Parasitology Research

, Volume 110, Issue 4, pp 1525–1530 | Cite as

Longitudinal field study on bovine Babesia spp. and Anaplasma phagocytophilum infections during a grazing season in Belgium

  • Laetitia LempereurEmail author
  • Maude Lebrun
  • Pascale Cuvelier
  • Géraldine Sépult
  • Yannick Caron
  • Claude Saegerman
  • Brian Shiels
  • Bertrand Losson
Original Paper


Anaplasmosis and babesiosis are major tick-borne diseases with a high economic impact but are also a public health concern. Blood samples collected in the spring, summer, and autumn of 2010 from 65 cows in seven different farms in Belgium were monitored with an indirect immunofluorescence antibody test to assess seroprevalence against these pathogens. Seroprevalences to Babesia spp. were measured as 10.7%, 20%, and 12.3% in spring, summer, and autumn, respectively, whereas seroprevalences to Anaplasma phagocytophilum were 30.8%, 77%, and 56.9%, respectively. A total of 805 Ixodes ricinus ticks were collected at the same time from both cattle (feeding ticks) and grazed pastures (questing ticks). The infection level of ticks, assessed by PCR assay, for Babesia spp. DNA was 14.6% and 7.9% in feeding and questing ticks, respectively, whereas 21.7% and 3% of feeding and questing ticks were found be positive for A. phagocytophilum cDNA. Fifty-five PCR-positive samples were identified by sequencing as Babesia sp. EU1, of which five from feeding ticks were positive for both A. phagocytophilum and Babesia sp. EU1. The high density of wild cervids in the study area could explain these observations, as deer are considered to be the main hosts for adults of I. ricinus. However, the absence of Babesia divergens both in feeding and questing ticks is surprising, as the study area is known to be endemic for cattle babesiosis. Increasing cervid populations and comorbidity could play an import role in the epidemiology of these tick-borne diseases.


Babesia Polymerase Chain Reaction Test Babesiosis Wild Ruminant Anaplasma Phagocytophilum 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Laetitia Lempereur is an early-stage researcher supported by the POSTICK ITN (postgraduate training network for capacity building to control ticks and tick-borne diseases) within the FP7–PEOPLE—ITN program (EU Grant No. 238511). The authors are very grateful to the veterinarians and farmers involved in this survey for the sample collections. The authors would like to thank Dr. Christian Quinet and Ir Cédric Mullender for their scientific support and their supervision and Françoise Maréchal for her technical support.


