that meteorological parameters, such as temperature and humidity influence ticks\u2019 survival and define their areas of habitat. Here, we study the link between climatic parameters and tick-related hospital visits as well as borreliosis incidence rates focusing on European Russia. We have used yearly incidence rates of borreliosis spanning a period of 20 years (1997-2016) and weekly tick-related hospital visits spanning two years (2018-2019). We identify regions in Russia characterized by similar dynamics of incidence rates and dominating tick species. For each cluster, we find a set of climatic parameters that are significantly correlated with the incidence rates, though a linear regression approach using exclusively climatic parameters to incidence prediction was less than 50% effective. On a weekly timescale, we find correlations of different climatic parameters with hospital visits. Finally, we trained two long short-term memory neural network models to project the tick-related hospital visits until the end of the century, under the RCP8.5 climate scenario, and present our findings in the evolution of the tick season length for different regions in Russia. Our results show that the regions with an expected increase in both tick season length and borreliosis incidence rates are located in the southern forested areas of European Russia. Oppositely, our projections suggest no prolongation of the tick season length in the northern areas with already established tick population.<\/jats:p>","DOI":"10.1371\/journal.pone.0269846","type":"journal-article","created":{"date-parts":[[2022,7,20]],"date-time":"2022-07-20T17:24:01Z","timestamp":1658337841000},"page":"e0269846","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":7,"title":["The impact of climatic factors on tick-related hospital visits and borreliosis incidence rates in European Russia"],"prefix":"10.1371","volume":"17","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-6497-3221","authenticated-orcid":true,"given":"Pantelis","family":"Georgiades","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ekaterina","family":"Ezhova","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Meri","family":"R\u00e4ty","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dmitry","family":"Orlov","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Markku","family":"Kulmala","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6307-3846","authenticated-orcid":true,"given":"Jos","family":"Lelieveld","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Svetlana","family":"Malkhazova","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2674-592X","authenticated-orcid":true,"given":"Kamil","family":"Erguler","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1881-9044","authenticated-orcid":true,"given":"Tuukka","family":"Pet\u00e4j\u00e4","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2022,7,20]]},"reference":[{"issue":"4","key":"pone.0269846.ref001","doi-asserted-by":"crossref","first-page":"496","DOI":"10.1134\/S0013873818040115","article-title":"Influence of Abiotic Factors on Different Developmental Stages of the Taiga Tick Ixodes persulcatus and the Sheep Tick Ixodes ricinus","volume":"98","author":"MB Sirotkin","year":"2018","journal-title":"Entomological Review"},{"key":"pone.0269846.ref002","unstructured":"Balashov YS. Ixodid ticks-parasites and vectors of diseases. St Petersburg, Nauka. 1998; p. 287 (In Russian)."},{"issue":"1","key":"pone.0269846.ref003","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1756-3305-6-1","article-title":"Driving forces for changes in geographical distribution of Ixodes ricinus ticks in Europe","volume":"6","author":"JM Medlock","year":"2013","journal-title":"Parasites and Vectors"},{"issue":"4","key":"pone.0269846.ref004","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1134\/S2079086419040078","article-title":"Modeling of Epizootic Process in Obligate Vector-Borne Infections Transmitted by Ticks","volume":"9","author":"ER Salman","year":"2019","journal-title":"Biology Bulletin Reviews"},{"issue":"S1","key":"pone.0269846.ref005","doi-asserted-by":"crossref","first-page":"S37","DOI":"10.1017\/S0031182004004925","article-title":"Tick ecology: