Cervids as sentinel-species for tick-borne encephalitis virus in Norway - A serological study.
cervids
sentinel animals
seroprevalence
tick-borne encephalitis virus
Journal
Zoonoses and public health
ISSN: 1863-2378
Titre abrégé: Zoonoses Public Health
Pays: Germany
ID NLM: 101300786
Informations de publication
Date de publication:
06 2020
06 2020
Historique:
received:
12
05
2019
revised:
19
11
2019
accepted:
24
11
2019
pubmed:
20
12
2019
medline:
30
1
2021
entrez:
20
12
2019
Statut:
ppublish
Résumé
Tick-borne encephalitis virus (TBEV) is the causative agent of tick-borne encephalitis (TBE). TBEV is one of the most important neurological pathogens transmitted by tick bites in Europe. The objectives of this study were to investigate the seroprevalence of TBE antibodies in cervids in Norway and the possible emergence of new foci, and furthermore to evaluate if cervids can function as sentinel animals for the distribution of TBEV in the country. Serum samples from 286 moose, 148 roe deer, 140 red deer and 83 reindeer from all over Norway were collected and screened for TBE immunoglobulin G (IgG) antibodies with a modified commercial enzyme-linked immunosorbent assay (ELISA) and confirmed by TBEV serum neutralisation test (SNT). The overall seroprevalence against the TBEV complex in the cervid specimens from Norway was 4.6%. The highest number of seropositive cervids was found in south-eastern Norway, but seropositive cervids were also detected in southern- and central Norway. Antibodies against TBEV detected by SNT were present in 9.4% of the moose samples, 1.4% in red deer, 0.7% in roe deer, and nil in reindeer. The majority of the positive samples in our study originated from areas where human cases of TBE have been reported in Norway. The study is the first comprehensive screening of cervid species in Norway for antibodies to TBEV, and shows that cervids are useful sentinel animals to indicate TBEV occurrence, as supplement to studies in ticks. Furthermore, the results indicate that TBEV might be spreading northwards in Norway. This information may be of relevance for public health considerations and supports previous findings of TBEV in ticks in Norway.
Substances chimiques
Antibodies, Viral
0
Immunoglobulin G
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
342-351Subventions
Organisme : Norwegian Environmental Agency
ID : Health's Surveillance Program for Cervids and Mu
Pays : International
Organisme : Norwegian Ministry of Health and Care Services
ID : B1412
Pays : International
Organisme : EU Interreg
ID : 167226
Pays : International
Organisme : EU Interreg
ID : 20200422
Pays : International
Informations de copyright
© 2019 The Authors. Zoonoses and Public Health published by Blackwell Verlag GmbH.
Références
Andersen, N. S., Larsen, S. L., Olesen, C. R., Stiasny, K., Kolmos, H. J., Jensen, P. M., & Skarphedinsson, S. (2019). Continued expansion of tick-borne pathogens: Tick-borne encephalitis virus complex and Anaplasma phagocytophilum in Denmark. Ticks and Tick-borne Diseases, 10(1), 115-123. https://doi.org/10.1016/j.ttbdis.2018.09.007
Andreassen, A., Jore, S., Cuber, P., Dudman, S., Tengs, T., Isaksen, K., … Vainio, K. (2012). Prevalence of tick borne encephalitis virus in tick nymphs in relation to climatic factors on the southern coast of Norway. Parasites & Vectors, 5, 177. https://doi.org/10.1186/1756-3305-5-177
Apollonio, M., R. Andersen, & R. Putman (Eds.) (2010). Present status and future challenges for European ungulate management. European ungulates and their management in the 21st century. Cambridge, UK: Cambridge University Press.
