https://doi.org/10.4081/gh.2020.843
Ecological niche modeling of Babesia sp infection in wildlife experimentally evaluated in questing Ixodes ricinus.
Submitted: 2 December 2019
Accepted: 4 February 2020
Published: 17 June 2020
Accepted: 4 February 2020
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All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
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Tick-borne diseases and especially protozoa of the genus Babesia, are gaining increasing attention as emerging zoonotic pathogens. Zoonotic species like B. venatorum and B. microti have wild animals as main reservoir hosts. We propose a habitat suitability model for Babesia spp., as tool for institutions and policy makes to better understand the entity of Babesia presence, to improve diagnostic awareness and to optimize screening and preventive actions. The probability of presence of Babesia spp. was estimated using as presence data, wild ruminants positive by PCR to Babesia spp. which were correlated to environmental factors that can favor or limit vector and host availability. We developed three separate models to discriminate the different roles of Red deer and Roe deer and Alpine chamois in Babesia spp. epidemiology. A comprehensive model using all presence data from all ungulates species was also developed. The overall suitable area for Babesia spp. in this simulation is of 3723 km2, which correspond to 15.51% of the background regional territory. The model developed was empirically validated assessing tick abundance in randomly chosen areas classified by the model as moderately or highly suitable for Babesia spp. Collected ticks were tested by PCR for Babesia spp. to confirm model predictions as infection prevalence with Babesia spp. was significantly higher in areas predicted as highly suitable compared to those classified by the model as moderately suitable for Babesia spp. (X2=5.05 p<0.05, Odds Ratio OR= 2.12 CI95% 1.1-4.1).
Baneth, G., Cardoso, L., Brilhante-Simões, P., Schnittger, L., 2019. Establishment of Babesia vulpes n. sp. (Apicomplexa: Babesiidae), a piroplasmid species pathogenic for domestic dogs. Parasites and Vectors 12, 1–8. https://doi.org/10.1186/s13071-019-3385-z
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, 416–424. https://doi.org/10.7589/0090-3558-48.2.416
Bock, R.E., Jackson, L.A., de vos, A.J., Jorgensen, W.K., 2008. Babesiosis of cattle, in: Ticks: Biology, Disease and Control. https://doi.org/10.1017/CBO9780511551802.014
Bonnet, S., Jouglin, M., L’Hostis, M., Chauvin, A., 2007. Babesia sp. EU1 from roe deer and transmission within Ixodes ricinus. Emerg. Infect. Dis. https://doi.org/10.3201/eid1308.061560
Cadenas, F.M., Rais, O., Humair, P.-F., Douet, V., Moret, J., Gern, L., 2007. Identification of Host Bloodmeal Source and Borrelia burgdorferi Sensu Lato in Field-Collected Ixodes ricinus Ticks in Chaumont (Switzerland) . J. Med. Entomol. 44, 1109–1117. https://doi.org/10.1093/jmedent/44.6.1109
Carnevali, L., Pedrotti, L., Riga, F., Toso, S., 2009. Banca Dati Ungulati. Status, distribuzione, consistenza, gestione e prelievo venatorio delle popolazioni di ungulati in Italia. Rapporto 2001-2005 [Ungulates in Italy. Status, distribution, abundance, management and hunting of ungulate populations in Ital.
Cézanne, R., Mrowietz, N., Eigner, B., Duscher, G.G., Glawischnig, W., Fuehrer, H.P., 2017. Molecular analysis of Anaplasma phagocytophilum and Babesia divergens in red deer (Cervus elaphus) in Western Austria. Mol. Cell. Probes 31, 55–58. https://doi.org/10.1016/j.mcp.2016.07.003
Criado-Fornelio, A., Martinez-Marcos, A., Buling-Saraña, A., Barba-Carretero, J.C., 2003. Molecular studies on Babesia, Theileria and Hepatozoon in southern Europe: Part I. Epizootiological aspects. Vet. Parasitol. 113, 189–201. https://doi.org/10.1016/S0304-4017(03)00078-5
Daniel, M., Danielová, V., KřÞ, B., Jirsa, A., NožiÄka, J., 2003. Shift of the tick Ixodes ricinus and tick-borne encephalitis to higher altitudes in Central Europe. Eur. J. Clin. Microbiol. Infect. Dis. 22, 327–328. https://doi.org/10.1007/s10096-003-0918-2
Daniel, M., Kol, J., Zeman, P., Pavelka, K., Sadlo, J., 1998. Predictive map of Ixodes ricinus high-incidence habitats and a tick-borne encephalitis risk assessment using satellite data. Exper 22, 417–433.