processes and patterns behind the epidemiological risk posed by ixodid ticks as vectors","volume":"129","author":"SE Randolph","year":"2004","journal-title":"Parasitology"},{"issue":"2","key":"pone.0269846.ref006","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1016\/j.vetpar.2009.06.001","article-title":"Influence of climatic factors on dynamics of questing Ixodes ricinus ticks in Slovenia","volume":"164","author":"N Knap","year":"2009","journal-title":"Veterinary Parasitology"},{"issue":"5","key":"pone.0269846.ref007","doi-asserted-by":"crossref","first-page":"992","DOI":"10.1016\/j.ttbdis.2016.05.006","article-title":"Diapause in ticks of the medically important Ixodes ricinus species complex","volume":"7","author":"JS Gray","year":"2016","journal-title":"Ticks and Tick-borne Diseases"},{"issue":"5","key":"pone.0269846.ref008","doi-asserted-by":"crossref","first-page":"101449","DOI":"10.1016\/j.ttbdis.2020.101449","article-title":"Monitoring of ticks and tick-borne pathogens through a nationwide research station network in Finland","volume":"11","author":"JJ Sormunen","year":"2020","journal-title":"Ticks and Tick-borne Diseases"},{"issue":"21","key":"pone.0269846.ref009","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3390\/ijerph17218006","article-title":"Study of the relationship between the average annual temperature of atmospheric air and the number of tick-bitten humans in the north of European Russia","volume":"17","author":"A Tronin","year":"2020","journal-title":"International Journal of Environmental Research and Public Health"},{"issue":"39","key":"pone.0269846.ref010","first-page":"558","article-title":"The taiga tick Ixodes persulcatus: Propagation under climate change conditions in the 21st century","author":"IO Popov","journal-title":"Russ Meteorol Hydrol"},{"issue":"3","key":"pone.0269846.ref011","doi-asserted-by":"crossref","first-page":"226","DOI":"10.1111\/j.1365-2915.2009.00813.x","article-title":"Risk indicators for the tick Ixodes ricinus and Borrelia burgdorferi sensu lato in Sweden","volume":"23","author":"TGT Jaenson","year":"2009","journal-title":"Medical and Veterinary Entomology"},{"issue":"1665","key":"pone.0269846.ref012","doi-asserted-by":"crossref","first-page":"20140051","DOI":"10.1098\/rstb.2014.0051","article-title":"Climate change and Ixodes tick-borne diseases of humans","volume":"370","author":"RS Ostfeld","year":"2015","journal-title":"Philosophical Transactions of the Royal Society B: Biological Sciences"},{"issue":"1","key":"pone.0269846.ref013","first-page":"1","article-title":"Changes in the geographical distribution and abundance of the tick Ixodes ricinus during the past 30 years in Sweden","volume":"5","author":"TGT Jaenson","year":"2012","journal-title":"Parasites and Vectors"},{"issue":"1","key":"pone.0269846.ref014","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1756-3305-4-84","article-title":"Multi-source analysis reveals latitudinal and altitudinal shifts in range of Ixodes ricinus at its northern distribution limit","volume":"4","author":"S Jore","year":"2011","journal-title":"Parasites and Vectors"},{"issue":"1","key":"pone.0269846.ref015","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41598-017-15742-6","article-title":"Emergence of tick-borne diseases at northern latitudes in Europe: A comparative approach","volume":"7","author":"A Mysterud","year":"2017","journal-title":"Scientific Reports"},{"issue":"1","key":"pone.0269846.ref016","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s13071-017-2375-2","article-title":"Surveillance of Ixodes ricinus ticks (Acari: Ixodidae) in Iceland","volume":"10","author":"M Alfredsson","year":"2017","journal-title":"Parasites and Vectors"},{"issue":"5","key":"pone.0269846.ref017","doi-asserted-by":"crossref","first-page":"101495","DOI":"10.1016\/j.ttbdis.2020.101495","article-title":"Establishing a baseline for tick surveillance in Alaska: Tick collection records from 1909-2019","volume":"11","author":"MB Hahn","year":"2020","journal-title":"Ticks and Tick-borne Diseases"},{"issue":"12","key":"pone.0269846.ref018","doi-asserted-by":"crossref","first-page":"1221","DOI":"10.1503\/cmaj.080148","article-title":"The emergence of Lyme disease