Balling, A., Plessow, U., Beer, M., & Pfeffer, M. (2014). Prevalence of antibodies against tick-borne encephalitis virus in wild game from Saxony. Germany. Ticks Tick Borne Dis, 5(6), 805-809. https://doi.org/10.1016/j.ttbdis.2014.06.007
Calisher, C. H., Karabatsos, N., Dalrymple, J. M., Shope, R. E., Porterfield, J. S., Westaway, E. G., & Brandt, W. E. (1989). Antigenic relationships between flaviviruses as determined by cross-neutralization tests with polyclonal antisera. Journal of General Virology, 70(Pt 1), 37-43. https://doi.org/10.1099/0022-1317-70-1-37
Carpi, G., Cagnacci, F., Neteler, M., & Rizzoli, A. (2008). Tick infestation on roe deer in relation to geographic and remotely sensed climatic variables in a tick-borne encephalitis endemic area. Epidemiology and Infection, 136(10), 1416-1424. https://doi.org/10.1017/S0950268807000039
Clarke, D. H., & Casals, J. (1958). Techniques for hemagglutination and hemagglutination-inhibition with arthropod-borne viruses. American Journal of Tropical Medicine and Hygiene, 7(5), 561-573. https://doi.org/10.4269/ajtmh.1958.7.561
Dai, X., Shang, G., Lu, S., Yang, J., & Xu, J. (2018). A new subtype of eastern tick-borne encephalitis virus discovered in Qinghai-Tibet Plateau. China. Emerg Microbes Infect, 7(1), 74. https://doi.org/10.1038/s41426-018-0081-6
Dobler, G., Gniel, D., Petermann, R., & Pfeffer, M. (2012). Epidemiology and distribution of tick-borne encephalitis. Wiener Medizinische Wochenschrift, 162(11-12), 230-238. https://doi.org/10.1007/s10354-012-0100-5
Duscher, G. G., Wetscher, M., Baumgartner, R., & Walder, G. (2015). Roe deer sera used for TBE surveillance in Austria. Ticks and Tick-borne Diseases, 6(4), 489-493. https://doi.org/10.1016/j.ttbdis.2015.03.018
Esser, H. J., Mogling, R., Cleton, N. B., van der Jeugd, H., Sprong, H., Stroo, A., … Reusken, C. (2019). Risk factors associated with sustained circulation of six zoonotic arboviruses: A systematic review for selection of surveillance sites in non-endemic areas. Parasites & Vectors, 12(1), 265. https://doi.org/10.1186/s13071-019-3515-7
Franzmann, A. W., & Schwartz, C. C. (2007). Ecology and management of the North American moose, Vol. 2. Boulder: University Press of Colorado.
Gao, G. F., Jiang, W. R., Hussain, M. H., Venugopal, K., Gritsun, T. S., Reid, H. W., & Gould, E. A. (1993). Sequencing and antigenic studies of a Norwegian virus isolated from encephalomyelitic sheep confirm the existence of louping ill virus outside Great Britain and Ireland. Journal of General Virology, 74(Pt 1), 109-114. https://doi.org/10.1099/0022-1317-74-1-109
Gerth, H. J., Grimshandl, D., Stage, B., Doller, G., & Kunz, C. (1995). Roe deer as sentinels for endemicity of tick-borne encephalitis virus. Epidemiology and Infection, 115(2), 355-365. https://doi.org/10.1017/s0950268800058477
Gilbert, L. (2010). Altitudinal patterns of tick and host abundance: A potential role for climate change in regulating tick-borne diseases? Oecologia, 162(1), 217-225. https://doi.org/10.1007/s00442-009-1430-x
Gilbert, L., Jones, L. D., Hudson, P. J., Gould, E. A., & Reid, H. W. (2000). Role of small mammals in the persistence of Louping-ill virus: Field survey and tick co-feeding studies. Medical and Veterinary Entomology, 14(3), 277-282. https://doi.org/10.1046/j.1365-2915.2000.00236.x
Gordon, W. S., Brownlee, A., Wilson, R., & Macleod, J. (1932). Studies In Louping-Ill. (An Encephalomyelitis of Sheep.). Journal of Comparative Pathology and Therapeutics, 45, 106-140. https://doi.org/10.1016/s0368-1742(32)80008-1
Grard, G., Moureau, G., Charrel, R. N., Lemasson, J. J., Gonzalez, J. P., Gallian, P., … de Lamballerie, X. (2007). Genetic characterization of tick-borne flaviviruses: New insights into evolution, pathogenetic determinants and taxonomy. Virology, 361(1), 80-92. https://doi.org/10.1016/j.virol.2006.09.015
Grist, N. R. (1966). Diagnostic methods in clinical virology.