Duh, D., Petrovec, M., Bidovec, A., Avsic-Zupanc, T., 2005. Cervids as Babesiae hosts, Slovenia. Emerg. Infect. Dis. 11, 1121–1123. https://doi.org/10.3201/eid1107.040724
Ebani, V.V., Rocchigiani, G., Bertelloni, F., Nardoni, S., Leoni, A., Nicoloso, S., Mancianti, F., 2016. Molecular survey on the presence of zoonotic arthropod-borne pathogens in wild red deer (Cervus elaphus). Comp. Immunol. Microbiol. Infect. Dis. 47, 77–80. https://doi.org/10.1016/j.cimid.2016.06.003
Eisen, R.J., Eisen, L., Girard, Y.A., Fedorova, N., Mun, J., Slikas, B., Leonhard, S., Kitron, U., Lane, R.S., 2010. A spatially-explicit model of acarological risk of exposure to Borrelia burgdorferi-infected Ixodes pacificus nymphs in northwestern California based on woodland type, temperature, and water vapor. Ticks Tick. Borne. Dis. 1, 35–43. https://doi.org/10.1016/j.ttbdis.2009.12.002
Elith, J., Leathwick, J.R., 2009. Species Distribution Models: Ecological Explanation and Prediction Across Space and Time. Annu. Rev. Ecol. Evol. Syst. 40, 677–697. https://doi.org/10.1146/annurev.ecolsys.110308.120159
Elith, J., Phillips, S.J., Hastie, T., DudÃk, M., Chee, Y.E., Yates, C.J., 2011. A statistical explanation of MaxEnt for ecologists. Divers. Distrib. 17, 43–57. https://doi.org/10.1111/j.1472-4642.2010.00725.x
Estrada-Pena, A., 2001. Forecasting habitat suitability for ticks and prevention of tick-borne diseases. Vet. Parasitol. 98, 111–132. https://doi.org/10.1016/S0304-4017(01)00426-5
Estrada-Peña, A., 2001. Distribution, abundance and habitat preferences of Ixodes ricinus (Acari: Ixodidae) in Northern Spain. J Med Entomol 38, 361–370.
Estrada-Peña, A., Bouattour, A., Camicas, J., Walker, A.R., 2004. Ticks of Veterinary and Medical Importance : the Mediterranean Basin.
Estrada-Peña, A., Venzal, J.M., 2006. Changes in habitat suitability for the tick Ixodes ricinus (Acari: Ixodidae) in Europe (1900-1999). Ecohealth 3, 154–162. https://doi.org/10.1007/s10393-006-0036-6
Gray, J., Von Stedingk, L.V., Gürtelschmid, M., Granström, M., 2002. Transmission studies of Babesia microti in Ixodes ricinus ticks and gerbils. J. Clin. Microbiol. https://doi.org/10.1128/JCM.40.4.1259-1263.2002
Guitián, F.J., Camacho, A.T., Telford, S.R., 2003. Case-control study of canine infection by a newly recognised Babesia microti-like piroplasm. Prev. Vet. Med. 61, 137–145. https://doi.org/10.1016/S0167-5877(03)00164-8
Hilpertshauser, H., Deplazes, P., Meli, M.L., Hofmann-Lehmann, R., Lutz, H., Mathis, A., 2007. Genotyping of Babesia bigemina from cattle from a non-endemic area (Switzerland). Vet. Parasitol. 145, 59–64. https://doi.org/10.1016/j.vetpar.2006.12.006
Hirzel, A.H., Le Lay, G., Helfer, V., Randin, C., Guisan, A., 2006. Evaluating the ability of habitat suitability models to predict species presences. Ecol. Modell. 199, 142–152. https://doi.org/10.1016/j.ecolmodel.2006.05.017
Hoby, S., Mathis, A., Doherr, M.G., Robert, N., Ryser-Degiorgis, M.-P., 2009. Babesia capreoli infections in Alpine Chamois ( Rupicapra R . Rupicapra ), Roe Deer ( Capreolus C . Capreolus) and Red Deer (Cervus elaphus) from Switzerland. J. Wildl. Dis. 45, 748–753.
