Severe Anaplasma phagocytophilum and Babesia divergens Concomitant Infection in Imported Captive Reindeer (Rangifer tarandus)

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:1687084710.7589/0090-3558-42.2.24916870847Search in Google Scholar

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:1768285110.1007/s11259-007-0071-y17682851Search in Google Scholar

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:2249311610.7589/0090-3558-48.2.41622493116Search in Google Scholar

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:PMC265764210.3201/eid1502.081247265764219193284Search in Google Scholar

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:PMC161030710.1128/AEM.00823-06161030717021198Search in Google Scholar

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.Search in Google Scholar

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:1254106110.1007/s00436-002-0737-x12541061Search in Google Scholar

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:PMC332179110.3201/eid1705.101834332179121529420Search in Google Scholar

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:2598632610.1016/j.vetpar.2015.04.02625986326Search in Google Scholar

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:1868964110.7589/0090-3558-44.3.56918689641Search in Google Scholar

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:879998810.1136/vr.138.24.5958799988Search in Google Scholar

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:PMC693377210.3389/fvets.2019.00461693377231921918Search in Google Scholar

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:2356889710.7589/2012-04-11523568897Search in Google Scholar

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:1929840510.1111/j.1469-0691.2008.02142.x19298405Search in Google Scholar

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:1929840410.1111/j.1469-0691.2008.02143.x19298404Search in Google Scholar

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:2057564710.1089/vbz.2009.018920575647Search in Google Scholar

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:2886919110.1016/j.ttbdis.2017.08.00528869191Search in Google Scholar

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.Search in Google Scholar

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:1936825510.1638/2008-0011.119368255Search in Google Scholar

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:1204945610.1007/s00436-001-0576-112049456Search in Google Scholar

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:PMC332308610.3201/eid1004.030377332308615200851Search in Google Scholar

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:1628229510.4269/ajtmh.2005.73.865Search in Google Scholar

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:PMC605612710.3201/eid2408.180309605612730016254Search in Google Scholar

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:PMC8835710.1128/JCM.39.9.3395-3397.20018835711526189Search in Google Scholar

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:PMC282807810.3201/eid1308.061560282807817953093Search in Google Scholar

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:PMC337178510.3201/eid1107.040724337178516022795Search in Google Scholar

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:1598662710.1645/GE-394R15986627Search in Google Scholar

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:PMC303789810.1186/1297-9716-42-7303789821314977Search in Google Scholar

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:1973357210.1016/j.ijpara.2009.08.00819733572Search in Google Scholar

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:PMC631893310.1186/s13071-018-3269-7631893330606253Search in Google Scholar

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:1981187810.1016/j.vetpar.2009.09.01319811878Search in Google Scholar

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:1251934910.1046/j.1469-0691.2002.00557.x12519349Search in Google Scholar

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:PMC343969110.1186/1756-3305-5-156343969122862883Search in Google Scholar

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:PMC348082710.1186/1756-3305-5-191348082722950642Search in Google Scholar

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:2194734110.1007/s00436-011-2657-021947341Search in Google Scholar

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:2357111510.1016/j.ttbdis.2013.01.00423571115Search in Google Scholar

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:PMC584526210.1186/s13071-018-2661-7584526229523202Search in Google Scholar