  1. Adam KM, Blewett DA, Brocklesby DW, Sharman GA (1976) The isolation and characterization of a Babesia from red deer (Cervus elaphus). Parasitology 73:1–11PubMedCrossRefGoogle Scholar
  2. Amusategui I, Sainz A, Tesouro MA (2006) Serological evaluation of Anaplasma phagocytophilum infection in livestock in northwestern Spain. Ann N Y Acad Sci 1078:487–490PubMedCrossRefGoogle Scholar
  3. Arthur DR (1963) British ticks. Butterworth, LondonGoogle Scholar
  4. Bakken JS, Dumler S (2008) Human granulocytic anaplasmosis. Infect Dis Clin North Am 22:433–448, viiiPubMedCrossRefGoogle Scholar
  5. Baumgarten BU, Rollinghoff M, Bogdan C (1999) Prevalence of Borrelia burgdorferi and granulocytic and monocytic ehrlichiae in Ixodes ricinus ticks from southern Germany. J Clin Microbiol 37:3448–3451PubMedGoogle Scholar
  6. Becker CA, Bouju-Albert A, Jouglin M, Chauvin A, Malandrin L (2009) Natural transmission of zoonotic Babesia spp. by Ixodes ricinus ticks. Emerg Infect Dis 15:320–322PubMedCrossRefGoogle Scholar
  7. Bonnet S, Brisseau N, Hermouet A, Jouglin M, Chauvin A (2009) Experimental in vitro transmission of Babesia sp. (EU1) by Ixodes ricinus. Vet Res 40:21PubMedCrossRefGoogle Scholar
  8. Boom R, Sol CJ, Salimans MM, Jansen CL, Wertheim-van Dillen PM, van der Noordaa J (1990) Rapid and simple method for purification of nucleic acids. J Clin Microbiol 28:495–503PubMedGoogle Scholar
  9. Bram RA (1978) Surveillance and collection of arthropods of veterinary importance. Agric Handb 518:108–109Google Scholar
  10. Casati S, Sager H, Gern L, Piffaretti JC (2006) Presence of potentially pathogenic Babesia sp. for human in Ixodes ricinus in Switzerland. Ann Agric Environ Med 13:65–70PubMedGoogle Scholar
  11. de la Fuente J, Massung RF, Wong SJ, Chu FK, Lutz H, Meli M, von Loewenich FD, Grzeszczuk A, Torina A, Caracappa S, Mangold AJ, Naranjo V, Stuen S, Kocan KM (2005a) Sequence analysis of the msp4 gene of Anaplasma phagocytophilum strains. J Clin Microbiol 43:1309–1317PubMedCrossRefGoogle Scholar
  12. de la Fuente J, Naranjo V, Ruiz-Fons F, Hofle U, Fernandez De Mera IG, Villanua D, Almazan C, Torina A, Caracappa S, Kocan KM, Gortazar C (2005b) Potential vertebrate reservoir hosts and invertebrate vectors of Anaplasma marginale and A. phagocytophilum in central Spain. Vector Borne Zoonotic Dis 5:390–401CrossRefGoogle Scholar
  13. Duh D, Petrovec M, Bidovec A, Avsic-Zupanc T (2005) Cervids as Babesiae hosts, Slovenia. Emerg Infect Dis 11:1121–1123PubMedGoogle Scholar
  14. Ebani V, Cerri D, Fratini F, Ampola M, Andreani E (2008) Seroprevalence of Anaplasma phagocytophilum in domestic and wild animals from central Italy. New Microbiol 31:371–375PubMedGoogle Scholar
  15. Ginsberg HS (2008) Potential effects of mixed infections in ticks on transmission dynamics of pathogens: comparative analysis of published records. Exp Appl Acarol 46:29–41PubMedCrossRefGoogle Scholar
  16. Granquist EG, Bardsen K, Bergstrom K, Stuen S (2010) Variant -and individual dependent nature of persistent Anaplasma phagocytophilum infection. Acta Vet Scand 52:25PubMedCrossRefGoogle Scholar
  17. Gray JS, Kaye B (1991) Studies on the use of gerbil-derived Babesia divergens antigen for diagnosis of bovine babesiosis. Vet Parasitol 39:215–224PubMedCrossRefGoogle Scholar
  18. Gray JS, Murphy TM, Taylor SM, Blewett DA, Harrington R (1990) Comparative morphological and cross transmission studies with bovine and deer babesias in Ireland. Prev Vet Med 9:193CrossRefGoogle Scholar
  19. Guyot H, Ramery E, O'Gradyc L, Sandersen C, Rollin F (2011) Emergence of bovine ehrlichiosis in Belgian cattle herds. Ticks Tick Borne Dis 2:116–118PubMedCrossRefGoogle Scholar
  20. Halos L, Bord S, Cotte V, Gasqui P, Abrial D, Barnouin J, Boulouis HJ, Vayssier-Taussat M, Vourc'h G (2010) Ecological factors characterizing the prevalence of bacterial tick-borne pathogens in Ixodes ricinus ticks in pastures and woodlands. Appl Environ Microbiol 76:4413–4420PubMedCrossRefGoogle Scholar