in Canada","volume":"180","author":"NH Ogden","year":"2009","journal-title":"Cmaj"},{"key":"pone.0269846.ref019","doi-asserted-by":"crossref","first-page":"8448","DOI":"10.3402\/gha.v4i0.8448","article-title":"The impact of climate change on the expansion of Ixodes persulcatus habitat and the incidence of tick-borne encephalitis in the north of European Russia","volume":"4","author":"NK Tokarevich","year":"2011","journal-title":"Global health action"},{"issue":"1","key":"pone.0269846.ref020","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1080\/22423982.2017.1298882","article-title":"Impact of air temperature variation on the ixodid ticks habitat and tick-borne encephalitis incidence in the Russian Arctic: The case of the Komi Republic","volume":"76","author":"N Tokarevich","year":"2017","journal-title":"International Journal of Circumpolar Health"},{"issue":"2","key":"pone.0269846.ref021","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3390\/atmos12020233","article-title":"Quantifying the northward spread of ticks (ixodida) as climate warms in northern Russia","volume":"12","author":"LN Vladimirov","year":"2021","journal-title":"Atmosphere"},{"issue":"116","key":"pone.0269846.ref022","article-title":"Modelling the seasonality of Lyme disease risk and the potential impacts of a warming climate within the heterogeneous landscapes of Scotland","volume":"13","author":"S Li","year":"2016","journal-title":"Journal of the Royal Society Interface"},{"issue":"6","key":"pone.0269846.ref023","first-page":"1","article-title":"Lyme disease risks in europe under multiple uncertain drivers of change","volume":"127","author":"S Li","year":"2019","journal-title":"Environmental Health Perspectives"},{"issue":"MAR(March)","key":"pone.0269846.ref024","first-page":"1","article-title":"Impact of climate trends on tick-borne pathogen transmission","volume":"3","author":"A Estrada-Pe\u00f1a","year":"2012","journal-title":"Frontiers in Physiology"},{"issue":"1","key":"pone.0269846.ref025","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1186\/1756-3305-6-271","article-title":"Effects of global changes on the climatic niche of the tick Ixodes ricinus inferred by species distribution modelling","volume":"6","author":"D Porretta","year":"2013","journal-title":"Parasites and Vectors"},{"issue":"10","key":"pone.0269846.ref026","doi-asserted-by":"crossref","first-page":"1568","DOI":"10.3201\/eid1210.060320","article-title":"Siberian subtype tickborne encephalitis virus, Finland","volume":"12","author":"AE J\u00e4\u00e4skel\u00e4inen","year":"2006","journal-title":"Emerging Infectious Diseases"},{"issue":"1","key":"pone.0269846.ref027","first-page":"1","article-title":"First evidence of established populations of the taiga tick Ixodes persulcatus (Acari: Ixodidae) in Sweden","volume":"9","author":"TGT Jaenson","year":"2016","journal-title":"Parasites and Vectors"},{"key":"pone.0269846.ref028","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3390\/ijerph17228453","article-title":"Healthy ecosystems are a prerequisite for human health\u2014a call for action in the era of climate change with a focus on russia","volume":"17","author":"D Orlov","year":"2020","journal-title":"International Journal of Environmental Research and Public Health"},{"key":"pone.0269846.ref029","unstructured":"Bulygina ON, Veselov VM, Razuvaev VN, Aleksandrova TM. Meteorological Data from the Russian Arctic, 1961-2000, Version 1. National Snow and Ice Data Center. 2020;."},{"key":"pone.0269846.ref030","unstructured":"Mu\u00f1oz Sabater J. ERA5-Land monthly averaged data from 1981 to present. Copernicus Climate Change Service (C3S) Climate Data Store (CDS). Copernicus Climate Change Service (C3S) Climate Data Store (CDS) (Accessed on 15-01-2021). 2019;."