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


Journal

Parasites & vectors
ISSN: 1756-3305
Titre abrégé: Parasit Vectors
Pays: England
ID NLM: 101462774

Informations de publication

Date de publication:
10 Jul 2021
Historique:
received: 13 01 2021
accepted: 24 06 2021
entrez: 11 7 2021
pubmed: 12 7 2021
medline: 5 11 2021
Statut: epublish

Résumé

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. 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. 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. 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.

Sections du résumé

BACKGROUND 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 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 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 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.

Identifiants

pubmed: 34246293
doi: 10.1186/s13071-021-04860-w
pii: 10.1186/s13071-021-04860-w
pmc: PMC8272276
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

360

Subventions

Organisme : Future Animals, Nature and Health platform at the Swedish University of Agricultural Sciences
ID : 2018.4.3-4511
Organisme : Naturvårdsverket
ID : NV-01337-15
Organisme : Naturvårdsverket
ID : NV-03047-16
Organisme : Naturvårdsverket
ID : NV-08503-18
Organisme : Dutch research council (NWO)
ID : 022.005.021

Informations de copyright

© 2021. The Author(s).

Références

Parasit Vectors. 2019 Jan 3;12(1):1
pubmed: 30606222
Environ Microbiol. 2013 Feb;15(2):663-73
pubmed: 23279105
J Med Entomol. 1994 Nov;31(6):880-6
pubmed: 7815401
Exp Appl Acarol. 2011 Jan;53(1):79-94
pubmed: 20585837
Emerg Infect Dis. 2012 Jun;18(6):998-1001
pubmed: 22607827
Parasit Vectors. 2016 Feb 20;9:97
pubmed: 26896940
Parasit Vectors. 2019 Sep 6;12(1):434
pubmed: 31492171
New Microbiol. 2002 Oct;25(4):437-48
pubmed: 12437223
Vector Borne Zoonotic Dis. 2012 Jan;12(1):21-7
pubmed: 21923267
Epidemiol Infect. 1996 Dec;117(3):563-6
pubmed: 8972683
Am J Trop Med Hyg. 1993 May;48(5):693-9
pubmed: 8517488
Parasit Vectors. 2020 Jan 20;13(1):34
pubmed: 31959217
Parasit Vectors. 2019 Dec 21;12(1):599
pubmed: 31864403
Zentralbl Bakteriol. 1997 Jun;286(1):93-106
pubmed: 9241805
Vector Borne Zoonotic Dis. 2014 May;14(5):371-3
pubmed: 24745766
Vet Parasitol. 2012 Jun 8;187(1-2):350-3
pubmed: 22260900
Parasit Vectors. 2012 Aug 04;5:156
pubmed: 22862883
Oecologia. 2015 May;178(1):275-84
pubmed: 25543852
Parasit Vectors. 2018 Sep 3;11(1):495
pubmed: 30176908
Parasit Vectors. 2012 Jan 10;5:8
pubmed: 22233771
Euro Surveill. 2019 Feb;24(9):
pubmed: 30862329
Ann Agric Environ Med. 2006;13(1):65-70
pubmed: 16841874
Appl Environ Microbiol. 2006 Dec;72(12):7594-601
pubmed: 17028227
J Clin Microbiol. 1999 Jul;37(7):2215-22
pubmed: 10364588
Trends Microbiol. 2002 Feb;10(2):74-9
pubmed: 11827808
J Insect Sci. 2003;3:34
pubmed: 15841249
Parasit Vectors. 2014 Aug 15;7:365
pubmed: 25127547
J Med Microbiol. 2020 Jun;69(6):781-791
pubmed: 32478654
Parasitology. 2015 Feb;142(2):290-302
pubmed: 25295405
Exp Appl Acarol. 2011 Apr;53(4):399-409
pubmed: 20963472
Front Cell Infect Microbiol. 2013 Jul 22;3:31
pubmed: 23885337
J Med Entomol. 1992 Sep;29(5):813-7
pubmed: 1404260
Ticks Tick Borne Dis. 2016 Jul;7(5):782-787
pubmed: 27020736
Lancet. 2013 Aug 17;382(9892):658
pubmed: 23953389
Ticks Tick Borne Dis. 2014 Oct;5(6):810-7
pubmed: 25113977

Auteurs

Nannet D Fabri (ND)

Department of Wildlife, Fish, and Environmental Studies, Swedish University of Agricultural Sciences, 901 83, Umeå, Sweden. nannet.fabri@slu.se.
Department of Population Health Sciences, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 7, 3584 CL, Utrecht, The Netherlands. nannet.fabri@slu.se.

Hein Sprong (H)

Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Antonie Van Leeuwenhoeklaan 9, 3721 MA, Bilthoven, The Netherlands.

Tim R Hofmeester (TR)

Department of Wildlife, Fish, and Environmental Studies, Swedish University of Agricultural Sciences, 901 83, Umeå, Sweden.

Hans Heesterbeek (H)

Department of Population Health Sciences, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 7, 3584 CL, Utrecht, The Netherlands.

Björn F Donnars (BF)

Department of Population Health Sciences, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 7, 3584 CL, Utrecht, The Netherlands.

Fredrik Widemo (F)

Department of Wildlife, Fish, and Environmental Studies, Swedish University of Agricultural Sciences, 901 83, Umeå, Sweden.

Frauke Ecke (F)

Department of Wildlife, Fish, and Environmental Studies, Swedish University of Agricultural Sciences, 901 83, Umeå, Sweden.

Joris P G M Cromsigt (JPGM)

Department of Wildlife, Fish, and Environmental Studies, Swedish University of Agricultural Sciences, 901 83, Umeå, Sweden.
Centre for African Conservation Ecology, Department of Zoology, Nelson Mandela University, PO Box 77000, Port Elizabeth, 6031, South Africa.
Copernicus Institute of Sustainable Development, Faculty of Geosciences, Utrecht University, Princetonlaan 8a, 3584 CB, Utrecht, The Netherlands.

Articles similaires

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male
Humans Meals Time Factors Female Adult

Classifications MeSH