Short Communication
Severe Anaplasma phagocytophilum and Babesia divergens concomitant infection in imported captive reindeer (Rangifer tarandus)
Lola Romanos ,
Renaud Pierre Maillard *

Mac Vet Rev 2020; 43 (2): 185 - 191

10.2478/macvetrev-2020-0023

Received: 04 February 2020

Received in revised form: 18 June 2020

Accepted: 14 July 2020

Available Online First: 13 August 2020

Published on: 15 October 2020

Correspondence: Renaud Pierre Maillard, renaud.maillard@envt.fr
PDF HTML

Abstract

Tick-borne diseases are highly prevalent in domestic and wild ruminants and they may be distributed in wide geographical ranges by animal transportation. The aim of the current study was to investigate the presence of European strains of Babesia spp. and/or Anaplasma spp. in oversea imported reindeer specimens. Imported specimens (n=7) were hospitalized with visible tick infestation (Ixodes ricinus) and signs of cachexia, anemia, and hemoglobinuria. Using blood smears, PCR, and BLAST comparisons, it was confirmed that the animals were infected with a French strain of Anaplasma phagocytophilum and Babesia divergens which is considered to be absent in the USA. We conclude that oversea importation of reindeers must be followed with a routine check for geographically-specific strains of pathogens from the place of origin. This monitoring process must be dynamic and according to recent reports of tick-borne pathogens.

