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      Determinants of Crimean–Congo haemorrhagic fever virus exposure dynamics in Mediterranean environments

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          Abstract

          Crimean–Congo haemorrhagic fever (CCHF) is an emerging tick‐borne human disease in Spain. Understanding the spatiotemporal dynamics and exposure risk determinants of CCHF virus (CCHFV) in animal models is essential to predict the time and areas of highest transmission risk. With this goal, we designed a longitudinal survey of two wild ungulate species, the red deer ( Cervus elaphus) and the Eurasian wild boar ( Sus scrofa), in Doñana National Park, a protected Mediterranean biodiversity hotspot with high ungulate and CCHFV vector abundance, and which is also one of the main stopover sites for migratory birds between Africa and western Europe. Both ungulates are hosts to the principal CCHFV vector in Spain, Hyalomma lusitanicum. We sampled wild ungulates annually from 2005 to 2020 and analysed the frequency of exposure to CCHFV by a double‐antigen ELISA. The annual exposure risk was modelled as a function of environmental traits in an approach to understanding exposure risk determinants that allow us to predict the most likely places and years for CCHFV transmission. The main findings show that H. lusitanicum abundance is a fundamental driver of the fine‐scale spatial CCHFV transmission risk, while inter‐annual risk variation is conditioned by virus/vector hosts, host community structure and weather variations. The most relevant conclusion of the study is that the emergence of CCHF in Spain might be associated with recent wild ungulate population changes promoting higher vector abundance. This work provides relevant insights into the transmission dynamics of CCHFV in enzootic scenarios that would allow deepening the understanding of the ecology of CCHFV and its major determinants.

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          Fitting Linear Mixed-Effects Models Usinglme4

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            A protocol for data exploration to avoid common statistical problems

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              Changes in the geographical distribution and abundance of the tick Ixodes ricinus during the past 30 years in Sweden

              Background Ixodes ricinus is the main vector in Europe of human-pathogenic Lyme borreliosis (LB) spirochaetes, the tick-borne encephalitis virus (TBEV) and other pathogens of humans and domesticated mammals. The results of a previous 1994 questionnaire, directed at people living in Central and North Sweden (Svealand and Norrland) and aiming to gather information about tick exposure for humans and domestic animals, suggested that Ixodes ricinus ticks had become more widespread in Central Sweden and the southern part of North Sweden from the early 1980s to the early 1990s. To investigate whether the expansion of the tick's northern geographical range and the increasing abundance of ticks in Sweden were still occurring, in 2009 we performed a follow-up survey 16 years after the initial study. Methods A questionnaire similar to the one used in the 1994 study was published in Swedish magazines aimed at dog owners, home owners, and hunters. The questionnaire was published together with a popular science article about the tick's biology and role as a pathogen vector in Sweden. The magazines were selected to get information from people familiar with ticks and who spend time in areas where ticks might be present. Results Analyses of data from both surveys revealed that during the near 30-year period from the early 1980s to 2008, I. ricinus has expanded its distribution range northwards. In the early 1990s ticks were found in new areas along the northern coastline of the Baltic Sea, while in the 2009 study, ticks were reported for the first time from many locations in North Sweden. This included locations as far north as 66°N and places in the interior part of North Sweden. During this 16-year period the tick's range in Sweden was estimated to have increased by 9.9%. Most of the range expansion occurred in North Sweden (north of 60°N) where the tick's coverage area doubled from 12.5% in the early 1990s to 26.8% in 2008. Moreover, according to the respondents, the abundance of ticks had increased markedly in LB- and TBE-endemic areas in South (Götaland) and Central Sweden. Conclusions The results suggest that I. ricinus has expanded its range in North Sweden and has become distinctly more abundant in Central and South Sweden during the last three decades. However, in the northern mountain region I. ricinus is still absent. The increased abundance of the tick can be explained by two main factors: First, the high availability of large numbers of important tick maintenance hosts, i.e., cervids, particularly roe deer (Capreolus capreolus) during the last three decades. Second, a warmer climate with milder winters and a prolonged growing season that permits greater survival and proliferation over a larger geographical area of both the tick itself and deer. High reproductive potential of roe deer, high tick infestation rate and the tendency of roe deer to disperse great distances may explain the range expansion of I. ricinus and particularly the appearance of new TBEV foci far away from old TBEV-endemic localities. The geographical presence of LB in Sweden corresponds to the distribution of I. ricinus. Thus, LB is now an emerging disease risk in many parts of North Sweden. Unless countermeasures are undertaken to keep the deer populations, particularly C. capreolus and Dama dama, at the relatively low levels that prevailed before the late 1970s - especially in and around urban areas where human population density is high - by e.g. reduced hunting of red fox (Vulpes vulpes) and lynx (Lynx lynx), the incidences of human LB and TBE are expected to continue to be high or even to increase in Sweden in coming decades.
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                Author and article information

