Skip to main content

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

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.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. 1.

    Chvostáč M, Špitalská E, Václav R, Vaculová T, Minichová L, Derdáková M (2018) Seasonal patterns in the prevalence and diversity of Tick-Borne Borrelia burgdorferi Sensu Lato, Anaplasma phagocytophilum and Rickettsia spp. in an Urban temperate forest in South Western Slovakia. Int J Environ Res Public Health 15. https://doi.org/10.3390/ijerph15050994

  2. 2.

    Stuen S, Granquist EG, Silaghi C (2013) Anaplasma phagocytophilum-a widespread multi-host pathogen with highly adaptive strategies. Front Cell Infect Microbiol 4:1–33. https://doi.org/10.3389/fcimb.2013.00031

    Article  CAS  Google Scholar 

  3. 3.

    Silaghi C, Skuballa J, Thiel C, Pfister K, Petney T, Pfäffle M, Taraschewski H, Passos LMF (2012) The European hedgehog (Erinaceus europaeus) - a suitable reservoir for variants of Anaplasma phagocytophilum? Ticks Tick Borne Dis 3:49–54. https://doi.org/10.1016/j.ttbdis.2011.11.005

    Article  PubMed  Google Scholar 

  4. 4.

    Matei IA, D’Amico G, Ionicǎ AM et al (2018) New records for Anaplasma phagocytophilum infection in small mammal species. Parasit Vectors 11:1–6. https://doi.org/10.1186/s13071-018-2791-y

    Article  CAS  Google Scholar 

  5. 5.

    Földvári G, Jahfari S, Rigó K et al (2014) Candidatus neoehrlichia mikurensis and anaplasma phagocytophilum in urban hedgehogs. Emerg Infect Dis 20:496–497

    Article  Google Scholar 

  6. 6.

    Jahfari S, Coipan EC, Fonville M, van Leeuwen A, Hengeveld P, Heylen D, Heyman P, van Maanen C, Butler CM, Földvári G, Szekeres S, van Duijvendijk G, Tack W, Rijks JM, van der Giessen J, Takken W, van Wieren SE, Takumi K, Sprong H (2014) Circulation of four Anaplasma phagocytophilum ecotypes in Europe. Parasit Vectors 7:1–11. https://doi.org/10.1186/1756-3305-7-365

    Article  Google Scholar 

  7. 7.

    Jaarsma RI, Sprong H, Takumi K, Kazimirova M, Silaghi C, Mysterud A, Rudolf I, Beck R, Földvári G, Tomassone L, Groenevelt M, Everts RR, Rijks JM, Ecke F, Hörnfeldt B, Modrý D, Majerová K, Votýpka J, Estrada-Peña A (2019) Anaplasma phagocytophilum evolves in geographical and biotic niches of vertebrates and ticks. Parasit Vectors 12:1–17. https://doi.org/10.1186/s13071-019-3583-8

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. 8.

    Svitálková Z, Haruštiaková D, Mahríková L, Berthová L, Slovák M, Kocianová E, Kazimírová M (2015) Anaplasma phagocytophilum prevalence in ticks and rodents in an urban and natural habitat in South-Western Slovakia. Parasit Vectors 8:1–12. https://doi.org/10.1186/s13071-015-0880-8

    Article  Google Scholar 

  9. 9.

    Stuen S (2007) Anaplasma phagocytophilum - the most widespread tick-borne infection in animals in Europe. Vet Res Commun 31:79–84. https://doi.org/10.1007/s11259-007-0071-y

    Article  PubMed  Google Scholar 

  10. 10.

    Víchová B, Majláthová V, Nováková M, Stanko M, Hviščová I, Pangrácová L, Chrudimský T, Čurlík J, Peťko B (2014) Anaplasma infections in ticks and reservoir host from Slovakia. Infect Genet Evol 22:265–272. https://doi.org/10.1016/j.meegid.2013.06.003

    Article  PubMed  CAS  Google Scholar 

  11. 11.

    Baráková I, Derdáková M, Carpi G, Rosso F, Collini M, Tagliapietra V, Ramponi C, Hauffe HC, Rizzoli A (2014) Genetic and ecologic variability among Anaplasma phagocytophilum strains, Northern Italy. Emerg Infect Dis 20:1082–1085. https://doi.org/10.3201/eid2006.131023

    Article  PubMed  PubMed Central  Google Scholar 

  12. 12.