Hoby, S., Robert, N., Mathis, A., Schmid, N., Meli, M.L., Hofmann-Lehmann, R., Lutz, H., Deplazes, P., Ryser-Degiorgis, M.P., 2007. Babesiosis in free-ranging chamois (Rupicapra r. rupicapra) from Switzerland. Vet. Parasitol. 148, 341–345. https://doi.org/10.1016/j.vetpar.2007.06.035
Hong, S.H., Kim, S.Y., Song, B.G., Rho, J.Y., Cho, C.R., Kim, C.N., Um, T.H., Kwak, Y.G., Cho, S.H., Lee, S.E., 2019. Detection and characterization of an emerging type of Babesia sp. similar to Babesia motasi for the first case of human babesiosis and ticks in Korea. Emerg. Microbes Infect. 8, 869–878. https://doi.org/10.1080/22221751.2019.1622997
Hönig, V., Vec, P.Š., Masař, O., Grubhoffer, L., 2011. Tick-Borne Diseases Risk Model for South Bohemia ( Czech Republic ). GIS Ostrava 2011 1, 23–26.
Hu, J., Jiang, Z., 2011. Climate change hastens the conservation urgency of an endangered ungulate. PLoS One 6. https://doi.org/10.1371/journal.pone.0022873
Humair, P.F., Douet, V., Moran Cadenas, F., Schouls, L.M., Van De Pol, I., Gern, L., 2007. Molecular identification of blood meal source in Ixodes ricinus ticks using 12S rDNA as a genetic marker. J. Med. Entomol. 44, 869–880.
Jore, S., Vanwambeke, S.O., Viljugrein, H., Isaksen, K., Kristoffersen, A.B., Woldehiwet, Z., Johansen, B., Brun, E., Brun-Hansen, H., Westermann, S., Larsen, I.L., Ytrehus, B., Hofshagen, M., 2014. Climate and environmental change drives Ixodes ricinus geographical expansion at the northern range margin. Parasites and Vectors 7, 1–14. https://doi.org/10.1186/1756-3305-7-11
Kauffmann, M., Rehbein, S., Hamel, D., Lutz, W., Heddergott, M., Pfister, K., Silaghi, C., 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
Kiffner, C., Lödige, C., Alings, M., Vor, T., Rühe, F., 2010. Abundance estimation of Ixodes ticks (Acari: Ixodidae) on roe deer (Capreolus capreolus). Exp. Appl. Acarol. 52, 73–84. https://doi.org/10.1007/s10493-010-9341-4
Kivaria, F.M., Ruheta, M.R., Mkonyi, P.A., Malamsha, P.C., 2007. Epidemiological aspects and economic impact of bovine theileriosis (East Coast fever) and its control: A preliminary assessment with special reference to Kibaha district, Tanzania. Vet. J. 173, 384–390. https://doi.org/10.1016/j.tvjl.2005.08.013
Kramer, V., Randolph, M., Hui, L., Irwin, W., Gutierrez, A., Duc, J., 1999. Detection of the agents of Human Ehrlichioses in Ixodid ticks from California. Am. J. Trop. Med. Hyg. 60, 62–65.
Kumar, S., Stecher, G., Li, M., Knyaz, C., Tamura, K., 2018. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 35, 1547–1549.
Lindgren, E., Tälleklint, L., Polfeldt, T., 2000. Impact of climatic change on the northern latitude limit and population density of the disease-transmitting European tick Ixodes ricinus. Environ. Health Perspect. 108, 119–123.
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, 277–284. https://doi.org/10.1016/j.ijpara.2009.08.008
Materna, J., Daniel, M., Metelka, L., Harcarik, J., 2008. The vertical distribution, density and the development of the tick Ixodes ricinus in mountain areas influenced by climate changes. Int J Med Microbiol 298, 25–37.