                Contributors
                josefrancisco.ruiz@uclm.es
                Journal
                Transbound Emerg Dis
                Transbound Emerg Dis
                10.1111/(ISSN)1865-1682
                TBED
                Transboundary and Emerging Diseases
                John Wiley and Sons Inc. (Hoboken )
                1865-1674
                1865-1682
                17 October 2022
                November 2022
                : 69
                : 6 ( doiID: 10.1111/tbed.v69.6 )
                : 3571-3581
                Affiliations
                [ 1 ] Instituto de Investigación en Recursos Cinegéticos (IREC) CSIC‐UCLM‐JCCM Ciudad Real Spain
                [ 2 ] Departamento de Sanidad Animal Facultad de Veterinaria Universidad de León León Spain
                [ 3 ] Departamento de Anatomía y Anatomía Patológica Comparadas y Toxicología, Grupo de Investigación en Sanidad Animal y Zoonosis (GISAZ), UIC Zoonosis y Enfermedades Emergentes ENZOEM Universidad de Córdoba Córdoba Spain
                [ 4 ] CIBERINFEC (ISCIII), CIBER de Enfermedades Infecciosas Instituto de Salud Carlos III Madrid Spain
                [ 5 ] Grupo de Investigación en Sanidad Animal y Zoonosis (GISAZ), Departamento de Sanidad Animal Universidad de Córdoba Córdoba Spain
                Author notes
                [*] [* ] Correspondence

                Francisco Ruiz‐Fons, Instituto de Investigación en Recursos Cinegéticos (IREC), CSIC‐UCLM‐JCCM, Ronda de Toledo, 12, 13071 Ciudad Real, Spain.

                Email: josefrancisco.ruiz@ 123456uclm.es

                Author information
                https://orcid.org/0000-0002-2431-5029
                https://orcid.org/0000-0002-0820-5292
                Article
                TBED14720
                10.1111/tbed.14720
                10092370
                36183164
                dae09849-25aa-42a5-b4dd-791627583e9b
                © 2022 The Authors. Transboundary and Emerging Diseases published by Wiley‐VCH GmbH.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 27 September 2022
                : 02 July 2022
                : 29 September 2022
                Page count
                Figures: 3, Tables: 5, Pages: 11, Words: 8128
                Funding
                Funded by: Ministerio de Ciencia e Innovación , doi 10.13039/501100004837;
                Funded by: European Social Fund , doi 10.13039/501100004895;
                Funded by: European Regional Development Fund , doi 10.13039/501100008530;
                Funded by: Junta de Comunidades de Castilla‐La Mancha , doi 10.13039/501100011698;
                Funded by: Universidad de Castilla‐La Mancha , doi 10.13039/501100007480;
                Categories
                Original Article
                Original Articles
                Custom metadata
                2.0
                November 2022
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.2.7 mode:remove_FC converted:12.04.2023

                Infectious disease & Microbiology
                disease ecology,host–tick–pathogen interactions,tick,wild ungulates,zoonosis

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