    Battilani M, De Arcangeli S, Balboni A, Dondi F (2017) Genetic diversity and molecular epidemiology of Anaplasma. Infect Genet Evol 49:195–211. https://doi.org/10.1016/j.meegid.2017.01.021

    Article  PubMed  CAS  Google Scholar 

  13. 13.

    Kauffmann M, Rehbein S, Hamel D et al (2017) Anaplasma phagocytophilum and Babesia spp. in roe deer (Capreolus capreolus), fallow deer (Dama dama) and mouflon (Ovis musimon) in Germany. Mol Cell Probes 31:46–54. https://doi.org/10.1016/j.mcp.2016.08.008 Epub 2016 Aug 19. PMID: 27546888

    Article  PubMed  CAS  Google Scholar 

  14. 14.

    Dugat T, Lagrée AC, Maillard R, Boulouis HJ, Haddad N (2015) Opening the black box of Anaplasma phagocytophilum diversity: current situation and future perspectives. Front Cell Infect Microbiol 5:1–18. https://doi.org/10.3389/fcimb.2015.00061

    Article  CAS  Google Scholar 

  15. 15.

    Hamšíková Z, Silaghi C, Takumi K, Rudolf I, Gunár K, Sprong H, Kazimírová M (2019) Presence of roe deer affects the occurrence of anaplasma phagocytophilum ecotypes in questing ixodes ricinus in different habitat types of central Europe. Int J Environ Res Public Health 16. https://doi.org/10.3390/ijerph16234725

  16. 16.

    Heylen D, Lasters R, Adriaensen F, Fonville M, Sprong H, Matthysen E (2019) Ticks and tick-borne diseases in the city: role of landscape connectivity and green space characteristics in a metropolitan area. Sci Total Environ 670:941–949. https://doi.org/10.1016/j.scitotenv.2019.03.235

    Article  PubMed  CAS  Google Scholar 

  17. 17.

    Hasle G (2013) Transport of ixodid ticks and tick-borne pathogens by migratory birds. Front Cell Infect Microbiol 4:1–6. https://doi.org/10.3389/fcimb.2013.00048

    Article  Google Scholar 

  18. 18.

    Rizzoli A, Silaghi C, Obiegala A, Rudolf I, Hubálek ZÄ›, Földvári Gá, Plantard O, Vayssier-Taussat M, Bonnet S, Å pitalská E, Kazimírová Má (2014) Ixodes ricinus and its transmitted pathogens in urban and peri-urban areas in Europe: new hazards and relevance for public health. Front Public Health 2:1–26. https://doi.org/10.3389/fpubh.2014.00251

    Article  Google Scholar 

  19. 19.

    Dziemian S, Sikora B, Piłacińska B, Michalik J, Zwolak R (2015) Ectoparasite loads in sympatric urban populations of the northern white-breasted and the European hedgehog. Parasitol Res 114:2317–2323. https://doi.org/10.1007/s00436-015-4427-x

    Article  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Jokimäki J, Selonen V, Lehikoinen A, Kaisanlahti-Jokimäki ML (2017) The role of urban habitats in the abundance of red squirrels (Sciurus vulgaris, L.) in Finland. Urban For Urban Green 27:100–108. https://doi.org/10.1016/j.ufug.2017.06.021

    Article  Google Scholar 

  21. 21.

    Jahfari S, Ruyts SC, Frazer-Mendelewska E, Jaarsma R, Verheyen K, Sprong H (2017) Melting pot of tick-borne zoonoses: the European hedgehog contributes to the maintenance of various tick-borne diseases in natural cycles urban and suburban areas. Parasit Vectors 10:1–9. https://doi.org/10.1186/s13071-017-2065-0

    Article  Google Scholar 

  22. 22.

    Liz JS, Sumner JW, Pfister K, Brossard M (2002) PCR detection and serological evidence of granulocytic ehrlichial infection in roe deer (Capreolus capreolus) and chamois (Rupicapra rupicapra). J Clin Microbiol 40:892–897. https://doi.org/10.1128/JCM.40.3.892-897.2002

    Article  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Skuballa J, Petney T, Pfäffle M, Oehme R, Hartelt K, Fingerle V, Kimmig P, Taraschewski H (2012) Occurrence of different Borrelia burgdorferi sensu lato genospecies including B. afzelii, B. bavariensis, and B. spielmanii in hedgehogs (Erinaceus spp.) in Europe. Ticks Tick Borne Dis 3:8–13. https://doi.org/10.1016/j.ttbdis.2011.09.008

    Article  PubMed  Google Scholar 

  24. 24.

