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The Role of Peridomestic Animals in the Eco-Epidemiology of Anaplasma phagocytophilum

  • Environmental Microbiology
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Abstract

Anaplasma phagocytophilum is an important tick-borne zoonotic agent of human granulocytic anaplasmosis (HGA). In Europe, the Ixodes ticks are the main vector responsible for A. phagocytophilum transmission. A wide range of wild animals is involved in the circulation of this pathogen in the environment. Changes in populations of vertebrates living in different ecosystems impact the ecology of ticks and the epidemiology of tick-borne diseases. In this study, we investigated four species, Western European hedgehog (Erinaceus europaeus), northern white-breasted hedgehog (Erinaceus roumanicus), Eurasian red squirrel (Sciurus vulgaris), and the common blackbird (Turdus merula), to describe their role in the circulation of A. phagocytophilum in urban and periurban ecosystems. Ten different tissues were collected from cadavers of the four species, and blood and ear/skin samples from live blackbirds and hedgehogs. Using qPCR, we detected a high rate of A. phagocytophilum: Western European hedgehogs (96.4%), northern white-breasted hedgehogs (92.9%), Eurasian red squirrels (60%), and common blackbirds (33.8%). In the groEL gene, we found nine genotypes belonging to three ecotypes; seven of the genotypes are associated with HGA symptoms. Our findings underline the role of peridomestic animals in the ecology of A. phagocytophilum and indicate that cadavers are an important source of material for monitoring zoonotic pathogens. Concerning the high prevalence rate, all investigated species play an important role in the circulation of A. phagocytophilum in municipal areas; however, hedgehogs present the greatest anaplasmosis risk for humans. Common blackbirds and squirrels carry different A. phagocytophilum variants some of which are responsible for HGA.

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Acknowledgements

The authors would like to thank Maryna Golovchenko and Barbora Černá Bolfíková for the molecular identification in hedgehogs, ornithologists Oldřich Sychra and Petr Veselý and their teams for help with bird trapping, and Jana Kvičerová with the hedgehog trapping and sampling, and to all the volunteers who participated in the cadaver reporting and collection.

Funding

This work was supported by the Czech Science Foundation (grant number 17-16009S). JV was financially supported by the grant CePaViP (CZ.02.1.01/16_019/0000759). HS and MF were financially supported by the Dutch Ministry of Health, Welfare, and Sport (VWS), and by a grant from the European Interreg North Sea Region program as part of the NorthTick project.

Author information

Authors and Affiliations

  1. Department of Pathology and Parasitology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences, Palackého třída 1946/1, Brno, Czech Republic

    Paulina Maria Lesiczka, Lada Hofmannová, Petr Papežík & David Modrý

  2. CEITEC VFU, University of Veterinary and Pharmaceutical Sciences, Palackého třída 1946/1, Brno, Czech Republic

    Paulina Maria Lesiczka, Kristýna Hrazdilová & Ludek Zurek

  3. Faculty of Medicine in Pilsen, Biomedical Center, Charles University, alej Svobody 1655, /76, Plzeň, Czech Republic

    Kristýna Hrazdilová

  4. Department of Parasitology, Faculty of Science, Charles University, Vinicna 7, Prague, Czech Republic

    Karolina Majerová & Jan Votýpka

  5. Biology Centre, Institute of Parasitology, Czech Academy of Sciences, Branišovská, 31, České Budějovice, Czech Republic

    Karolina Majerová, Václav Hönig, Daniel Růžek, Jan Votýpka & David Modrý

  6. Laboratory for Zoonoses and Environmental Microbiology, National Institute for Public Health and Environment (RIVM), Antonie van Leeuwenhoeklaan 9, P.O. Box 1, Bilthoven, The Netherlands

    Manoj Fonville & Hein Sprong

  7. Veterinary Research Institute, Brno, Hudcova, 70, Brno, Czech Republic

    Václav Hönig & Daniel Růžek

  8. Department of Microbiology, Nutrition and Dietetics, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Kamýcka, 129, Prague, Czech Republic, Czech Republic

    Ludek Zurek

  9. Department of Chemistry and Biochemistry, Mendel University, Zemědělská, 1665, Brno, Czech Republic

    Ludek Zurek

  10. Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2, Brno, Czech Republic

    David Modrý

  11. Department of Veterinary Sciences/CINeZ, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Kamýcka, 129, Prague, Czech Republic

    David Modrý

Authors
  1. Paulina Maria Lesiczka
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  2. Kristýna Hrazdilová
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  3. Karolina Majerová
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  4. Manoj Fonville
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  5. Hein Sprong
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  6. Václav Hönig
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  7. Lada Hofmannová
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  8. Petr Papežík
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  9. Daniel Růžek
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  10. Ludek Zurek
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  11. Jan Votýpka
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  12. David Modrý
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Contributions

Conceptualization: David Modrý, Jan Votýpka, Lada Hofmannová. Methodology: David Modrý, Ludek Zurek, Lada Hofmannová, Kristýna Hrazdilová. Formal analysis and investigation: Paulina Maria Lesiczka, Manoj Fonville, Karolina Majerová. Writing—original draft preparation: Paulina Maria Lesiczka, David Modrý. Writing—review and editing: David Modrý, Ludek Zurek, Jan Votýpka, Hein Sprong, Kristýna Hrazdilová. Funding acquisition: David Modrý, Daniel Růžek, Hein Sprong. Resources: David Modrý, Lada Hofmannová, Václav Hönig, Petr Papežík. Supervision: David Modrý

Corresponding author

Correspondence to David Modrý.

Ethics declarations

Ethics Approval

Capture and treatment were performed in agreement with the Czech legislation (Act No 246/1992 Coll.) and protocols (62-2016 UVPS Brno and BC SOS 1520/2017) approved by the responsible authorities of the Czech Republic.

Consent to Participate

Not applicable

Consent for Publication

Not applicable

Conflict of Interest

The authors declare no conflicts of interest.

Supplementary Information

ESM 1

Number of tissues from the four species collected in the Czech Republic and the positivity of the tissue samples for Anaplasma phagocytophilum. (DOCX 14 kb)

ESM 2

Prevalence of Anaplasma phagocytophilum based on results obtained from all organs from the four species from the Czech Republic in relation to sex and age. L, living animals; C, cadavers; n, number of individuals. (DOCX 14 kb)

ESM 3

MLVA results based on five different loci for cadavers and live animals collected in the Czech Republic. Grey indicates positive samples in the analysis; white indicates no effective results. aPositive control. (DOCX 15 kb)

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Lesiczka, P.M., Hrazdilová, K., Majerová, K. et al. The Role of Peridomestic Animals in the Eco-Epidemiology of Anaplasma phagocytophilum. Microb Ecol 82, 602–612 (2021). https://doi.org/10.1007/s00248-021-01704-z

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  • DOI: https://doi.org/10.1007/s00248-021-01704-z

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