Abstract
Southern Germany is known as tick-borne encephalitis (TBE) risk area; however, the north of the country is almost free of human TBE cases. Due to its location in the transition zone between TBE risk areas and areas with only sporadic cases, Saxony is of importance in the surveillance of TBE. Roe deer (Capreolus capreolus), showing high seroprevalence of TBE virus (TBEV) antibodies, are considered to be sentinels for TBE risk assessment. Thus, roe deer could be used as indicators helping to better understand the focality of the TBEV in nature and as a possible source to isolate TBEV. Therefore, the aims of this study were to examine roe deer coats for the presence of ticks to establish the tick burden and to detect the TBEV in attached ticks. One hundred thirty-four roe deer coats were provided by hunters from the Hunting Association in Saxony (August 2017–January 2019). The coats were frozen at − 80 °C and after de-freezing examined on both sides—inside and outside. Attached and nonattached ticks were collected, morphologically identified and tested using real-time RT-PCR for the presence of TBEV. In total, 1279 ticks were found on 48 coats. The predominant species was Ixodes ricinus (99.76%; n = 1276). Three remaining specimens were Ixodes spp. (0.16%, 1 female and 1 nymph) and Dermacentor reticulatus (0.08%, 1 male). The average infestation rate was 26.7 (SD = 69.5), with maximum of 439 ticks per animal. Females were the dominant life stage of ticks (n = 536; 42%), followed by nymphs (n = 397; n = 31.1%), males (n = 175; 13.7%), and larvae (n = 168; 13.2%). Only half of collected ticks were attached (n = 662; 51.8%). TBEV was detected only in one tick out of 1279 tested ticks. It was a female infesting a roe deer from Saxon Switzerland-East Ore Mountain. The results show that the method used in this study is not sufficient as a sentinel marker to predict TBEV spreading in nature. Although previous studies demonstrated the usefulness of serological testing of roe deer in order to trace TBE-endemic regions, using ticks attached to them to get virus isolates is not productive.
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References
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 5:805–809. https://doi.org/10.1016/j.ttbdis.2014.06.007
Chitimia-Dobler L, Lemhöfer G, Król N, Bestehorn M, Dobler G, Pfeffer M (2019) Repeated isolation of tick-borne encephalitis virus from adult Dermacentor reticulatus ticks in an endemic area in Germany. Parasit Vectors 12:90. https://doi.org/10.1186/s13071-019-3346-6
Duscher GG, Wetscher M, Baumgartner R, Walder G (2015) Roe deer sera used for TBE surveillance in Austria. Ticks Tick Borne Dis 6:489–493. https://doi.org/10.1016/j.ttbdis.2015.03.018
Estrada-Peña A, Mihalca AD, Petney TN (2017) In: Mihalca AD, Petney TN (eds) Ticks of Europe and North Africa: a guide to species identification/Agustin Estrada-Pena. Springer Berlin Heidelberg, Cham
Gerth HJ, Grimshandl D, Stage B, Döller G, Kunz C (1995) Roe deer as sentinels for endemicity of tick-borne encephalitis virus. Epidemiol Infect 115:355–365
Handeland K, Qviller L, Vikøren T, Viljugrein H, Lillehaug A, Davidson RK (2013) Ixodes ricinus infestation in free-ranging cervids in Norway--a study based upon ear examinations of hunted animals. Vet Parasitol 195:142–149. https://doi.org/10.1016/j.vetpar.2013.02.012
Hellenbrand W, Kreusch T, Böhmer MM, Wagner-Wiening C, Dobler G, Wichmann O, Altmann D (2019) Epidemiology of Tick-Borne Encephalitis (TBE) in Germany, 2001–2018. Pathogens 8. https://doi.org/10.3390/pathogens8020042
Imhoff M, Hagedorn P, Schulze Y, Hellenbrand W, Pfeffer M, Niedrig M (2015) Review: sentinels of tick-borne encephalitis risk. Ticks Tick Borne Dis 6:592–600. https://doi.org/10.1016/j.ttbdis.2015.05.001