    Szekeres S, Docters van Leeuwen A, Tóth E, Majoros G, Sprong H, Földvári G (2019) Road-killed mammals provide insight into tick-borne bacterial pathogen communities within urban habitats. Transbound Emerg Dis 66:277–286. https://doi.org/10.1111/tbed.13019

    Article  PubMed  CAS  Google Scholar 

  25. 25.

    Földvári G, Rigó K, Jablonszky M, Biró N, Majoros G, Molnár V, Tóth M (2011) Ticks and the city: ectoparasites of the Northern white-breasted hedgehog (Erinaceus roumanicus) in an urban park. Ticks Tick Borne Dis 2:231–234. https://doi.org/10.1016/j.ttbdis.2011.09.001

    Article  PubMed  Google Scholar 

  26. 26.

    Hasle G, Bjune G, Edvardsen E, Jakobsen C, Linnehol B, Røer JE, Mehl R, Røed KH, Pedersen J, Leinaas HP (2009) Transport of ticks by migratory passerine birds to Norway. J Parasitol 95:1342–1351. https://doi.org/10.1645/GE-2146.1

    Article  PubMed  Google Scholar 

  27. 27.

    Capligina V, Salmane I, Keišs O, Vilks K, Japina K, Baumanis V, Ranka R (2014) Prevalence of tick-borne pathogens in ticks collected from migratory birds in Latvia. Ticks Tick Borne Dis 5:75–81. https://doi.org/10.1016/j.ttbdis.2013.08.007

    Article  PubMed  Google Scholar 

  28. 28.

    Heylen D, Fonville M, Docters Van Leeuwen A et al (2017) Pathogen communities of songbird-derived ticks in Europe’s low countries. Parasit Vectors 10:1–12. https://doi.org/10.1186/s13071-017-2423-y

    Article  CAS  Google Scholar 

  29. 29.

    Šťastný K, Hudec K (2011) Ptáci 3/I. Academia, II Fauna. ČR

    Google Scholar 

  30. 30.

    Wilson DE, Mittermeier RA, Ruff S, et al (2016) Handbook of the Mammals of the World: Lagomorphs and Rodents I

  31. 31.

    Wilson DE, Mittermeier RA, Ruff S et al (2018) Handbook of the Mammals of the World: Insectivores, sloths and colungos. Lynx

  32. 32.

    Alberti A, Zobba R, Chessa B, Addis MF, Sparagano O, Pinna Parpaglia ML, Cubeddu T, Pintori G, Pittau M (2005) Equine and canine Anaplasma phagocytophilum strains isolated on the island of Sardinia (Italy) are phylogenetically related to pathogenic strains from the United States. Appl Environ Microbiol 71:6418–6422. https://doi.org/10.1128/AEM.71.10.6418-6422.2005

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. 33.

    Liz JS (2002) Ehrlichiosis in Ixodes ricinus and wild mammals. Int J Med Microbiol 291(Suppl):104–105

    Article  Google Scholar 

  34. 34.

    Glez-Peña D, Gómez-Blanco D, Reboiro-Jato M et al (2010) ALTER: program-oriented conversion of DNA and protein alignments. Nucleic Acids Res 38:14–18. https://doi.org/10.1093/nar/gkq321

    Article  CAS  Google Scholar 

  35. 35.

    Katoh K, Rozewicki J, Yamada KD MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization [published online ahead of print September 6, 2017]. Br Bioinform

  36. 36.

    Dugat T, Chastagner A, Lagrée AC, Petit E, Durand B, Thierry S, Corbière F, Verheyden H, Chabanne L, Bailly X, Leblond A, Vourc’h G, Boulouis HJ, Maillard R, Haddad N (2014) A new multiple-locus variable-number tandem repeat analysis reveals different clusters for Anaplasma phagocytophilum circulating in domestic and wild ruminants. Parasit Vectors 7:1–11. https://doi.org/10.1186/1756-3305-7-439

    Article  Google Scholar 

  37. 37.