Hasle, G. (2013). Transport of ixodid ticks and tick-borne pathogens by migratory birds. Frontiers in Cellular and Infection Microbiology, 3, 48. https://doi.org/10.3389/fcimb.2013.00048
Hasle, G., Bjune, G., Edvardsen, E., Jakobsen, C., Linnehol, B., Roer, J. E., … Leinaas, H. P. (2009). Transport of ticks by migratory passerine birds to Norway. Journal of Parasitology, 95(6), 1342-1351. https://doi.org/10.1645/GE-2146.1
Hofmann, R. R. (1989). Evolutionary Steps of Ecophysiological Adaptation and Diversification of Ruminants - a Comparative View of Their Digestive-System. Oecologia, 78(4), 443-457. https://doi.org/10.1007/Bf00378733
Hvidsten, D., Stordal, F., Lager, M., Rognerud, B., Kristiansen, B. E., Matussek, A., … Stuen, S. (2015). Borrelia burgdorferi sensu lato-infected Ixodes ricinus collected from vegetation near the Arctic Circle. Ticks and Tick-borne Diseases, 6(6), 768-773. https://doi.org/10.1016/j.ttbdis.2015.07.002
Hvidsten, D., Stuen, S., Jenkins, A., Dienus, O., Olsen, R. S., Kristiansen, B. E., … Matussek, A. (2014). Ixodes ricinus and Borrelia prevalence at the Arctic Circle in Norway. Ticks Tick Borne Dis, 5(2), 107-112. https://doi.org/10.1016/j.ttbdis.2013.09.003
Imhoff, M., Hagedorn, P., Schulze, Y., Hellenbrand, W., Pfeffer, M., & Niedrig, M. (2015). Review: Sentinels of tick-borne encephalitis risk. Ticks Tick Borne Dis, 6(5), 592-600. https://doi.org/10.1016/j.ttbdis.2015.05.001
Jaenson, T. G., Hjertqvist, M., Bergstrom, T., & Lundkvist, A. (2012). Why is tick-borne encephalitis increasing? A review of the key factors causing the increasing incidence of human TBE in Sweden. Parasites & Vectors, 5, 184. https://doi.org/10.1186/1756-3305-5-184
Jaenson, T. G. T., Petersson, E. H., Jaenson, D. G. E., Kindberg, J., Pettersson, J. H., Hjertqvist, M., … Bengtsson, H. (2018). The importance of wildlife in the ecology and epidemiology of the TBE virus in Sweden: Incidence of human TBE correlates with abundance of deer and hares. Parasit Vectors, 11(1), 477. https://doi.org/10.1186/s13071-018-3057-4
Jahfari, S., de Vries, A., Rijks, J. M., Van Gucht, S., Vennema, H., Sprong, H., & Rockx, B. (2017). Tick-Borne Encephalitis Virus in Ticks and Roe Deer, the Netherlands. Emerging Infectious Diseases, 23(6), 1028-1030. https://doi.org/10.3201/eid2306.161247
Jeffries, C. L., Mansfield, K. L., Phipps, L. P., Wakeley, P. R., Mearns, R., Schock, A., … Johnson, N. (2014). Louping ill virus: An endemic tick-borne disease of Great Britain. Journal of General Virology, 95(Pt 5), 1005-1014. https://doi.org/10.1099/vir.0.062356-0
Jenkins, A., Hvidsten, D., Matussek, A., Lindgren, P. E., Stuen, S., & Kristiansen, B. E. (2012). Borrelia burgdorferi sensu lato in Ixodes ricinus ticks from Norway: Evaluation of a PCR test targeting the chromosomal flaB gene. Experimental and Applied Acarology, 58(4), 431-439. https://doi.org/10.1007/s10493-012-9585-2
Jensen, P. M., Skarphedinsson, S., & Semenov, A. (2004). Densities of the tick (Ixodes ricinus) and coexistence of the Louping ill virus and tick borne encephalitis on the island of Bornholm. Ugeskrift for Laeger, 166(26-31), 2563-2565.