  21. Herwaldt BL, Caccio S, Gherlinzoni F, Aspock H, Slemenda SB, Piccaluga P, Martinelli G, Edelhofer R, Hollenstein U, Poletti G, Pampiglione S, Loschenberger K, Tura S, Pieniazek NJ (2003) Molecular characterization of a non-Babesia divergens organism causing zoonotic babesiosis in Europe. Emerg Infect Dis 9:942–948PubMedGoogle Scholar
  22. Lempereur L, De Cat A, Caron Y, Madder M, Claerebout E, Saegerman C, Losson B (2011) First molecular evidence of potentially zoonotic Babesia microti and Babesia sp. EU1 in Ixodes ricinus ticks in Belgium. Vector Borne Zoonotic Dis 11:125–130PubMedCrossRefGoogle Scholar
  23. Losson B, Lefevre F (1989) La babesiose bovine en Belgique. Une enquête sérologique en zone d'endémie. Ann Med Vet 133:421–426Google Scholar
  24. Malandrin L, Jouglin M, Sun Y, Brisseau N, Chauvin A (2010) Redescription of Babesia capreoli (Enigk and Friedhoff, 1962) from roe deer (Capreolus capreolus): isolation, cultivation, host specificity, molecular characterisation and differentiation from Babesia divergens. Int J Parasitol 40:277–284PubMedCrossRefGoogle Scholar
  25. Pusterla N, Braun U (1997) Clinical findings in cows after experimental infection with Ehrlichia phagocytophila. Zentralbl Veterinarmed A 44:385–390PubMedGoogle Scholar
  26. Pusterla N, Pusterla JB, Braun U, Lutz H (1998) Serological, hematologic, and PCR studies of cattle in an area of Switzerland in which tick-borne fever (caused by Ehrlichia phagocytophila) is endemic. Clin Diagn Lab Immunol 5:325–327PubMedGoogle Scholar
  27. Rosef O, Paulauskas A, Radzijevskaja J (2009) Prevalence of Borrelia burgdorferi sensu lato and Anaplasma phagocytophilum in questing Ixodes ricinus ticks in relation to the density of wild cervids. Acta Vet Scand 51:47PubMedCrossRefGoogle Scholar
  28. Saegerman C, Claerebout E, Kalume M, Losson B (2007) Bovine babesiosis in Belgium: preliminary results of postal survey of veterinarians in 2006. Renc Rech Rumin 14:220Google Scholar
  29. SPW—DGO3 Agriculture-Ressources naturelles et Environnement-Département de la Nature et des Forêts, F.c. 2011. Report of Wild ruminants evolution in BelgiumGoogle Scholar
  30. Telfer S, Lambin X, Birtles R, Beldomenico P, Burthe S, Paterson S, Begon M (2010) Species interactions in a parasite community drive infection risk in a wildlife population. Science 330:243–246PubMedCrossRefGoogle Scholar
  31. Thomas RJ, Dumler JS, Carlyon JA (2009) Current management of human granulocytic anaplasmosis, human monocytic ehrlichiosis and Ehrlichia ewingii ehrlichiosis. Expert Rev Anti Infect Ther 7:709–722PubMedCrossRefGoogle Scholar
  32. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedCrossRefGoogle Scholar
  33. Woldehiwet Z (2006) Anaplasma phagocytophilum in ruminants in Europe. Ann N Y Acad Sci 1078:446–460PubMedCrossRefGoogle Scholar
  34. Zintl A, Mulcahy G, Skerrett HE, Taylor SM, Gray JS (2003) Babesia divergens, a bovine blood parasite of veterinary and zoonotic importance. Clin Microbiol Rev 16:622–636PubMedCrossRefGoogle Scholar
  35. Zintl A, Finnerty EJ, Murphy TM, de Waal T, Gray JS (2011) Babesias of red deer (Cervus elaphus) in Ireland. Vet Res 42:7PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Laetitia Lempereur
    • 1
    • 4
    Email author
  • Maude Lebrun
    • 2
  • Pascale Cuvelier
    • 2
  • Géraldine Sépult
    • 2
  • Yannick Caron
    • 1
  • Claude Saegerman
    • 3
  • Brian Shiels
    • 4
  • Bertrand Losson
    • 1
  1. 1.Laboratory of Parasitology and Parasitic Diseases, Department of Infectious and Parasitic Diseases, Faculty of Veterinary MedicineUniversity of LiègeLiègeBelgium
  2. 2.Laboratory Animal Health Department of the Regional Association of Animal Health and Identification (ARSIA)CineyBelgium
  3. 3.Research Unit in Epidemiology and Risk Analysis Applied to the Veterinary Sciences (UREAR), Department of Infectious and Parasitic Diseases, Faculty of Veterinary MedicineUniversity of LiègeLiègeBelgium
  4. 4.Institute of Infection, Immunity & Inflammation, College of Medical, Veterinary & Life SciencesUniversity of GlasgowGlasgowUK

Personalised recommendations