    Blazejak K, Janecek E, Strube C (2017) A 10-year surveillance of Rickettsiales (Rickettsia spp. and Anaplasma phagocytophilum) in the city of Hanover, Germany, reveals Rickettsia spp. as emerging pathogens in ticks. Parasit Vectors 10:1–10. https://doi.org/10.1186/s13071-017-2537-2

    Article  CAS  Google Scholar 

  38. 38.

    Huhn C, Winter C, Wolfsperger T, Wüppenhorst N, Strašek Smrdel K, Skuballa J, Pfäffle M, Petney T, Silaghi C, Dyachenko V, Pantchev N, Straubinger RK, Schaarschmidt-Kiener D, Ganter M, Aardema ML, von Loewenich FD (2014) Analysis of the population structure of Anaplasma phagocytophilum using multilocus sequence typing. PLoS One 9:e93725. https://doi.org/10.1371/journal.pone.0093725

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. 39.

    Grochowska A, Milewski R, Pancewicz S, Dunaj J, Czupryna P, Milewska AJ, Róg-Makal M, Grygorczuk S, Moniuszko-Malinowska A (2020) Comparison of tick-borne pathogen prevalence in Ixodes ricinus ticks collected in urban areas of Europe. Sci Rep 10:1–9. https://doi.org/10.1038/s41598-020-63883-y

    Article  CAS  Google Scholar 

  40. 40.

    Pfäffle M, Petney T, Skuballa J, Taraschewski H (2011) Comparative population dynamics of a generalist (Ixodes ricinus) and specialist tick (I. hexagonus) species from European hedgehogs. Exp Appl Acarol 54:151–164. https://doi.org/10.1007/s10493-011-9432-x

    Article  PubMed  Google Scholar 

  41. 41.

    Norte AC, Margos G, Becker NS, Albino Ramos J, Núncio MS, Fingerle V, Araújo PM, Adamík P, Alivizatos H, Barba E, Barrientos R, Cauchard L, Csörgő T, Diakou A, Dingemanse NJ, Doligez B, Dubiec A, Eeva T, Flaisz B, Grim T, Hau M, Heylen D, Hornok S, Kazantzidis S, Kováts D, Krause F, Literak I, Mänd R, Mentesana L, Morinay J, Mutanen M, Neto JM, Nováková M, Sanz JJ, Pascoal da Silva L, Sprong H, Tirri IS, Török J, Trilar T, Tyller Z, Visser ME, Lopes de Carvalho I (2020) Host dispersal shapes the population structure of a tick-borne bacterial pathogen. Mol Ecol 29:485–501. https://doi.org/10.1111/mec.15336

    Article  PubMed  Google Scholar 

  42. 42.

    Aronson MFJ, Lepczyk CA, Evans KL, et al (2017) Biodiversity in the city: key challenges for urban green space management. In: Front. Ecol. Environ. https://esajournals.onlinelibrary.wiley.com/doi/epdf/10.1002/fee.1480. Accessed 5 Aug 2020

  43. 43.

    Santos AS, de Bruin A, Veloso AR, Marques C, Pereira da Fonseca I, de Sousa R, Sprong H, Santos-Silva MM (2018) Detection of Anaplasma phagocytophilum, Candidatus Neoehrlichia sp., Coxiella burnetii and Rickettsia spp. in questing ticks from a recreational park, Portugal. Ticks Tick Borne Dis 9:1555–1564. https://doi.org/10.1016/j.ttbdis.2018.07.010

    Article  PubMed  Google Scholar 

  44. 44.

    Hoffman T, Wilhelmsson P, Barboutis C, Fransson T, Jaenson TGT, Lindgren PE, von Loewenich FD, Lundkvist Å, Olsen B, Salaneck E (2020) A divergent Anaplasma phagocytophilum variant in an Ixodes tick from a migratory bird; Mediterranean basin. Infect Ecol Epidemiol 10. https://doi.org/10.1080/20008686.2020.1729653

  45. 45.

    Rézouki C, Dozières A, Le Coeur C et al (2014) A viable population of the European red squirrel in an urban park. PLoS One 9:1–7. https://doi.org/10.1371/journal.pone.0105111

    Article  CAS  Google Scholar 

  46. 46.

    Krawczyk AI, Van Leeuwen AD, Jacobs-Reitsma W et al (2015) Presence of zoonotic agents in engorged ticks and hedgehog faeces from Erinaceus europaeus in (sub) urban areas. Parasit Vectors 8:210. https://doi.org/10.1186/s13071-015-0814-5

    Article  PubMed  PubMed Central  Google Scholar 

  47. 47.