Jouda, F., Perret, J. L., & Gern, L. (2004a). Density of questing Ixodes ricinus nymphs and adults infected by Borrelia burgdorferi sensu lato in Switzerland: Spatio-temporal pattern at a regional scale. Vector Borne Zoonotic Dis, 4(1), 23-32. https://doi.org/10.1089/153036604773082960
Jouda, F., Perret, J. L., & Gern, L. (2004b). Ixodes ricinus density, and distribution and prevalence of Borrelia burgdorferi sensu lato infection along an altitudinal gradient. Journal of Medical Entomology, 41(2), 162-169. https://doi.org/10.1603/0022-2585-41.2.162
Kaiser, R. (2012). Tick-borne encephalitis: Clinical findings and prognosis in adults. Wiener Medizinische Wochenschrift, 162(11-12), 239-243. https://doi.org/10.1007/s10354-012-0105-0
Kiffner, C., Vor, T., Hagedorn, P., Niedrig, M., & Ruhe, F. (2012). Determinants of tick-borne encephalitis virus antibody presence in roe deer (Capreolus capreolus) sera. Medical and Veterinary Entomology, 26(1), 18-25. https://doi.org/10.1111/j.1365-2915.2011.00961.x
Klaus, C., Horugel, U., Hoffmann, B., & Beer, M. (2013). Tick-borne encephalitis virus (TBEV) infection in horses: Clinical and laboratory findings and epidemiological investigations. Veterinary Microbiology, 163(3-4), 368-372. https://doi.org/10.1016/j.vetmic.2012.12.041
Klaus, C., Ziegler, U., Kalthoff, D., Hoffmann, B., & Beer, M. (2014). Tick-borne encephalitis virus (TBEV) - findings on cross reactivity and longevity of TBEV antibodies in animal sera. BMC Veterinary Research, 10, 78. https://doi.org/10.1186/1746-6148-10-78
Kovalev, S. Y., & Mukhacheva, T. A. (2017). Reconsidering the classification of tick-borne encephalitis virus within the Siberian subtype gives new insights into its evolutionary history. Infect Genet Evol, 55, 159-165. https://doi.org/10.1016/j.meegid.2017.09.014
Labuda, M., & Randolph, S. E. (1999). Survival strategy of tick-borne encephalitis virus: Cellular basis and environmental determinants. Zentralbl Bakteriol, 289(5-7), 513-524. https://doi.org/10.1016/s0934-8840(99)80005-x
Larsen, A. L., Kanestrom, A., Bjorland, M., Andreassen, A., Soleng, A., Vene, S., & Dudman, S. G. (2014). Detection of specific IgG antibodies in blood donors and tick-borne encephalitis virus in ticks within a non-endemic area in southeast Norway. Scandinavian Journal of Infectious Diseases, 46(3), 181-184. https://doi.org/10.3109/00365548.2013.865140
Larsson, C., Hvidsten, D., Stuen, S., Henningsson, A. J., & Wilhelmsson, P. (2018). "Candidatus Neoehrlichia mikurensis" in Ixodes ricinus ticks collected near the Arctic Circle in Norway. Parasit Vectors, 11(1), 620. https://doi.org/10.1186/s13071-018-3168-y
Mehl, R. (1983). The distribution and host relations of Norwegian ticks (Acari, Ixodides). Fauna Norwgica Series B, 30, 46-51.
Mlera, L., & Bloom, M. E. (2018). The Role of Mammalian Reservoir Hosts in Tick-Borne Flavivirus Biology. Frontiers in Cellular and Infection Microbiology, 8, 298. https://doi.org/10.3389/fcimb.2018.00298
Morellet, N., Klein, F., Solberg, E., & Andersen, R. (2010). The census and management of populations of ungulates in Europe (pp. 106-143). Cambridge, UK: Cambridge University Press.
