Serological signature of tick-borne pathogens in Scandinavian brown bears over two decades

Particle and Fibre Toxicology

Maarten J. Voordouw⁴  Jon E. Swenson⁶  Jon M. Arnemo⁵  Mahmoud Bouzelboudjen³  Reto Lienhard¹  Maxime Jacquet⁴  Jérémy Berret⁴  Alina L. Evans²  Krista L. Jones²  Lye Paillard⁴ 

[1] ADMED Microbiologie, Boucle de Cydalise 16, la Chaux-de-Fonds, 2300, Switzerland;Department of Forestry and Wildlife Management, Faculty of Forestry and Wildlife Management, Hedmark University College, Campus Evenstad, NO-2418, Elverum, Norway;Informatics and Telematics Service, University of Neuchâtel, Rue Emile-Argand 11, Neuchâtel, 2000, Switzerland;Laboratory of Ecology and Evolution of Parasites, Institute of Biology, University of Neuchâtel, Rue Emile-Argand 11, Neuchâtel, 2000, Switzerland;Department of Wildlife, Fish and Environmental Studies, Faculty of Forest Sciences, Swedish University of Agricultural Sciences, Umeå, SE-901 83, Sweden;Norwegian Institute for Nature Research, Trondheim, NO-7485, Norway

关键词: Zoonoses;    Vector-borne diseases;    Ursus arctos;    Tick-borne encephalitis virus;    Tick-borne diseases;    Serology;    Scandinavia;    Lyme disease;    Ixodes ricinus;    Borrelia burgdorferi;   

Others  :  1222138
DOI  :  10.1186/s13071-015-0967-2

 received in 2015-05-08, accepted in 2015-06-25,  发布年份 2015

【 摘 要 】

Background

Anthropogenic disturbances are changing the geographic distribution of ticks and tick-borne diseases. Over the last few decades, the tick Ixodes ricinus has expanded its range and abundance considerably in northern Europe. Concurrently, the incidence of tick-borne diseases, such as Lyme borreliosis and tick-borne encephalitis, has increased in the human populations of the Scandinavian countries.

Methods

Wildlife populations can serve as sentinels for changes in the distribution of tick-borne diseases. We used serum samples from a long-term study on the Scandinavian brown bear, Ursus arctos, and standard immunological methods to test whether exposure to Borrelia burgdorferi sensu lato, the causative agent of Lyme borreliosis, and tick-borne encephalitis virus (TBEV) had increased over time. Bears had been sampled over a period of 18 years (1995–2012) from a southern area, where Ixodes ricinus ticks are present, and a northern area where ticks are uncommon or absent.

Results

Bears had high levels of IgG antibodies against B. burgdorferi sensu lato but not TBEV. Bears at the southern area had higher values of anti-Borrelia IgG antibodies than bears at the northern area. Over the duration of the study, the value of anti-Borrelia IgG antibodies increased in the southern area but not the northern area. Anti-Borrelia IgG antibodies increased with the age of the bear but declined in the oldest age classes.

Conclusions

Our study is consistent with the view that ticks and tick-borne pathogens are expanding their abundance and prevalence in Scandinavia. Long-term serological monitoring of large mammals can provide insight into how anthropogenic disturbances are changing the distribution of ticks and tick-borne diseases.

