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Role of mustelids in the life-cycle of ixodid ticks and transmission cycles of four tick-borne pathogens.
Parasit Vectors. 2018 Nov 20; 11(1):600.PV

Abstract

BACKGROUND

Elucidating which wildlife species significantly contribute to the maintenance of Ixodes ricinus populations and the enzootic cycles of the pathogens they transmit is imperative in understanding the driving forces behind the emergence of tick-borne diseases. Here, we aimed to quantify the relative contribution of four mustelid species in the life-cycles of I. ricinus and Borrelia burgdorferi (sensu lato) in forested areas and to investigate their role in the transmission of other tick-borne pathogens. Road-killed badgers, pine martens, stone martens and polecats were collected in Belgium and the Netherlands. Their organs and feeding ticks were tested for the presence of tick-borne pathogens.

RESULTS

Ixodes hexagonus and I. ricinus were found on half of the screened animals (n = 637). Pine martens had the highest I. ricinus burden, whereas polecats had the highest I. hexagonus burden. We detected DNA from B. burgdorferi (s.l.) and Anaplasma phagocytophilum in organs of all four mustelid species (n = 789), and Neoehrlichia mikurensis DNA was detected in all species, except badgers. DNA from B. miyamotoi was not detected in any of the investigated mustelids. From the 15 larvae of I. ricinus feeding on pine martens (n = 44), only one was positive for B. miyamotoi DNA, and all tested negative for B. burgdorferi (s.l.), N. mikurensis and A. phagocytophilum. The two feeding larvae from the investigated polecats (n = 364) and stone martens (n = 39) were negative for all four pathogens. The infection rate of N. mikurensis was higher in feeding nymphs collected from mustelids compared to questing nymphs, but not for B. burgdorferi (s.l.), B. miyamotoi or A. phagocytophilum.

CONCLUSIONS

Although all stages of I. ricinus can be found on badgers, polecats, pine and stone martens, their relative contribution to the life-cycle of I. ricinus in forested areas is less than 1%. Consequently, the relative contribution of mustelids to the enzootic cycles of I. ricinus-borne pathogens is negligible, despite the presence of these pathogens in organs and feeding ticks. Interestingly, all four mustelid species carried all stages of I. hexagonus, potentially maintaining enzootic cycles of this tick species apart from the cycle involving hedgehogs as main host species.

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Authors+Show Affiliations

Hofmeester TR
Resource Ecology Group, Wageningen University, Wageningen, the Netherlands. tim.hofmeester@slu.se. Present address: Department of Wildlife, Fish, and Environmental Studies, Swedish University of Agricultural Sciences, Skogsmarksgränd 17, 907 36, Umeå, Sweden. tim.hofmeester@slu.se.
Krawczyk AI
Centre for Zoonoses and Environmental Microbiology, Centre for Infectious Disease Control, National Institute for Public Health and the Environment (RIVM), Bilthoven, the Netherlands.
van Leeuwen AD
Centre for Zoonoses and Environmental Microbiology, Centre for Infectious Disease Control, National Institute for Public Health and the Environment (RIVM), Bilthoven, the Netherlands.
Fonville M
Centre for Zoonoses and Environmental Microbiology, Centre for Infectious Disease Control, National Institute for Public Health and the Environment (RIVM), Bilthoven, the Netherlands.
Montizaan MGE
Dutch Wildlife Health Centre (DWHC), Utrecht University, Utrecht, the Netherlands.
van den Berge K
Research Institute for Nature and Forest (INBO), Geraardsbergen, Belgium.
Gouwy J
Research Institute for Nature and Forest (INBO), Geraardsbergen, Belgium.
Ruyts SC
Forest and Nature Lab, Department of Environment, Ghent University, Geraardsbergsesteenweg 267, 9090, Gontrode, Melle, Belgium.
Verheyen K
Forest and Nature Lab, Department of Environment, Ghent University, Geraardsbergsesteenweg 267, 9090, Gontrode, Melle, Belgium.
Sprong H
Centre for Zoonoses and Environmental Microbiology, Centre for Infectious Disease Control, National Institute for Public Health and the Environment (RIVM), Bilthoven, the Netherlands. hein.sprong@rivm.nl.

