Abstract
Ixodes ricinus serves as vector for a range of microorganisms capable of causing clinical illness in humans. The microorganisms occur in the same vector populations and are generally affected by the same tick–host interactions. Still, the instars have different host preferences which should manifest in different transmission patterns for various microorganisms in the tick populations, i.e., most microorganisms increase in prevalence rate from larvae to nymphs because their reservoirs are among small mammals and birds that serve as blood hosts for larvae. Other microorganisms, like Anaplasma phagocytophilum, mainly increase in prevalence rates from nymphs to adults, because their reservoirs are larger ungulates that serve as primary blood hosts for nymphs and adults. We sampled a representative sample of ticks from 12 locations on Zealand and Funen, Denmark, and investigated the differences in prevalence rate of infection in larvae, nymphs and adults for multiple pathogens. Prevalence of infection for larvae, nymphs and adults, respectively, was: 0, 1.5 and 4.5% for Borrelia burgdorferi; 0, 4.2 and 3.9% for Borrelia garinii; 0, 6.6 and 6.1% for Borrelia afzelii; 0, 0 and 0.6% for Borrelia valaisiana; 0, 3.7 and 0.6% for Borrelia spielmanii; 0, 0.7 and 1.2% for Babesia divergens; 0, 0, 0.6% for Babesia venatorum; 0, 1.5 and 6.1% for A. phagocytophilum. The results were in general compatible with the hypothesis i.e., that differences in blood host for larvae and nymphs define differences in transmission of infectious agents, but other factors than differences in blood hosts between larvae and nymphs may also be important to consider.
Similar content being viewed by others
References
Alekseev AN, Jensen PM, Dubinina HV, Smirnova LA, Makrouchina NA, Zharkov SD (2000) Peculiarities of behaviour of taiga (Ixodes persulcatus) and sheep (Ixodes ricinus) ticks (Acarina: Ixodidae) determined by different methods. Folia Parasitol 47(2):147–153
AUSVET (2015) AUSVET epitools. The data entry feature for true prevalence estimates as given by: http://epitools.ausvet.com.au/content.php?page=TruePrevalence&SampleSize=1000&Pos=5&Sens=1&Spec=1&M=&R=&Conf=0.95. Accessed July 2015
Azad AF, Beard CB (1998) Rickettsial pathogens and their arthropod vectors. Emerg infec Dis 4(2):179–186. doi:10.3201/eid0402.980205
Barbour AG, Bunikis J, Fish D, Hanincová K (2015) Association between body size and reservoir competence of mammals bearing Borrelia burgdorferi at an endemic site in the northeastern United States. Parasit Vectors 8(1):299. doi:10.1186/s13071-015-0903-5
Baumann T, Kuhn-Nentwig L, Largiadèr CR, Nentwig W (2010) Expression of defensins in non-infected araneomorph spiders. Cell Mol Life Sci 67(15):2643–2651. doi:10.1007/s00018-010-0354-2
Cadenas FM, Rais O, Humair PF, 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(6):1109–1117. doi:10.1093/jmedent/44.6.1109
Gern L, Rais O (1996) Efficient transmission of Borrelia burgdorferi between cofeeding Ixodes ricinus ticks (Acari: Ixodidae). J Med Entomol 33(1):189–192. doi:10.1093/jmedent/33.1.189
Gern L, Lebet N, Moret J (1996) Dynamics of Borrelia burgdorferi infection in nymphal Ixodes ricinus ticks during feeding. Exp Appl Acarol 20(11):649–658. doi:10.1007/BF00053328
Gern L, Estrada-Pena A, Frandsen F, Gray JS, Jaenson TGT, Jongejan F, Kahl O, Korenberg E, Mehl R, Nuttall PA (1998) European reservoir hosts of Borrelia burgdorferi sensu lato. Zentralblat Bakteriol 287(3):196–204. doi:10.1016/S0934-8840(98)80121-7
Havlíková S, Ličková M, Klempa B (2013) Non-viraemic transmission of tick-borne viruses. Acta Virol 57(2):123–129. doi:10.4149/av_2013_02_123
Hubálek Z, Halouzka J (1998) Prevalence rates of Borrelia burgdorferi sensu lato in host-seeking Ixodes ricinus ticks in Europe. Parasitol Res 84(3):167–172. doi:10.1007/s004360050378
Jensen PM, Hansen H, Frandsen F (2000) Spatial risk assessment for Lyme borreliosis in Denmark. Scand J Infect Dis 32(5):545–550. doi:10.1080/003655400458857
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(1):79–94. doi:10.1007/s10493-010-9378-4
Kurtenbach K, De Michelis S, Etti S, Schäfer SM, Sewell HS, Brade V, Kraiczy P (2002) Host association of Borrelia burgdorferi sensu lato—the key role of host complement. Trends Microbiol 10(2):74–79. doi:10.1016/S0966-842X(01)02298-3
Landbo AS, Flöng PT (1992) Borrelia burgdorferi infection in Ixodes ricinus from habitats in Denmark. Med Vet Entomol 6(2):165–167. doi:10.1111/j.1365-2915.1992.tb00596.x
Liu L, Dai J, Zhao YO, Narasimhan S, Yang Y, Zhang L, Fikrig E (2012) Ixodes scapularis JAK-STAT pathway regulates tick antimicrobial peptides, thereby controlling the agent of human granulocytic anaplasmosis. J Infect Dis 206(8):1233–1241. doi:10.1093/infdis/jis484