Norman, R., Ross, D., Laurenson, M. K., & Hudson, P. J. (2004). The role of non-viraemic transmission on the persistence and dynamics of a tick borne virus-Louping ill in red grouse ( Lagopus lagopus scoticus) and mountain hares ( Lepus timidus). Journal of Mathematical Biology, 48(2), 119-134. https://doi.org/10.1007/s00285-002-0183-5
Norwegian Surveillance System for Communicable Diseases (MSIS) (2019). Norwegian Surveillance System for Communicable Diseases.
Norwegian Veterinary Institute (2019). Retrieved from www.vetinst.no, 31.10.19.
Paulsen, K. M., Pedersen, B. N., Soleng, A., Okbaldet, Y. B., Pettersson, J. H., Dudman, S. G., … Andreassen, A. (2015). Prevalence of tick-borne encephalitis virus in Ixodes ricinus ticks from three islands in north-western Norway. APMIS, 123(9), 759-764. https://doi.org/10.1111/apm.12412
Paulsen, K. M., Stuen, S., das Neves, C. G., Suhel, F., Gurung, D., Soleng, A., … Granquist, E. G. (2019). Tick-borne encephalitis virus in cows and unpasteurized cow milk from Norway. Zoonoses and Public Health, 66(2), 216-222. https://doi.org/10.1111/zph.12554
Paulsen, K. M., Vikse, R., Soleng, A., Edgar, K. S., Dudman, S., Wiklund, B. S., & Andreassen, A.. (2017). TBE in Norway. In: G. Dobler, W. Erber, & H. J. Schmitt (Eds.), TBE-The Book. Global Health Press, Singapore 2017 Available online: https://id-ea.org/tbe/tbe-countries-norway/
Perret, J. L., Guigoz, E., Rais, O., & Gern, L. (2000). Influence of saturation deficit and temperature on Ixodes ricinus tick questing activity in a Lyme borreliosis-endemic area (Switzerland). Parasitology Research, 86(7), 554-557. https://doi.org/10.1007/s004360000209
Pettersson, J. H., Golovljova, I., Vene, S., & Jaenson, T. G. (2014). Prevalence of tick-borne encephalitis virus in Ixodes ricinus ticks in northern Europe with particular reference to Southern Sweden. Parasites & Vectors, 7, 102. https://doi.org/10.1186/1756-3305-7-102
Randolph, S. E. (2004). Tick ecology: Processes and patterns behind the epidemiological risk posed by ixodid ticks as vectors. Parasitology, 129(Suppl), S37-65. https://doi.org/10.1017/s0031182004004925
Randolph, S. E. (2011). Transmission of tick-borne pathogens between co-feeding ticks: Milan Labuda's enduring paradigm. Ticks and Tick-borne Diseases, 2(4), 179-182. https://doi.org/10.1016/j.ttbdis.2011.07.004
Reid, H. W., Duncan, J. S., Phillips, J. D., Moss, R., & Watson, A. (1978). Studies of louping-ill virus (Flavivirus group) in wild red grouse (Lagopus lagopus scoticus). The Journal of Hygiene, 81(2), 321-329. https://doi.org/10.1017/s002217240002516x
Ruzek, D., Avsic Zupanc, T., Borde, J., Chrdle, A., Eyer, L., Karganova, G., … Zajkowska, J. (2019). Tick-borne encephalitis in Europe and Russia: Review of pathogenesis, clinical features, therapy, and vaccines. Antiviral Research, 164, 23-51. https://doi.org/10.1016/j.antiviral.2019.01.014
Skarphedinsson, S., Jensen, P. M., & Kristiansen, K. (2005). Survey of tickborne infections in Denmark. Emerging Infectious Diseases, 11(7), 1055-1061. https://doi.org/10.3201/eid1107.041265
Solberg, E. J., Strand, O., Veiberg, V., Andersen, R., Heim, M., Rolandsen, C., … Astrup, R. (2010). Hjortevilt 2009 - Årsrapport fra Overvåkingsprogrammet for hjortevilt.