MeSH

Anaplasma phagocytophilumAnaplasmataceaeAnimalsAnimals, WildBelgiumBorrelia InfectionsBorrelia burgdorferiDNA, BacterialEhrlichiosisFerretsHedgehogsIxodesLife Cycle StagesLyme DiseaseMustelidaeNetherlandsNymphRickettsiaTick InfestationsTick-Borne Diseases

Pub Type(s)

Journal Article

Language

eng

PubMed ID

30458847

Citation

Hofmeester, Tim R., et al. "Role of Mustelids in the Life-cycle of Ixodid Ticks and Transmission Cycles of Four Tick-borne Pathogens." Parasites & Vectors, vol. 11, no. 1, 2018, p. 600.
Hofmeester TR, Krawczyk AI, van Leeuwen AD, et al. Role of mustelids in the life-cycle of ixodid ticks and transmission cycles of four tick-borne pathogens. Parasit Vectors. 2018;11(1):600.
Hofmeester, T. R., Krawczyk, A. I., van Leeuwen, A. D., Fonville, M., Montizaan, M. G. E., van den Berge, K., Gouwy, J., Ruyts, S. C., Verheyen, K., & Sprong, H. (2018). Role of mustelids in the life-cycle of ixodid ticks and transmission cycles of four tick-borne pathogens. Parasites & Vectors, 11(1), 600. https://doi.org/10.1186/s13071-018-3126-8
Hofmeester TR, et al. Role of Mustelids in the Life-cycle of Ixodid Ticks and Transmission Cycles of Four Tick-borne Pathogens. Parasit Vectors. 2018 Nov 20;11(1):600. PubMed PMID: 30458847.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Role of mustelids in the life-cycle of ixodid ticks and transmission cycles of four tick-borne pathogens. AU - Hofmeester,Tim R, AU - Krawczyk,Aleksandra I, AU - van Leeuwen,Arieke Docters, AU - Fonville,Manoj, AU - Montizaan,Margriet G E, AU - van den Berge,Koen, AU - Gouwy,Jan, AU - Ruyts,Sanne C, AU - Verheyen,Kris, AU - Sprong,Hein, Y1 - 2018/11/20/ PY - 2018/04/26/received PY - 2018/09/28/accepted PY - 2018/11/22/entrez PY - 2018/11/22/pubmed PY - 2019/1/4/medline KW - Anaplasma phagocytophilum KW - Borrelia burgdorferi (s.l.) KW - Borrelia miyamotoi KW - Ixodes hexagonus KW - Ixodes ricinus KW - Martes foina KW - Martes martes KW - Meles meles KW - Mustela putorius KW - Neoehrlichia mikurensis SP - 600 EP - 600 JF - Parasites & vectors JO - Parasit Vectors VL - 11 IS - 1 N2 - BACKGROUND: Elucidating which wildlife species significantly contribute to the maintenance of Ixodes ricinus populations and the enzootic cycles of the pathogens they transmit is imperative in understanding the driving forces behind the emergence of tick-borne diseases. Here, we aimed to quantify the relative contribution of four mustelid species in the life-cycles of I. ricinus and Borrelia burgdorferi (sensu lato) in forested areas and to investigate their role in the transmission of other tick-borne pathogens. Road-killed badgers, pine martens, stone martens and polecats were collected in Belgium and the Netherlands. Their organs and feeding ticks were tested for the presence of tick-borne pathogens. RESULTS: Ixodes hexagonus and I. ricinus were found on half of the screened animals (n = 637). Pine martens had the highest I. ricinus burden, whereas polecats had the highest I. hexagonus burden. We detected DNA from B. burgdorferi (s.l.) and Anaplasma phagocytophilum in organs of all four mustelid species (n = 789), and Neoehrlichia mikurensis DNA was detected in all species, except badgers. DNA from B. miyamotoi was not detected in any of the investigated mustelids. From the 15 larvae of I. ricinus feeding on pine martens (n = 44), only one was positive for B. miyamotoi DNA, and all tested negative for B. burgdorferi (s.l.), N. mikurensis and A. phagocytophilum. The two feeding larvae from the investigated polecats (n = 364) and stone martens (n = 39) were negative for all four pathogens. The infection rate of N. mikurensis was higher in feeding nymphs collected from mustelids compared to questing nymphs, but not for B. burgdorferi (s.l.), B. miyamotoi or A. phagocytophilum. CONCLUSIONS: Although all stages of I. ricinus can be found on badgers, polecats, pine and stone martens, their relative contribution to the life-cycle of I. ricinus in forested areas is less than 1%. Consequently, the relative contribution of mustelids to the enzootic cycles of I. ricinus-borne pathogens is negligible, despite the presence of these pathogens in organs and feeding ticks. Interestingly, all four mustelid species carried all stages of I. hexagonus, potentially maintaining enzootic cycles of this tick species apart from the cycle involving hedgehogs as main host species. SN - 1756-3305 UR - https://www.unboundmedicine.com/medline/citation/30458847/Role_of_mustelids_in_the_life_cycle_of_ixodid_ticks_and_transmission_cycles_of_four_tick_borne_pathogens_ DB - PRIME DP - Unbound Medicine ER -