Maurelli, M.P., Pepe, P., Colombo, L., Armstrong, R., Battisti, E., Morgoglione, M.E., Counturis, D., Rinaldi, L., Cringoli, G., Ferroglio, E., Zanet, S., 2018. A national survey of Ixodidae ticks on privately owned dogs in Italy. Parasites and Vectors 11. https://doi.org/10.1186/s13071-018-2994-2
Merow, C., Smith, M.J., Silander, J.A., 2013. A practical guide to MaxEnt for modeling species’ distributions: What it does, and why inputs and settings matter. Ecography (Cop.). 36, 1058–1069. https://doi.org/10.1111/j.1600-0587.2013.07872.x
Michel, A.O., Mathis, A., Ryser-Degiorgis, M.P., 2014. Babesia spp. in European wild ruminant species: Parasite diversity and risk factors for infection. Vet. Res. 45, 1–11. https://doi.org/10.1186/1297-9716-45-65
Overzier, E., Pfister, K., Herb, I., Mahling, M., Böck, G., 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, 320–328. https://doi.org/10.1016/j.ttbdis.2013.01.004
Pérez De León, A.A., Strickman, D.A., Knowles, D.P., Fish, D., Thacker, E., De La Fuente, J., Krause, P.J., Wikel, S.K., Miller, R.S., Wagner, G.G., Almazn, C., Hillman, R., Messenger, M.T., Ugstad, P.O., Duhaime, R.A., Teel, P.D., Ortega-Santos, A., Hewitt, D.G., Bowers, E.J., Bent, S.J., Cochran, M.H., McElwain, T.F., Scoles, G.A., Suarez, C.E., Davey, R., Howell Freeman, J.M., Lohmeyer, K., Li, A.Y., Guerrero, F.D., Kammlah, D.M., Phillips, P., Pound, J.M., 2010. One health approach to identify research needs in bovine and human babesioses: Workshop report. Parasites and Vectors 3, 1–12. https://doi.org/10.1186/1756-3305-3-36
Pfeffer, M., Krol, N., Obiegala, A., 2018. Prevention and control of tick-borne anaplasmosis, cowdriosis and babesiosis in the cattle industry, in: Ecology and Control of Vector-Borne Diseases. Wageningen Academic Pub, pp. 175–194.
Phillips, S.J., Anderson, R.P., Schapire, R.E., 2006. Maximum entropy modeling of species geographic distributions. Ecol. Modell. 190, 231–259. https://doi.org/10.1016/j.ecolmodel.2005.03.026
Pulliam, H.R., 2000. On the relationship between niche and distribution. Ecol. Lett. 3, 349–361. https://doi.org/10.1046/j.1461-0248.2000.00143.x
Randolph, S.E., 2010. Human activities predominate in determining changing incidence of tick-borne encephalitis in Europe. Euro Surveill. 15, 24–31. https://doi.org/10.2807/ese.15.27.19606-en
Razanske, I., Rosef, O., Radzijevskaja, J., Bratchikov, M., Griciuviene, L., Paulauskas, A., 2019. Prevalence and co-infection with tick-borne Anaplasma phagocytophilum and Babesia spp. in red deer (Cervus elaphus) and roe deer (Capreolus capreolus) in Southern Norway. Int. J. Parasitol. Parasites Wildl. 8, 127–134. https://doi.org/10.1016/j.ijppaw.2019.01.003
Remesar, S., Fernández, P.D., Venzal, J.M., Pérez-Creo, A., Prieto, A., Estrada-Peña, A., López, C.M., Panadero, R., Fernández, G., DÃez-Baños, P., Morrondo, P., 2019. Tick species diversity and population dynamics of Ixodes ricinus in Galicia (north-western Spain). Ticks Tick. Borne. Dis. 10, 132–137. https://doi.org/10.1016/j.ttbdis.2018.09.006
Rizzoli, A., Silaghi, C., Obiegala, A., Rudolf, I., Hubálek, Z., Földvári, G., Plantard, O., Vayssier-Taussat, M., Bonnet, S., Ã… pitalská, E., KazimÃÂrová, M., 2014. Ixodes ricinus and Its Transmitted Pathogens in Urban and Peri-Urban Areas in Europe: New Hazards and Relevance for Public Health. Front. Public Heal. 2, 251. https://doi.org/10.3389/fpubh.2014.00251
Ryan, E.T., Hill, D.R., Solomon, T., Aronson, N.E., Endy, T.P., 2020. Hunter’s tropical medicine and emerging infectious diseases (10th).