【 授权许可】

   
2015 Paillard et al.

【 图 表 】

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【 参考文献 】

• [1]Knap N, Avsic-Zupanc T. Correlation of TBE incidence with red deer and roe deer abundance in Slovenia. PLoS One. 2013; 8:6.
• [2]Rizzoli A, Hauffe HC, Carpi G, Vourc’h GI, Neteler M, Rosa R. Lyme borreliosis in Europe. Eurosurveillance. 2011; 16(27):2-9.
• [3]Randolph SE. Evidence that climate change has caused ‘emergence’ of tick-borne diseases in Europe? Int J Med Microbiol. 2004; 293:5-15.
• [4]Gilbert L. Altitudinal patterns of tick and host abundance: a potential role for climate change in regulating tick-borne diseases? Oecologia. 2010; 162(1):217-225.
• [5]Gray JS. Ixodes ricinus seasonal activity: Implications of global warming indicated by revisiting tick and weather data. Int J Med Microbiol. 2008; 298:19-24.
• [6]Leger E, Vourc’h G, Vial L, Chevillon C, McCoy KD. Changing distributions of ticks: causes and consequences. Exp Appl Acarol. 2013; 59(1–2):219-244.
• [7]Medlock JM, Hansford KM, Bormane A, Derdakova M, Estrada-Pena A, George J-C, et al. Driving forces for changes in geographical distribution of Ixodes ricinus ticks in Europe. Parasites Vectors. 2013;6.
• [8]Jaenson TGT, Hjertqvist M, Bergstrom T, Lundkvist A. Why is tick-borne encephalitis increasing? A review of the key factors causing the increasing incidence of human TBE in Sweden. Parasites Vectors. 2012;5.
• [9]Jore S, Viljugrein H, Hofshagen M, Brun-Hansen H, Kristoffersen AB, Nygard K, et al. Multi-source analysis reveals latitudinal and altitudinal shifts in range of Ixodes ricinus at its northern distribution limit. Parasites Vectors. 2011;4.
• [10]Jaenson TGT, Jaenson DGE, Eisen L, Petersson E, Lindgren E. Changes in the geographical distribution and abundance of the tick Ixodes ricinus during the past 30 years in Sweden. Parasites Vectors. 2012;5.
• [11]Lindgren E, Talleklint L, Polfeldt T. Impact of climatic change on the northern latitude limit and population density of the disease-transmitting European tick Ixodes ricinus. Environ Health Perspect. 2000; 108(2):119-123.
• [12]Danielova V, Schwarzova L, Materna J, Daniel M, Metelka L, Holubova J et al.. Tick-borne encephalitis virus expansion to higher altitudes correlated with climate warming. Int J Med Microbiol. 2008; 298:68-72.
• [13]Kriz B, Benes C, Danielova V, Daniel M. Socio-economic conditions and other anthropogenic factors influencing tick-borne encephalitis incidence in the Czech Republic. Int J Med Microbiol. 2004; 293:63-68.
• [14]Materna J, Daniel M, Metelka L, Harcarika J. The vertical distribution, density and the development of the tick Ixodes ricinus in mountain areas influenced by climate changes (The Krkonose Mts., Czech Republic). Int J Med Microbiol. 2008; 298:25-37.
• [15]Rizzoli A, Hauffe HC, Tagliapietra V, Neteler M, Rosa R. Forest structure and roe deer abundance predict tick-borne encephalitis risk in Italy. Plos One. 2009; 4:2.
• [16]Bennet L, Halling A, Berglund J. Increased incidence of Lyme borreliosis in southern Sweden following mild winters and during warm, humid summers. Eur J Clin Microbiol Infect Dis. 2006; 25(7):426-432.
• [17]Jaenson TGT, Lindgren E. The range of Ixodes ricinus and the risk of contracting Lyme borreliosis will increase northwards when the vegetation period becomes longer. Ticks Tick-Borne Dis. 2011; 2(1):44-49.
• [18]Jaenson TGT, Eisen L, Comstedt P, Mejlon HA, Lindgren E, Bergstrom S et al.. Risk indicators for the tick Ixodes ricinus and Borrelia burgdorferi sensu lato in Sweden. Med Vet Entomol. 2009; 23(3):226-237.
• [19]Randolph SE. To what extent has climate change contributed to the recent epidemiology of tick-borne diseases? Vet Parasitol. 2010; 167(2–4):92-94.