Jahfari S, de Vries A, Rijks JM, van Gucht S, Vennema H, Sprong H, Rockx B (2017) Tick-borne encephalitis virus in ticks and roe deer, the Netherlands. Emerg Infect Dis 23:1028–1030. https://doi.org/10.3201/eid2306.161247
Kiffner C, Lödige C, Alings M, Vor T, Rühe F (2010a) 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
Kiffner C, Zucchini W, Schomaker P, Vor T, Hagedorn P, Niedrig M, Rühe F (2010b) Determinants of tick-borne encephalitis in counties of southern Germany, 2001-2008. Int J Health Geogr 9:42. https://doi.org/10.1186/1476-072X-9-42
Kiffner C, Lödige C, Alings M, Vor T, Rühe F (2011) Attachment site selection of ticks on roe deer, Capreolus capreolus. Exp Appl Acarol 53:79–94. https://doi.org/10.1007/s10493-010-9378-4
Kiffner C, Vor T, Hagedorn P, Niedrig M, Rühe F (2012) Determinants of tick-borne encephalitis virus antibody presence in roe deer (Capreolus capreolus) sera. Med Vet Entomol 26:18–25. https://doi.org/10.1111/j.1365-2915.2011.00961.x
Kriz B, Daniel M, Benes C, Maly M (2014) The role of game (wild boar and roe deer) in the spread of tick-borne encephalitis in the Czech Republic. Vector Borne Zoonotic Dis 14:801–807. https://doi.org/10.1089/vbz.2013.1569
Lindquist L, Vapalahti O (2008) Tick-borne encephalitis. Lancet 371:1861–1871. https://doi.org/10.1016/S0140-6736(08)60800-4
Matthee S, Meltzer DG, Horak IG (1997) Sites of attachment and density assessment of ixodid ticks (Acari:Ixodidae) on impala (Aepyceros melampus). Exp Appl Acarol 21:179–192. https://doi.org/10.1023/a:1018438719827
Muders SV (2015) The role of European big game (Capreolus capreolus and Sus scrofa) as hosts for ticks and in the epidemiological life cycle of tick-borne diseases. PhD thesis, Karlsruher Institut für Technologie
Mysterud A, Hatlegjerde IL, Sørensen OJ (2014) Attachment site selection of life stages of Ixodes ricinus ticks on a main large host in Europe, the red deer (Cervus elaphus). Parasit Vectors 7:510. https://doi.org/10.1186/s13071-014-0510-x
Robert Koch Institute (2019) Karte der FSME-Risikogebiete. https://www.rki.de/DE/Content/InfAZ/F/FSME/Karte_Tab.html. Accessed 13 June 2019
Schulz M, Mahling M, Pfister K (2014) Abundance and seasonal activity of questing Ixodes ricinus ticks in their natural habitats in southern Germany in 2011. J Vector Ecol 39:56–65. https://doi.org/10.1111/j.1948-7134.2014.12070.x
Schwaiger M, Cassinotti P (2003) Development of a quantitative real-time RT-PCR assay with internal control for the laboratory detection of tick borne encephalitis virus (TBEV) RNA. J Clin Virol 27:136–145
Stefanoff P, Pfeffer M, Hellenbrand W, Rogalska J, Rühe F, Makówka A, Michalik J, Wodecka B, Rymaszewska A, Kiewra D, Baumann-Popczyk A, Dobler G (2013) Virus detection in questing ticks is not a sensitive indicator for risk assessment of tick-borne encephalitis in humans. Zoonoses Public Health 60:215–226. https://doi.org/10.1111/j.1863-2378.2012.01517.x
Süss J (2011) Tick-borne encephalitis 2010: epidemiology, risk areas, and virus strains in Europe and Asia-an overview. Ticks Tick Borne Dis 2:2–15. https://doi.org/10.1016/j.ttbdis.2010.10.007
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
Acknowledgments
The authors would like to thank Johanna Fürst, Hannah Schmuck, and Philipp Koch for their help at the laboratory and collecting the samples. Funding by Pfizer Pharma GmbH (project no. WI211246) is highly appreciated.
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Król, N., Chitimia-Dobler, L., Dobler, G. et al. Tick burden on European roe deer (Capreolus capreolus) from Saxony, Germany, and detection of tick-borne encephalitis virus in attached ticks. Parasitol Res 119, 1387–1392 (2020). https://doi.org/10.1007/s00436-020-06637-z
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DOI: https://doi.org/10.1007/s00436-020-06637-z