Soleng, A., Edgar, K. S., Paulsen, K. M., Pedersen, B. N., Okbaldet, Y. B., Skjetne, I. E. B., … Andreassen, A. K. (2018). Distribution of Ixodes ricinus ticks and prevalence of tick-borne encephalitis virus among questing ticks in the Arctic Circle region of northern Norway. Ticks and Tick-borne Diseases, 9(1), 97-103. https://doi.org/10.1016/j.ttbdis.2017.10.002
Stiasny, K., Holzmann, H., & Heinz, F. X. (2009). Characteristics of antibody responses in tick-borne encephalitis vaccination breakthroughs. Vaccine, 27(50), 7021-7026. https://doi.org/10.1016/j.vaccine.2009.09.069
Suss, J. (2011). Tick-borne encephalitis 2010: Epidemiology, risk areas, and virus strains in Europe and Asia-an overview. Ticks and Tick-borne Diseases, 2(1), 2-15. https://doi.org/10.1016/j.ttbdis.2010.10.007
Svedmyr, A., von Zeipel, G., Borg, K., & Hansen, H. J. (1965). Infections with tick-borne encephalitis virus in the Swedish population of the elk (Alces a. alces). Acta Pathologica Microbiologica Scandinavica, 65(4), 613-620. https://doi.org/10.1111/apm.1965.65.4.613
Tambs-Lyche, H. (1943). Ixodes ricinus og piroplasmisen i Norge (Meddelselse fra Bergens Museums zoologisk avdeling.). Norsk Veterinaertidskrift, 55, 337-366.
Tavernier, P., Sys, S. U., De Clercq, K., De Leeuw, I., Caij, A. B., De Baere, M., … Roels, S. (2015). Serologic screening for 13 infectious agents in roe deer (Capreolus capreolus) in Flanders. Infection Ecology & Epidemiology, 5, 29862. https://doi.org/10.3402/iee.v5.29862
Thrusfield, M. V. (2007). Veterinary epidemiology. Oxford; Ames, IA: Blackwell Science.
Tonteri, E., Jokelainen, P., Matala, J., Pusenius, J., & Vapalahti, O. (2016). Serological evidence of tick-borne encephalitis virus infection in moose and deer in Finland: Sentinels for virus circulation. Parasites & Vectors, 9, 54. https://doi.org/10.1186/s13071-016-1335-6
Ulvund, M., Vik, T., & Krogsrud, J. (1983). Louping-ill (tick-borne encephalitis) in sheep in Norway. Norsk Veterinaertidskrift, 95, 639-664|.
van der Poel, W. H., Van der Heide, R., Bakker, D., De Looff, M., De Jong, J., Van Manen, N., … Borgsteede, F. H. (2005). Attempt to detect evidence for tick-borne encephalitis virus in ticks and mammalian wildlife in The Netherlands. Vector-Borne and Zoonotic Diseases, 5(1), 58-64. https://doi.org/10.1089/vbz.2005.5.58
Waldenstrom, J., Lundkvist, A., Falk, K. I., Garpmo, U., Bergstrom, S., Lindegren, G., … Olsen, B. (2007). Migrating birds and tickborne encephalitis virus. Emerging Infectious Diseases, 13(8), 1215-1218. https://doi.org/10.3201/eid1308.061416
Weissenbock, H., Suchy, A., & Holzmann, H. (1998). Tick-borne encephalitis in dogs: Neuropathological findings and distribution of antigen. Acta Neuropathologica, 95(4), 361-366. https://doi.org/10.1007/s004010050811
Ytrehus, B., Vainio, K., Dudman, S. G., Gilray, J., & Willoughby, K. (2013). Tick-borne encephalitis virus and louping-ill virus may co-circulate in Southern Norway. Vector-Borne and Zoonotic Diseases, 13(10), 762-768. https://doi.org/10.1089/vbz.2012.1023
Zeimes, C. B., Olsson, G. E., Hjertqvist, M., & Vanwambeke, S. O. (2014). Shaping zoonosis risk: Landscape ecology vs. landscape attractiveness for people, the case of tick-borne encephalitis in Sweden. Parasites & Vectors, 7, 370. https://doi.org/10.1186/1756-3305-7-370