• [20]Randolph SE. The shifting landscape of tick-borne zoonoses: tick-borne encephalitis and Lyme borreliosis in Europe. Philos Trans R Soc Lond B Biol Sci. 2001; 356(1411):1045-1056.
• [21]Sumilo D, Bormane A, Asokliene L, Vasilenko V, Golovljova I, Avsic-Zupanc T et al.. Socio-economic factors in the differential upsurge of tick-borne encephalitis in central and eastern Europe. Rev Med Virol. 2008; 18(2):81-95.
• [22]Balling A, Plessow U, Beer M, Pfeffer M. Prevalence of antibodies against tick-borne encephalitis virus in wild game from Saxony, Germany. Ticks Tick-Borne Dis. 2014; 5(6):805-809.
• [23]Ebani VV, Bertelloni F, Torracca B, Cerri D. Serological survey of Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum, and Ehrlichia canis infections in rural and urban dogs in central Italy. Ann Agric Environ Med. 2014; 21(4):671-675.
• [24]Foley JE, Queen EV, Sacks B, Foley P. GIS-facilitated spatial epidemiology of tick-borne diseases in coyotes (Canis latrans) in northern and coastal California. Comp Immunol Microbiol Infect Dis. 2005; 28(3):197-212.
• [25]Krause PJ, Telford SR, Ryan R, Hurta AB, Kwasnik I, Luger S et al.. Geographical and temporal distribution of babesial infection in Connecticut. J Clin Microbiol. 1991; 29(1):1-4.
• [26]Kazmierczak JJ, Amundson TE, Burgess EC. Borreliosis in free-ranging black bears from Wisconsin. J Wildl Dis. 1988; 24(2):366-368.
• [27]Murray DL, Kapke CA, Evermann JF, Fuller TK. Infectious disease and the conservation of free-ranging large carnivores. Anim Conserv. 1999; 2(4):241-254.
• [28]Rogers LL. Parasites of black bears of the Lake Superior region. J Wildl Dis. 1975; 11(2):189-192.
• [29]Yabsley MJ, Nims TN, Savage MY, Durden LA. Ticks and tick-borne pathogens and putative symbionts of black bears (Ursus americanus floridanus) from Georgia and Florida. J Parasitol. 2009; 95(5):1125-1128.
• [30]Andreassen A, Jore S, Cuber P, Dudman S, Tengs T, Isaksen K, et al. Prevalence of tick borne encephalitis virus in tick nymphs in relation to climatic factors on the southern coast of Norway. Parasites Vectors. 2012;5.
• [31]Berglund J, Eitrem R, Ornstein K, Lindberg A, Ringner A, Elmrud H et al.. An epidemiologic study of Lyme-disease in southern Sweden. N Engl J Med. 1995; 333(20):1319-1324.
• [32]Csango PA, Blakstad E, Kirtz GC, Pedersen JE, Czettel B. Tick-borne encephalitis in southern Norway. Emerg Infect Dis. 2004; 10(3):533-534.
• [33]Haglund M. Occurrence of TBE in areas previously considered being non-endemic: Scandinavian data generate an international study by the International Scientific Working Group for TBE (ISW-TBE). Int J Med Microbiol. 2002; 291:50-54.
• [34]Soleng A, Kjelland V. Borrelia burgdorferi sensu lato and Anaplasma phagocytophilum in Ixodes ricinus ticks in Bronnoysund in northern Norway. Ticks Tick-Borne Dis. 2013; 4(3):218-221.
• [35]Burri C, Korva M, Bastic V, Knap N, Avsic-Zupanc T, Gern L. Serological evidence of tick-borne encephalitis virus infection in rodents captured at four sites in Switzerland. J Med Entomol. 2012; 49(2):436-439.
• [36]Magnarelli LA. Serologic diagnosis of Lyme-disease. Ann N Y Acad Sci. 1988; 539:154-161.
• [37]Wilske B, Fingerle V, Schulte-Spechtel U. Microbiological and serological diagnosis of Lyme borreliosis. FEMS Immunol Med Microbiol. 2007; 49(1):13-21.
• [38]Arnemo JM, Ahlqvist P, Andersen R, Berntsen F, Ericsson G, Odden J et al.. Risk of capture-related mortality in large free-ranging mammals: experiences from Scandinavia. Wildl Biol. 2006; 12(1):109-113.
• [39]Alonso S, Marquez FJ, Solano-Gallego L. Borrelia burgdorferi serosurvey in wild deer in England and Wales. Vector-Borne Zoonotic Dis. 2012; 12(6):448-455.
