SHORT_COMMUNICATION 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. https://macvetrev.mk/Files/Article/2020/10.2478/macvetrev-2020-0023/macvetrev-2020-0023.pdf 2020-10-15T09:00:00 185 191 10.2478/macvetrev-2020-0023 Anaplasma Babesia Ixodes ricinus reindeer Lola Romanos false 1 Ruminant Health Management/Interaction of Host and Pathogen Agents (IHAP), National Veterinary School of Toulouse (ENVT), 23 Chemin Des Capelles, Toulouse 31076, France AUTHOR Renaud Pierre Maillard renaud.maillard@envt.fr false 2 Ruminant Health Management/Interaction of Host and Pathogen Agents (IHAP), National Veterinary School of Toulouse (ENVT), 23 Chemin Des Capelles, Toulouse 31076, France LEAD_AUTHOR 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. PMid:16870847 1 10.7589/0090-3558-42.2.249 Stuen, S. (2007). Anaplasma phagocytophilum - the most widespread tick-borne infection in animals in Europe. Vet Res Commun. 31 (Suppl. 1): 79-84. PMid:17682851 2 10.1007/s11259-007-0071-y 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. PMid:22493116 3 10.7589/0090-3558-48.2.416 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. PMid:19193284 PMCid:PMC2657642 4 10.3201/eid1502.081247 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. PMid:17021198 PMCid:PMC1610307 5 10.1128/AEM.00823-06 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. 6 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. PMid:12541061 7 10.1007/s00436-002-0737-x 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. PMid:21529420 PMCid:PMC3321791 8 10.3201/eid1705.101834 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. PMid:25986326 9 10.1016/j.vetpar.2015.04.026 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. PMid:18689641 10 10.7589/0090-3558-44.3.569 Stuen, S. (1996). Experimental tick-borne fever infection in reindeer (Rangifer tarandus tarandus). Vet Rec. 138(24): 595-596. PMid:8799988 11 10.1136/vr.138.24.595 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. PMid:31921918 PMCid:PMC6933772 12 10.3389/fvets.2019.00461 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. PMid:23568897 13 10.7589/2012-04-115 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. PMid:19298405 14 10.1111/j.1469-0691.2008.02142.x 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. PMid:19298404 15 10.1111/j.1469-0691.2008.02143.x 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. PMid:20575647 16 10.1089/vbz.2009.0189 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. PMid:28869191 17 10.1016/j.ttbdis.2017.08.005 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. 18 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. PMid:19368255 19 10.1638/2008-0011.1 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. PMid:12049456 20 10.1007/s00436-001-0576-1 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. PMid:15200851 PMCid:PMC3323086 21 10.3201/eid1004.030377 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. PMid:16282295 22 10.4269/ajtmh.2005.73.865 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. PMid:30016254 PMCid:PMC6056127 23 10.3201/eid2408.180309 Duh, D., Petrovec, M., Avsic-Zupanc, T. (2001). Diversity of Babesia Infecting European sheep ticks (Ixodes ricinus). J Clin Microbiol. 39(9): 3395-3397. PMid:11526189 PMCid:PMC88357 24 10.1128/JCM.39.9.3395-3397.2001 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. PMid:17953093 PMCid:PMC2828078 25 10.3201/eid1308.061560 Duh, D., Petrovec, M., Bidovec, A., Avsic-Zupanc, T. (2005). Cervids as Babesiae hosts, Slovenia. Emerg Infect Dis. 11(7): 1121-1123. PMid:16022795 PMCid:PMC3371785 26 10.3201/eid1107.040724 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. PMid:15986627 27 10.1645/GE-394R 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. PMid:21314977 PMCid:PMC3037898 28 10.1186/1297-9716-42-7 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. PMid:19733572 29 10.1016/j.ijpara.2009.08.008 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. PMid:30606253 PMCid:PMC6318933 30 10.1186/s13071-018-3269-7 Woldehiwet, Z. (2010). The natural history of Anaplasma phagocytophilum. Vet Parasitol. 167(2-4): 108-122. PMid:19811878 31 10.1016/j.vetpar.2009.09.013 Blanco, J.R., Oteo, J.A. (2002). Human granulocytic ehrlichiosis in Europe. Clin Microbiol Infect. 8(12): 763-772. PMid:12519349 32 10.1046/j.1469-0691.2002.00557.x 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. PMid:22862883 PMCid:PMC3439691 33 10.1186/1756-3305-5-156 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. PMid:22950642 PMCid:PMC3480827 34 10.1186/1756-3305-5-191 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. PMid:21947341 35 10.1007/s00436-011-2657-0 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. PMid:23571115 36 10.1016/j.ttbdis.2013.01.004 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. PMid:29523202 PMCid:PMC5845262 37 10.1186/s13071-018-2661-7