},{"issue":"11-12","key":"pone.0269846.ref031","doi-asserted-by":"crossref","first-page":"3237","DOI":"10.1007\/s00382-014-2418-8","article-title":"Selecting CMIP5 GCMs for downscaling over multiple regions","volume":"44","author":"CF McSweeney","year":"2015","journal-title":"Climate Dynamics"},{"issue":"9","key":"pone.0269846.ref032","doi-asserted-by":"crossref","first-page":"3309","DOI":"10.5194\/hess-16-3309-2012","article-title":"Technical Note: Bias correcting climate model simulated daily temperature extremes with quantile mapping","volume":"16","author":"B Thrasher","year":"2012","journal-title":"Hydrology and Earth System Sciences"},{"issue":"1","key":"pone.0269846.ref033","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/0304-3800(81)90011-9","article-title":"Calculating solar radiation for ecological studies","volume":"14","author":"TD Brock","year":"1981","journal-title":"Ecological Modelling"},{"issue":"1","key":"pone.0269846.ref034","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/0304-3800(94)00034-F","article-title":"A model comparison for daylength as a function of latitude and day of year","volume":"80","author":"WC Forsythe","year":"1995","journal-title":"Ecological Modelling"},{"issue":"8","key":"pone.0269846.ref035","doi-asserted-by":"crossref","first-page":"1735","DOI":"10.1162\/neco.1997.9.8.1735","article-title":"Long Short-Term Memory","volume":"9","author":"S Hochreiter","year":"1997","journal-title":"Neural Computation"},{"key":"pone.0269846.ref036","first-page":"473","article-title":"LSTM can solve hard long time lag problems","author":"S Hochreiter","year":"1997","journal-title":"Advances in Neural Information Processing Systems"},{"issue":"2","key":"pone.0269846.ref037","doi-asserted-by":"crossref","first-page":"654","DOI":"10.1016\/j.ejor.2017.11.054","article-title":"Deep learning with long short-term memory networks for financial market predictions","volume":"270","author":"T Fischer","year":"2018","journal-title":"European Journal of Operational Research"},{"key":"pone.0269846.ref038","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1134\/S0013873817020117","article-title":"History of the species range of ixodid ticks, vectors of pathogens with natural nidality (Acari, Ixodidae), as a prerequisite of their intraspecific biodiversity","volume":"97","author":"N Filippova","year":"2017","journal-title":"Entomological Review"},{"key":"pone.0269846.ref039","unstructured":"Met Office. Cartopy: a cartographic python library with a Matplotlib interface; 2010\u20142015. Available from: https:\/\/scitools.org.uk\/cartopy."},{"key":"pone.0269846.ref040","article-title":"Influence of Abiotic Factors on Infectious Agents Environmentally Associated with Ixodidae Ticks on the Example of Borrelia and Tick-Borne Encephalitis Virus","volume":"9","author":"MB Sirotkin","year":"2020","journal-title":"Biology Bulletin Reviews"},{"issue":"6","key":"pone.0269846.ref041","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0000500","article-title":"Climate Change Cannot Explain the Upsurge of Tick-Borne Encephalitis in the Baltics","volume":"2","author":"D Sumilo","year":"2007","journal-title":"PLoS ONE"},{"key":"pone.0269846.ref042","unstructured":"Evstegneeva VA, Smolyaninova OL, Ignatkova AC. About the influence of climatic factors on the incidence of Ixodes tick borreliosis. In: Gulyaev GY, editor. Proceedings of the VII International conference \u2018Science and Education: keeping the past, we create the future\u2019; 2017. p. 263\u2013267."},{"issue":"1","key":"pone.0269846.ref043","doi-asserted-by":"crossref","first-page":"207","DOI":"10.5194\/bg-18-207-2021","article-title":"Fire and vegetation dynamics in northwest Siberia during the last 60 years based on high-resolution remote sensing","volume":"18","author":"O Sizov","year":"2021","journal-title":"Biogeosciences"}],"updated-by":[{"DOI":"10.1371\/journal.pone.0322231","type":"correction","label":"Correction","source":"publisher","updated":{"date-parts":[[2025,4,4]],"date-time":"2025-04-04T00:00:00Z","timestamp":1743724800000}}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0269846","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,7,20]],"date-time":"2022-07-20T17:24:50Z","timestamp":1658337890000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0269846"}},"subtitle":[],"editor":[{"given":"Sam R.","family":"Telford III","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2022,7,20]]},"references-count":43,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2022,7,20]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0269846","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,7,20]]}}}