• [40]Asbakk K, Aars J, Derocher AE, Wiig O, Oksanen A, Born EW et al.. Serosurvey for Trichinella in polar bears (Ursus maritimus) from Svalbard and the Barents sea. Vet Parasitol. 2010; 172(3–4):256-263.
• [41]Deruaz D, Eid P, Deruaz J, Sempere A, Bourgouin C, Rodhain F et al.. Use of enzyme-labelled protein G assay for the detection of anti Borrelia burgdorferi antibodies in wild animal sera. Eur J Epidemiol. 1996; 12(5):515-519.
• [42]Inoshima Y, Shimizu S, Minamoto N, Hirai K, Sentsui H. Use of protein AG in an enzyme-linked immunosorbent assay for screening for antibodies against parapoxvirus in wild animals in Japan. Clin Diagn Lab Immunol. 1999; 6(3):388-391.
• [43]Rah H, Chomel BB, Follmann EH, Kasten RW, Hew CH, Farver TB et al.. Serosurvey of selected zoonotic agents in polar bears (Ursus maritimus). Vet Rec. 2005; 156(1):7-13.
• [44]Tryland M, Derocher AE, Wiig O, Godfroid J. Brucella sp antibodies in polar bears from Svalbard and the Barents sea. J Wildl Dis. 2001; 37(3):523-531.
• [45]Stobel K, Schonberg A, Staak C. A new non-species dependent ELISA for detection of antibodies to Borrelia burgdorferi s. l. in zoo animals. Int J Med Microbiol. 2002; 291:88-99.
• [46]Rieille N, Bressanelli S, Freire CCM, Arcioni S, Gern L, Peter O, et al. Prevalence and phylogenetic analysis of tick-borne encephalitis virus (TBEV) in field-collected ticks (Ixodes ricinus) in southern Switzerland. Parasites Vectors. 2014;7.
• [47]Berret J, Voordouw MJ. Lyme disease bacterium does not affect attraction to rodent odour in the tick vector. Parasites & Vectors. 2015;8.
• [48]Schwaiger M, Peter O, Cassinotti P. Routine diagnosis of Borrelia burgdorferi (sensu lato) infections using a real-time PCR assay. Clin Microbiol Infect. 2001; 7(9):461-469.
• [49]R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria; 2014.
• [50]Ekstrom C. MESS: Miscellaneous Esoteric Statistical Scripts. R package version 0.3-2 edn. 2014.
• [51]Pinheiro J, Bates D, DebRoy S, Sarkar D. nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-117 edn. 2014.
• [52]Bartoń K. MuMIn: Multi-Model Inference. R package version 1.12.1 edn. 2014.
• [53]Johnson JB, Omland KS. Model selection in ecology and evolution. Trends Ecol Evol. 2004; 19(2):101-108.
• [54]Stafford KC, Cartter ML, Magnarelli LA, Ertel SH, Mshar PA. Temporal correlations between tick abundance and prevalence of ticks infected with Borrelia burgdorferi and increasing incidence of Lyme disease. J Clin Microbiol. 1998; 36(5):1240-1244.
• [55]Leighton PA, Koffi JK, Pelcat Y, Lindsay LR, Ogden NH. Predicting the speed of tick invasion: an empirical model of range expansion for the Lyme disease vector Ixodes scapularis in Canada. J Appl Ecol. 2012; 49(2):457-464.
• [56]Ogden NH, Maarouf A, Barker IK, Bigras-Poulin M, Lindsay LR, Morshed MG et al.. Climate change and the potential for range expansion of the Lyme disease vector Ixodes scapularis in Canada. Int J Parasitol. 2006; 36(1):63-70.
• [57]Behnke JM, Lewis JW, Zain SNM, Gilbert FS. Helminth infections in Apodemus sylvaticus in southern England: interactive effects of host age, sex and year on the prevalence and abundance of infections. J Helminthol. 1999; 73(1):31-44.
• [58]Benavides JA, Huchard E, Pettorelli N, King AJ, Brown ME, Archer CE et al.. From parasite encounter to infection: Multiple-scale drivers of parasite richness in a wild social primate population. Am J Phys Anthropol. 2012; 147(1):52-63.
• [59]Bunikis J, Tsao J, Luke CJ, Luna MG, Fish D, Barbour AG. Borrelia burgdorferi infection in a natural population of Peromyscus leucopus mice: A longitudinal study in an area where Lyme borreliosis is highly endemic. J Infect Dis. 2004; 189(8):1515-1523.