Schnittger, L., Yin, H., Gubbels, M.J., Beyer, D., Niemann, S., Jongejan, F., Ahmed, J.S., 2003. Phylogeny of sheep and goat Theileria and Babesia parasites. Parasitol. Res. 91, 398–406. https://doi.org/10.1007/s00436-003-0979-2
Semenza, J.C., Lindgren, E., Balkanyi, L., Espinosa, L., Almqvist, M.S., Penttinen, P., Rocklöv, J., 2016. Determinants and drivers of infectious disease threat events in europe. Emerg. Infect. Dis. 22, 581–589. https://doi.org/10.3201/eid2204.151073
Sillero, N., 2011. What does ecological modelling model? A proposed classification of ecological niche models based on their underlying methods. Ecol. Modell. 222, 1343–1346. https://doi.org/10.1016/j.ecolmodel.2011.01.018
Stainforth, D.A., Chapman, S.C., Watkins, N.W., 2013. Mapping climate change in European temperature distributions. Environ. Res. Lett. 8. https://doi.org/10.1088/1748-9326/8/3/034031
Svensson, J., Hunfeld, K.P., Persson, K.E.M., 2019. High seroprevalence of Babesia antibodies among Borrelia burgdorferi-infected humans in Sweden. Ticks Tick. Borne. Dis. 10, 186–190. https://doi.org/10.1016/j.ttbdis.2018.10.007
Tälleklint, L., Jaenson, T.G.T., 1998. Increasing Geographical Distribution and Density of Ixodes ricinus (Acari: Ixodidae) in Central and Northern Sweden. J. Med. Entomol. 35, 521–526. https://doi.org/10.1093/jmedent/35.4.521
Tampieri, M.P., Galuppi, R., Bonoli, C., Cancrini, G., Moretti, A., Pietrobelli, M., 2008. Wild ungulates as Babesia hosts in Northern and Central Italy. Vector-Borne Zoonotic Dis. 8, 667–674. https://doi.org/10.1089/vbz.2008.0001
Vannier, E., Krause, P.J., 2012. Human babesiosis. N. Engl. J. Med. 366, 2397–2407. https://doi.org/10.1016/j.ijpara.2018.11.007
Vor, T., Kiffner, C., Hagedorn, P., Niedrig, M., Rühe, F., 2010. Tick burden on European roe deer (Capreolus capreolus). Exp. Appl. Acarol. 51, 405–417. https://doi.org/10.1007/s10493-010-9337-0
Walker, A., 2003. Ticks of domestic animals in Africa. Edinburgh: Bioscience Reports.
Wilson, M.L., Ducey, A.M., Litwin, T.S., Gavin, T.A., Spielman, A., 1990. Microgeographic distribution of immature Ixodes dammini ticks correlated with that of deer. Med. Vet. Entomol. 4, 151–159.
Yabsley, M.J., Shock, B.C., 2013. Natural history of Zoonotic Babesia: Role of wildlife reservoirs. Int. J. Parasitol. Parasites Wildl. 2, 18–31. https://doi.org/10.1016/j.ijppaw.2012.11.003
Zanet, S., Bassano, M., Trisciuoglio, A., Taricco, I., Ferroglio, E., 2017. Horses infected by Piroplasms different from Babesia caballi and Theileria equi: species identification and risk factors analysis in Italy. Vet. Parasitol. 236, 38–41. https://doi.org/10.1016/j.vetpar.2017.01.003
Zanet, S., Trisciuoglio, A., Bottero, E., De Mera, I.G.F., Gortazar, C., Carpignano, M.G., Ferroglio, E., 2014. Piroplasmosis in wildlife: Babesia and Theileria affecting free-ranging ungulates and carnivores in the Italian Alps. Parasites and Vectors 7, 1–7. https://doi.org/10.1186/1756-3305-7-70
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, 1–6. https://doi.org/10.1186/1297-9716-42-7
Zintl, A., Mulcahy, G., Skerrett, H.E., Taylor, S.M., Gray, J.S., 2003. Babesia divergens, a bovine blood parasite of veterinary and zoonotic importance. Clin. Microbiol. Rev. 16, 622–636. https://doi.org/10.1128/CMR.16.4.622
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Regione Piemonte – Convenzione smaltimento animali vagantiHow to Cite
Zanet, S., Ferroglio, E., Battisti, E., & Tizzani, P. (2020). Ecological niche modeling of Babesia sp infection in wildlife experimentally evaluated in questing Ixodes ricinus. Geospatial Health, 15(1). https://doi.org/10.4081/gh.2020.843
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