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Wild ungulate species differ in their contribution to the transmission of Ixodes ricinus-borne pathogens

BACKGROUND: Several ungulate species are feeding and propagation hosts for the tick Ixodes ricinus as well as hosts to a wide range of zoonotic pathogens. Here, we focus on Anaplasma phagocytophilum and Borrelia burgdorferi (s.l.), two important pathogens for which ungulates are amplifying and dilut...

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Autores principales: Fabri, Nannet D., Sprong, Hein, Hofmeester, Tim R., Heesterbeek, Hans, Donnars, Björn F., Widemo, Fredrik, Ecke, Frauke, Cromsigt, Joris P. G. M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8272276/
https://www.ncbi.nlm.nih.gov/pubmed/34246293
http://dx.doi.org/10.1186/s13071-021-04860-w
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author Fabri, Nannet D.
Sprong, Hein
Hofmeester, Tim R.
Heesterbeek, Hans
Donnars, Björn F.
Widemo, Fredrik
Ecke, Frauke
Cromsigt, Joris P. G. M.
author_facet Fabri, Nannet D.
Sprong, Hein
Hofmeester, Tim R.
Heesterbeek, Hans
Donnars, Björn F.
Widemo, Fredrik
Ecke, Frauke
Cromsigt, Joris P. G. M.
author_sort Fabri, Nannet D.
collection PubMed
description BACKGROUND: Several ungulate species are feeding and propagation hosts for the tick Ixodes ricinus as well as hosts to a wide range of zoonotic pathogens. Here, we focus on Anaplasma phagocytophilum and Borrelia burgdorferi (s.l.), two important pathogens for which ungulates are amplifying and dilution hosts, respectively. Ungulate management is one of the main tools to mitigate human health risks associated with these tick-borne pathogens. Across Europe, different species of ungulates are expanding their ranges and increasing in numbers. It is currently unclear if and how the relative contribution to the life-cycle of I. ricinus and the transmission cycles of tick-borne pathogens differ among these species. In this study, we aimed to identify these relative contributions for five European ungulate species. METHODS: We quantified the tick load and collected ticks and spleen samples from hunted fallow deer (Dama dama, n = 131), moose (Alces alces, n = 15), red deer (Cervus elaphus, n = 61), roe deer (Capreolus capreolus, n = 30) and wild boar (Sus scrofa, n = 87) in south-central Sweden. We investigated the presence of tick-borne pathogens in ticks and spleen samples using real-time PCR. We determined if ungulate species differed in tick load (prevalence and intensity) and in infection prevalence in their tissue as well as in the ticks feeding on them. RESULTS: Wild boar hosted fewer adult female ticks than any of the deer species, indicating that deer are more important as propagation hosts. Among the deer species, moose had the lowest number of female ticks, while there was no difference among the other deer species. Given the low number of infected nymphs, the relative contribution of all ungulate species to the transmission of B. burgdorferi (s.l.) was low. Fallow deer, red deer and roe deer contributed more to the transmission of A. phagocytophilum than wild boar. CONCLUSIONS: The ungulate species clearly differed in their role as a propagation host and in the transmission of B. burgdorferi and A. phagocytophilum. This study provides crucial information for ungulate management as a tool to mitigate zoonotic disease risk and argues for adapting management approaches to the local ungulate species composition and the pathogen(s) of concern. GRAPHIC ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-021-04860-w.
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spelling pubmed-82722762021-07-12 Wild ungulate species differ in their contribution to the transmission of Ixodes ricinus-borne pathogens Fabri, Nannet D. Sprong, Hein Hofmeester, Tim R. Heesterbeek, Hans Donnars, Björn F. Widemo, Fredrik Ecke, Frauke Cromsigt, Joris P. G. M. Parasit Vectors Research BACKGROUND: Several ungulate species are feeding and propagation hosts for the tick Ixodes ricinus as well as hosts to a wide range of zoonotic pathogens. Here, we focus on Anaplasma phagocytophilum and Borrelia burgdorferi (s.l.), two important pathogens for which ungulates are amplifying and dilution hosts, respectively. Ungulate management is one of the main tools to mitigate human health risks associated with these tick-borne pathogens. Across Europe, different species of ungulates are expanding their ranges and increasing in numbers. It is currently unclear if and how the relative contribution to the life-cycle of I. ricinus and the transmission cycles of tick-borne pathogens differ among these species. In this study, we aimed to identify these relative contributions for five European ungulate species. METHODS: We quantified the tick load and collected ticks and spleen samples from hunted fallow deer (Dama dama, n = 131), moose (Alces alces, n = 15), red deer (Cervus elaphus, n = 61), roe deer (Capreolus capreolus, n = 30) and wild boar (Sus scrofa, n = 87) in south-central Sweden. We investigated the presence of tick-borne pathogens in ticks and spleen samples using real-time PCR. We determined if ungulate species differed in tick load (prevalence and intensity) and in infection prevalence in their tissue as well as in the ticks feeding on them. RESULTS: Wild boar hosted fewer adult female ticks than any of the deer species, indicating that deer are more important as propagation hosts. Among the deer species, moose had the lowest number of female ticks, while there was no difference among the other deer species. Given the low number of infected nymphs, the relative contribution of all ungulate species to the transmission of B. burgdorferi (s.l.) was low. Fallow deer, red deer and roe deer contributed more to the transmission of A. phagocytophilum than wild boar. CONCLUSIONS: The ungulate species clearly differed in their role as a propagation host and in the transmission of B. burgdorferi and A. phagocytophilum. This study provides crucial information for ungulate management as a tool to mitigate zoonotic disease risk and argues for adapting management approaches to the local ungulate species composition and the pathogen(s) of concern. GRAPHIC ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-021-04860-w. BioMed Central 2021-07-10 /pmc/articles/PMC8272276/ /pubmed/34246293 http://dx.doi.org/10.1186/s13071-021-04860-w Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Fabri, Nannet D.
Sprong, Hein
Hofmeester, Tim R.
Heesterbeek, Hans
Donnars, Björn F.
Widemo, Fredrik
Ecke, Frauke
Cromsigt, Joris P. G. M.
Wild ungulate species differ in their contribution to the transmission of Ixodes ricinus-borne pathogens
title Wild ungulate species differ in their contribution to the transmission of Ixodes ricinus-borne pathogens
title_full Wild ungulate species differ in their contribution to the transmission of Ixodes ricinus-borne pathogens
title_fullStr Wild ungulate species differ in their contribution to the transmission of Ixodes ricinus-borne pathogens
title_full_unstemmed Wild ungulate species differ in their contribution to the transmission of Ixodes ricinus-borne pathogens
title_short Wild ungulate species differ in their contribution to the transmission of Ixodes ricinus-borne pathogens
title_sort wild ungulate species differ in their contribution to the transmission of ixodes ricinus-borne pathogens
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8272276/
https://www.ncbi.nlm.nih.gov/pubmed/34246293
http://dx.doi.org/10.1186/s13071-021-04860-w
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