• [60]Hofmeister EK, Ellis BA, Glass GE, Childs JE. Longitudinal study of infection with Borrelia burgdorferi in a population of Peromyscus leucopus at a Lyme disease-enzootic site in Maryland. Am J Trop Med Hyg. 1999; 60(4):598-609.
• [61]Day MJ. Immune system development in the dog and cat. J Comp Pathol. 2007; 137:S10-S15.
• [62]Holt PG, Jones CA. The development of the immune system during pregnancy and early life. Allergy. 2000; 55(8):688-697.
• [63]Pawelec G, Koch S, Franceschi C, Wikby A. Human immunosenescence does it have an infectious component? In: Understanding and Modulating Aging. 2006.56-65.
• [64]Solana R, Pawelec G, Tarazona R. Aging and innate immunity. Immunity. 2006; 24(5):491-494.
• [65]Leydet BF, Liang F-T. Detection of human bacterial pathogens in ticks collected from Louisiana black bears (Ursus americanus luteolus). Ticks Tick-Borne Dis. 2013; 4(3):191-196.
• [66]Manville AM. Ecto-parasite and endoparasite of black bear in northern Wisconsin. J Wildl Dis. 1978; 14(1):97-101.
• [67]Vichova B, Majlathova V, Novakova M, Straka M, Pet’ko B. First molecular detection of Anaplasma phagocytophilum in european brown bear (Ursus arctos). Vector-Borne Zoonotic Dis. 2010; 10(5):543-545.
• [68]Zele D, Avbersek J, Gruntar I, Ocepek M, Vengust G. Evidence of Anaplasma phagocytophilum in game animals from Slovenia. Acta Vet Hung. 2012; 60(4):441-448.
• [69]Bronson E, Spiker H, Driscoll CP. Serosurvey for selected pathogens in free-ranging american black bears (Ursus americanus) in Maryland, USA. J Wildl Dis. 2014; 50(4):829-836.
• [70]Schultz SM, Nicholson WL, Comer JA, Childs JE, Humphreys JG. Serologic evidence of infection with granulocytic ehrlichiae in black bears in Pennsylvania. J Wildl Dis. 2002; 38(1):47-53.
• [71]Gern L, Estrada-Pena A, Frandsen F, Gray JS, Jaenson TGT, Jongejan F et al.. European reservoir hosts of Borrelia burgdorferi sensu lato. Zentralbl Bakteriol. 1998; 287(3):196-204.
• [72]Gern L, Siegenthaler M, Hu CM, Leubagarcia S, Humair PF, Moret J. Borrelia burgdorferi in rodents (Apodemus flavicollis and A. sylvaticus) duration and enhancement of infectivity for Ixodes ricinus ticks. Eur J Epidemiol. 1994; 10(1):75-80.
• [73]Humair PF, Rais O, Gern L. Transmission of Borrelia afzelii from Apodemus mice and Clethrionomys voles to Ixodes ricinus ticks: differential transmission pattern and overwintering maintenance. Parasitology. 1999; 118:33-42.
• [74]Jaenson TGT, Talleklint L. Incompetence of roe deer as reservoirs of the Lyme borreliosis spirochete. J Med Entomol. 1992; 29(5):813-817.
• [75]Matuschka FR, Heiler M, Eiffert H, Fischer P, Lotter H, Spielman A. Diversionary role of hoofed game in the transmission of Lyme-disease spirochetes. Am J Trop Med Hyg. 1993; 48(5):693-699.
• [76]Telford SR, Mather TN, Moore SI, Wilson ML, Spielman A. Incompetence of deer as reservoirs of the Lyme-disease spirochete. Am J Trop Med Hyg. 1988; 39(1):105-109.
• [77]Kirchgessner MS, Freer H, Whipps CM, Wagner B. Detection of Borrelia burgdorferi outer surface protein antibodies in wild white-tailed deer (Odocoileus virginianus) in New York and Pennsylvania, USA. Vet Immunol Immunopathol. 2013; 153(1–2):165-169.
• [78]Magnarelli LA, Williams SC, Fikrig E. Seasonal prevalence of serum antibodies to whole cell and recombinant antigens of Borrelia burgdorferi and Anaplasma phagocytophilum in white-tailed deer in Connecticut. J Wildl Dis. 2010; 46(3):781-790.
• [79]Magnarelli LA, Anderson JF, Johnson RC. Cross-reactivity in serological tests for Lyme-disease and other spirochetal infections. J Infect Dis. 1987; 156(1):183-188.
• [80]Magnarelli LA, Miller JN, Anderson JF, Riviere GR. Cross-reactivity of nonspecific treponemal antibody in serologic tests for Lyme-disease. J Clin Microbiol. 1990; 28(6):1276-1279.