Keywords: Anaplasma, Babesia, Ixodes ricinus, reindeer

References

  1. Stoffregen, W.C., Alt, D.P., Olsen, S.C., Waters, S.C., Stasko, J.A. (2006). Identification of a haemoplasma species in anemic reindeer (Rangifer tarandus). J Wildl Dis. 42(2): 249-258. https://doi.org/10.7589/0090-3558-42.2.249 PMid:16870847
  2. Stuen, S. (2007). Anaplasma phagocytophilum - the most widespread tick-borne infection in animals in Europe. Vet Res Commun. 31 (Suppl. 1): 79-84. https://doi.org/10.1007/s11259-007-0071-y PMid:17682851
  3. Bastian, S., Jouglin, M., Brisseau, N., Malandrin, L., Klegou, G., L'Hostis, M., Chauvin, A. (2012). Antibody prevalence and molecular identification of Babesia spp. in roe deer in France. J Wildl Dis. 48(2): 416-424. https://doi.org/10.7589/0090-3558-48.2.416 PMid:22493116   
  4. Becker, C.A., Bouju-Albert, A., Jouglin, M., Chauvin, A., Malandrin, L. (2009). Natural transmission of zoonotic Babesia spp. by Ixodes ricinus ticks. Emerg Infect Dis. 15(2): 320-322. https://doi.org/10.3201/eid1502.081247 PMid:19193284 PMCid:PMC2657642 
  5. Hilpertshauser, H., Deplazes, P., Schnyder, M., Gern, L., Mathis, A. (2006). Babesia spp. identified by PCR in ticks collected from domestic and wild ruminants in southern Switzerland. Appl Environ Microbiol. 72(10): 6503-6507. https://doi.org/10.1128/AEM.00823-06 PMid:17021198 PMCid:PMC1610307             
  6. Asman, M., Nowak, M., Cuber, P., Strzelczyk, J., Szilman, E., Szilman, P., Trapp, G., Siuda, K., Solarz, K., Wiczkowski, A. (2013). The risk of exposure to Anaplasma phagocytophilum, Borrelia burgdorferi sensu lato, Babesia sp. and co-infections in Ixodes ricinus ticks on the territory of Niepołomice forest (southern Poland). Ann Parasitol. 59(1): 13-19.     
  7. Langton, C., Gray, J.S., Waters, P.F., Holman, P.J. (2003). Naturally acquired babesiosis in a reindeer (Rangifer tarandus tarandus) herd in Great Britain. Parasitol Res. 89(3): 194-198. https://doi.org/10.1007/s00436-002-0737-x PMid:12541061     
  8. Kik, M., Nijhof, A.M., Balk, J.A., Jongejan, F. (2011). Babesia sp. EU1 infection in a forest reindeer, The Netherlands. Emerg Infect Dis. 17(5): 936-938. https://doi.org/10.3201/eid1705.101834 PMid:21529420 PMCid:PMC3321791    
  9. Wiegmann, L., Silaghi, C., Obiegala, A., Karnath, C., Langer, S., Ternes, K., Kämmerling, J., Osmann, C., Pfeffer, M. (2015). Occurrence of Babesia species in captive reindeer (Rangifer tarandus) in Germany. Vet Parasitol. 211(1-2): 16-22. https://doi.org/10.1016/j.vetpar.2015.04.026 PMid:25986326     
  10. Haigh, J.C., Gerwing, V., Erdenebaatar, J., Hill, J.E. (2008). A novel clinical syndrome and detection of Anaplasma ovis in Mongolian reindeer (Rangifer tarandus). J Wildl Dis. 44(3): 569-577. https://doi.org/10.7589/0090-3558-44.3.569 PMid:18689641   
  11. Stuen, S. (1996). Experimental tick-borne fever infection in reindeer (Rangifer tarandus tarandus). Vet Rec. 138(24): 595-596. https://doi.org/10.1136/vr.138.24.595 PMid:8799988    
  12. Sánchez Romano, J., Grund, L., Obiegala, A., Nymo, I.H., Ancin-Murguzur, F.J., Li, H., Król, N., Pfeffer, M., Tryland, M. (2019). A multi-pathogen screening of captive reindeer (Rangifer tarandus) in Germany based on serological and molecular assays. Front Vet Sci. 6, 461. https://doi.org/10.3389/fvets.2019.00461 PMid:31921918 PMCid:PMC6933772
  13. Miller, A.L., Evans, A.L., Os, Ø., Arnemo, J.M. (2013). Biochemical and hematologic reference values for free-ranging, chemically immobilized wild norwegian reindeer (Rangifer tarandus tarandus) during early winter. J Wildl Dis. 49(2): 221-228. https://doi.org/10.7589/2012-04-115 PMid:23568897           
  14. Laloy, E., Petit, E., Boulouis, H.J., Gandoin, C., Bouillin, C., Gounot, G., Bonnet, S., Maillard, R. (2009). Dynamics of natural infection by Anaplasma phagocytophilum in a dairy cattle herd in Brittany, France. Clin Microbiol Infect. 15 (Suppl 2): 24-25. https://doi.org/10.1111/j.1469-0691.2008.02142.x PMid:19298405
  15. Laloy, E., Petit, E., Boulouis, H.J., Lacroux, C., Corbiere, F., Schelcher, F., Bonnet, S., Maillard, R. (2009). First detection of Anaplasma phagocytophilum-like DNA in the French lizard Rupricapra pyrenaica. Clin Microbiol Infect. 15 (Suppl 2): 26-27. https://doi.org/10.1111/j.1469-0691.2008.02143.x PMid:19298404
  16. 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(2): 125-130. https://doi.org/10.1089/vbz.2009.0189 PMid:20575647
  17. Andersson, M.O., Víchová, B., Tolf, C., Krzyzanowska, S., Waldenström, J., Karlsson, M.E. (2017). Co-infection with Babesia divergens and Anaplasma phagocytophilum in cattle (Bos taurus), Sweden. Ticks Tick Borne Dis. 8(6): 933-935. https://doi.org/10.1016/j.ttbdis.2017.08.005 PMid:28869191       
  18. Mathieu, A., Pastor, A.R., Berkvens, C.N., Gara-Boivin, C., Hébert, M., Léveillé, A.N., Barta, J.R., Smith, D.A. (2018). Babesia odocoilei as a cause of mortality in captive cervids in Canada. Can Vet J. 59(1): 52-58.       
  19. Bartlett, S.L., Abou-Madi, N., Messick, J.B., Birkenheuer, A. Kollias, G.V. (2009). Diagnosis and treatment of Babesia odocoilei in captive reindeer (Rangifer tarandus tarandus) and recognition of three novel host species. J Zoo Wildl Med. 40(1): 152-159. https://doi.org/10.1638/2008-0011.1 PMid:19368255