Matuschka FR, Fischer P, Heiler M, Richter D, Spielman A (1992) Capacity of European animals as reservoir hosts for the Lyme disease spirochete. J Infect Dis 165(3):479–483. doi:10.1093/infdis/165.3.479
Mejlon HA, Jaenson TG (1997) Questing behaviour of Ixodes ricinus ticks (Acari: Ixodidae). Exp Appl Acarol 21(12):747–754. doi:10.1023/A:1018421105231
Michelet L, Delannoy S, Devillers E, Umhang G, Aspan A, Juremalm M et al (2014) High-throughput screening of tick-borne pathogens in Europe. Front Cell Infect Microbiol. doi:10.3389/fcimb.2014.00103
Nguyen TP, Lam TT, Barthold SW, Telford SR, Flavell RA, Fikrig E (1994) Partial destruction of Borrelia burgdorferi within ticks that engorged on OspE-or OspF-immunized mice. Infect Immun 62(5):2079–2084
Oehme R, Hartelt K, Backe H, Brockmann S, Kimmig P (2002) Foci of tick-borne diseases in southwest Germany. Int J Med Microbiol 291:22–29. doi:10.1016/S1438-4221(02)80005-4
Ogden NH, Nuttall PA, Randolph SE (1997) Natural Lyme disease cycles maintained via sheep by co-feeding ticks. Parasitology 115(06):591–599
Ostfeld RS, Keesing F (2000) Biodiversity and disease risk: the case of Lyme disease. Conserv Biol 14(3):722–728. doi:10.1046/j.1523-1739.2000.99014.x
Paulauskas A, Radzijevskaja J, Rosef O, Turcinaviciene J, Ambrasiene D (2009) Infestation of mice and voles with Ixodes ricinus ticks in Lithuania and Norway. Estonian J Ecol 58(2):112–125. doi:10.3176/eco.2009.2.05
Randolph SE (2011) Transmission of tick-borne pathogens between co-feeding ticks: Milan Labuda’s enduring paradigm. Ticks Tick Borne Dis 2(4):179–182. doi:10.1016/j.ttbdis.2011.07.004
Randolph SE, Miklisova D, Lysy J, Rogers DJ, Labuda M (1999) Incidence from coincidence: patterns of tick infestations on rodents facilitate transmission of tick-borne encephalitis virus. Parasitology 118(02):177–186
Rauter C, Hartung T (2005) Prevalence of Borrelia burgdorferi sensu lato genospecies in Ixodes ricinus ticks in Europe: a metaanalysis. Appl Environ Microbiol 71(11):7203–7216. doi:10.1128/AEM.71.11.7203-7216.2005
Richter D, Schlee DB, Matuschka FR (2011) Reservoir competence of various rodents for the Lyme disease spirochete Borrelia spielmanii. Appl Environ Microbiol 77(11):3565–3570. doi:10.1128/AEM.00022-11
Skarphédinsson S, Jensen PM, Kristiansen K (2005) Survey of tickborne infections in Denmark. Emerg Infect Dis 11(7):1055–1061. doi:10.3201/eid1107.041265
Skarphédinsson S, Lyholm BF, Ljungberg M, Søgaard P, Kolmos HJ, Nielsen LP (2007) Detection and identification of Anaplasma phagocytophilum, Borrelia burgdorferi, and Rickettsia helvetica in Danish Ixodes ricinus ticks. Apmis 115(3):225–230. doi:10.1111/j.1600-0463.2007.apm_256.x
Sonenshine DE (1993) The biology of ticks, vol II. Oxford University Press, Oxford. ISBN 0195084314, 9780195084313
Sréter-Lancz Z, Sréter T, Szell Z, Egyed L (2005) Molecular evidence of Rickettsia helvetica and R. monacensis infections in Ixodes ricinus from Hungary. Ann Trop Med Parasitol 99(3):325–330. doi:10.1179/136485905X28027
Stensvold CR, Al Marai D, Andersen LOB, Krogfelt KA, Jensen JS, Larsen KS, Nielsen HV (2015) Babesia spp. and other pathogens in ticks recovered from domestic dogs in Denmark. Parasit Vectors 8(1):262. doi:10.1186/s13071-015-0843-0
Stuen S, Granquist EG, Silaghi C (2013) Anaplasma phagocytophilum—a widespread multi-host pathogen with highly adaptive strategies. Front Cell Infect Microbiol. doi:10.3389/fcimb.2013.00031
Talleklint L, Jaenson TG (1994) Transmission of Borrelia burgdorferi sl from mammal reservoirs to the primary vector of Lyme borreliosis, Ixodes ricinus (Acari: Ixodidae), Sweden. J Med Entomol 31(6):880–886. doi:10.1093/jmedent/31.6.880
Víchová B, Majláthová V, Nováková M, Stanko M, Hviščová I, Pangrácová L, Chrudimský T, Čurlík J, Peťko B (2014) Anaplasma infections in ticks and reservoir host from Slovakia. Infect Genet Evol 22:265–272. doi:10.1016/j.meegid.2013.06.003
Acknowledgements
This study was included as part of the MSc thesis work for C.S Christoffersen. The work was supported by The Danish Veterinary and Food Administration (DVFA), Ministry of Environment and Food Denmark and Collaborating Veterinary Laboratories [CoVetLab: Anses (France), APHA (United Kingdom), CVI (The Netherlands), DTU (Denmark) and SVA (Sweden)].
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Jensen, P.M., Christoffersen, C.S., Moutailler, S. et al. Transmission differentials for multiple pathogens as inferred from their prevalence in larva, nymph and adult of Ixodes ricinus (Acari: Ixodidae). Exp Appl Acarol 71, 171–182 (2017). https://doi.org/10.1007/s10493-017-0110-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10493-017-0110-5