    Skuballa J, Petney T, Pfäffle M, Taraschewski H (2010) Molecular detection of Anaplasma phagocytophilum in the European hedgehog (Erinaceus europaeus) and its ticks. Vector-Borne Zoonotic Dis 10:1055–1057. https://doi.org/10.1089/vbz.2009.0150

    Article  PubMed  Google Scholar 

  48. 48.

    Mysterud A, Stigum VM, Jaarsma RI, Sprong H (2019) Genospecies of Borrelia burgdorferi sensu lato detected in 16 mammal species and questing ticks from northern Europe. Sci Rep 9. https://doi.org/10.1038/s41598-019-41686-0

  49. 49.

    von Loewenich FD, Seckert C, Dauber E et al (2020) Prosthetic valve endocarditis with Bartonella washoensis in a human European patient and its detection in red squirrels (Sciurus vulgaris). J Clin Microbiol 58. https://doi.org/10.1128/JCM.01404-19

  50. 50.

    Honig V, Carolan HE, Vavruskova Z, Massire C, Mosel MR, Crowder CD, Rounds MA, Ecker DJ, Ruzek D, Grubhoffer L, Luft BJ, Eshoo MW (2017) Broad-range survey of vector-borne pathogens and tick host identification of Ixodes ricinus from Southern Czech Republic. FEMS Microbiol Ecol 93:1–13. https://doi.org/10.1093/femsec/fix129

    Article  CAS  Google Scholar 

  51. 51.

    Buczek AM, Buczek W, Buczek A, Bartosik K (2020) The potential role of migratory birds in the rapid spread of ticks and tick-borne pathogens in the changing climatic and environmental conditions in europe. Int J Environ Res Public Health 17. https://doi.org/10.3390/ijerph17062117

  52. 52.

    Matei IA, Estrada-Peña A, Cutler SJ, Vayssier-Taussat M, Varela-Castro L, Potkonjak A, Zeller H, Mihalca AD (2019) A review on the eco-epidemiology and clinical management of human granulocytic anaplasmosis and its agent in Europe. Parasit Vectors 12:599

    Article  Google Scholar 

  53. 53.

    Dondi F, Russo S, Agnoli C, Mengoli N, Balboni A, Alberti A, Battilani M (2014) Clinicopathological and molecular findings in a case of canine Anaplasma phagocytophilum infection in Northern Italy. Sci World J 2014:1–6. https://doi.org/10.1155/2014/810587

    Article  CAS  Google Scholar 

  54. 54.

    Smrdel KS, Serdt M, Duh D, Knap N, Županc T (2010) Anaplasma phagocytophilum in ticks in Slovenia. Parasit Vectors 3:1–5. https://doi.org/10.1186/1756-3305-3-102

    Article  CAS  Google Scholar 

  55. 55.

    Klitgaard K, Kjær LJ, Isbrand A, Hansen MF, Bødker R (2019) Multiple infections in questing nymphs and adult female Ixodes ricinus ticks collected in a recreational forest in Denmark. Ticks Tick Borne Dis 10:1060–1065. https://doi.org/10.1016/j.ttbdis.2019.05.016

    Article  PubMed  Google Scholar 

  56. 56.

    Margos G (2012) Population, genetics, taxonomy and phylogeny borrelia burgdorrferi 2011:1545–1563. https://doi.org/10.1016/j.meegid.2011.07.022.Population

  57. 57.

    Mukhacheva TA, Shaikhova DR, Kovalev SY (2019) Asian isolates of Anaplasma phagocytophilum: multilocus sequence typing. Ticks Tick Borne Dis 10:775–780. https://doi.org/10.1016/j.ttbdis.2019.03.011

    Article  PubMed  Google Scholar 

  58. 58.

    Mukhacheva TA, Shaikhova DR, Kovalev SY, von Loewenich FD (2020) Phylogeographical diversity of Anaplasma phagocytophilum in the Asian part of Russia based on multilocus sequence typing and analysis of the ankA gene. Infect Genet Evol 80:104234. https://doi.org/10.1016/j.meegid.2020.104234

    Article  PubMed  CAS  Google Scholar 

Download references

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

Affiliations

Authors

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)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

Keywords

  • Tick-borne diseases
  • HGA
  • Urban wildlife
  • Hedgehog
  • Squirrel
  • Blackbird