  20. Holman, P.J., Swift, P.K., Frey, R.E., Bennett, J., Cruz, D. Wagner, G.G. (2002). Genotypically unique Babesia spp. isolated from reindeer (Rangifer tarandus tarandus) in the United States. Parasitol Res. 88(5): 405-411. https://doi.org/10.1007/s00436-001-0576-1 PMid:12049456     
  21. Herwaldt, B.L., de Bruyn, G., Pieniazek, N.J., Homer, M., Lofy, K.H., Slemenda, S.B., Fritsche, T.R., Persing, D.H. Limaye, A.P. (2004). Babesia divergens-like infection, Washington State. Emerg Infect Dis. 10(4): 622-629. https://doi.org/10.3201/eid1004.030377 PMid:15200851 PMCid:PMC3323086
  22. Holman, P.J., Spencer, A.M., Telford, S.R 3rd, Goethert, H.K., Allen, A.J., Knowles, D.P., Goff, W.L. (2005). Comparative infectivity of Babesia divergens and a zoonotic Babesia divergens-like parasite in cattle. Am J Trop Med. 73(5): 865-870. https://doi.org/10.4269/ajtmh.2005.73.865 PMid:16282295            
  23. Herc, E., Pritt, B., Huizenga, T., Douce, R., Hysell, M., Newton, D., Sidge, J., Losman, E., Sherbeck, J., Kaul, D.R. (2018). Probable locally acquired Babesia divergens-like infection in Woman, Michigan, USA. Emerg Infect Dis. 24(8): 1558-1560. https://doi.org/10.3201/eid2408.180309 PMid:30016254 PMCid:PMC6056127    
  24. Duh, D., Petrovec, M., Avsic-Zupanc, T. (2001). Diversity of Babesia Infecting European sheep ticks (Ixodes ricinus). J Clin Microbiol. 39(9): 3395-3397. https://doi.org/10.1128/JCM.39.9.3395-3397.2001 PMid:11526189 PMCid:PMC88357        
  25. Bonnet, S., Jouglin, M., L'Hostis, M., Chauvin, A. (2007). Babesia sp. EU1 from roe deer and transmission within Ixodes ricinus. Emerg Infect Dis. 13(8): 1208-1210. https://doi.org/10.3201/eid1308.061560 PMid:17953093 PMCid:PMC2828078    
  26. Duh, D., Petrovec, M., Bidovec, A., Avsic-Zupanc, T. (2005). Cervids as Babesiae hosts, Slovenia. Emerg Infect Dis. 11(7): 1121-1123. https://doi.org/10.3201/eid1107.040724 PMid:16022795 PMCid:PMC3371785    
  27. Duh, D., Petrovec, M., Avsic-Zupanc, T. (2005). Molecular characterization of human pathogen Babesia EU1 in Ixodes ricinus ticks from Slovenia. J Parasitol. 91(2): 463-465. https://doi.org/10.1645/GE-394R PMid:15986627
  28. Zintl, A., Finnerty, E.J., Murphy, T.M., de Waal, T., Gray, J.S. (2011). Babesias of red deer (Cervus elaphus) in Ireland. Vet Res. 42(1): 7. https://doi.org/10.1186/1297-9716-42-7 PMid:21314977 PMCid:PMC3037898    
  29. 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(3): 277-284. https://doi.org/10.1016/j.ijpara.2009.08.008 PMid:19733572   
  30. Cabezas-Cruz, A., Gallois, M., Fontugne, M., Allain, E., Denoual, M., Moutailler, S., Devillers, E., Zientara, S., Memmi, M., Chauvin, A., Agoulon, A., Vayssier-Taussat, M., Chartier, C. (2019). Epidemiology and genetic diversity of Anaplasma ovis in goats in Corsica, France. Parasit Vectors 12(1): 3. https://doi.org/10.1186/s13071-018-3269-7 PMid:30606253 PMCid:PMC6318933         
  31. Woldehiwet, Z. (2010). The natural history of Anaplasma phagocytophilum. Vet Parasitol. 167(2-4): 108-122. https://doi.org/10.1016/j.vetpar.2009.09.013 PMid:19811878       
  32. Blanco, J.R., Oteo, J.A. (2002). Human granulocytic ehrlichiosis in Europe. Clin Microbiol Infect. 8(12): 763-772. https://doi.org/10.1046/j.1469-0691.2002.00557.x PMid:12519349    
  33. Oines, O., Radzijevskaja, J., Paulauskas, A., Rosef, O. (2012). Prevalence and diversity of Babesia spp. in questing Ixodes ricinus ticks from Norway. Parasit Vectors. 5, 156. https://doi.org/10.1186/1756-3305-5-156 PMid:22862883 PMCid:PMC3439691       
  34. Silaghi, C., Woll, D., Hamel, D., Pfister, K., Mahling, M., Pfeffer, M. (2012). Babesia spp. and Anaplasma phagocytophilum in questing ticks, ticks parasitizing rodents and the parasitized rodents - Analyzing the host-pathogen-vector interface in a metropolitan area. Parasit Vectors. 5, 191. https://doi.org/10.1186/1756-3305-5-191 PMid:22950642 PMCid:PMC3480827
  35. Lempereur, L., Lebrun, M., Cuvelier, P., Sépult, G., Caron, Y., Saegerman, C., Shiels, B., Losson, B. (2012). Longitudinal field study on bovine Babesia spp. and Anaplasma phagocytophilum infections during a grazing season in Belgium. Parasitol Res. 110(4): 1525-1530. https://doi.org/10.1007/s00436-011-2657-0 PMid:21947341         
  36. Overzier, E., Pfister, K., Herb, I., Mahling, M., Böck, G. Jr, Silaghi, C. (2013). Detection of tick-borne pathogens in roe deer (Capreolus capreolus), in questing ticks (Ixodes ricinus), and in ticks infesting roe deer in southern Germany. Ticks Tick Borne Dis. 4(4): 320-328. https://doi.org/10.1016/j.ttbdis.2013.01.004 PMid:23571115   
  37. Lagrée, A.C., Rouxel, C., Kevin, M., Dugat, T., Girault, G., Durand, B., Pfeffer, M., Silaghi, C., Nieder, M., Boulouis, H.J., Haddad, N. (2018). Co-circulation of different A. phagocytophilum variants within cattle herds and possible reservoir role for cattle. Parasit Vectors. 11, 163. https://doi.org/10.1186/s13071-018-2661-7 PMid:29523202 PMCid:PMC5845262

Copyright

© 2020 Romanos L. This is an open-access article published under the terms of the Creative Commons Attribution License which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Conflict of Interest Statement

The authors have declared that no competing interests exist.

Citation Information

Macedonian Veterinary Review. Volume 43, Issue 2, Pages 185-191, e-ISSN 1857-7415, p-ISSN 1409-7621, DOI: 10.2478/macvetrev-2020-0023, 2020

The all content of the Macedonian Veterinary Review, except where otherwise noted, is licensed under a Creative Commons Attribution License.