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Investigating the persistence of tick-borne pathogens via the R0 model

  • A. HARRISON (a1), W. I. MONTGOMERY (a1) and K. J. BOWN (a2)

In the epidemiology of infectious diseases, the basic reproduction number, R0, has a number of important applications, most notably it can be used to predict whether a pathogen is likely to become established, or persist, in a given area. We used the R0 model to investigate the persistence of 3 tick-borne pathogens; Babesia microti, Anaplasma phagocytophilum and Borrelia burgdorferi sensu lato in an Apodemus sylvaticus-Ixodes ricinus system. The persistence of these pathogens was also determined empirically by screening questing ticks and wood mice by PCR. All 3 pathogens behaved differently in response to changes in the proportion of transmission hosts on which I. ricinus fed, the efficiency of transmission between the host and ticks and the abundance of larval and nymphal ticks found on small mammals. Empirical data supported theoretical predictions of the R0 model. The transmission pathway employed and the duration of systemic infection were also identified as important factors responsible for establishment or persistence of tick-borne pathogens in a given tick-host system. The current study demonstrates how the R0 model can be put to practical use to investigate factors affecting tick-borne pathogen persistence, which has important implications for animal and human health worldwide.

Corresponding author
*Corresponding author and present address: Department of Zoology and Entomology, University of Pretoria, Pretoria, 0002, South Africa. Tel: +0027 (0)713815103. E-mail:
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Anderson R. M. and May R. M. (1990). Modern vaccines: Immunisation and herd immunity. Lancet 335, 641645.
Arthur D. R. (1963). British Ticks. 1st Edn. Butterworths, London.
Bown K. J., Begon M., Bennett M., Woldehiwet Z. and Ogden N. H. (2003). Seasonal dynamics of Anaplasma phagocytophila in a rodent-tick (Ixodes trianguliceps) system, United Kingdom. Emerging Infectious Diseases 9, 6370.
Bown K. J., Lambin X., Ogden N. H., Begon M., Telford G., Woldehiwet Z. and Birtles R. J. (2009). Delineating Anaplasma phagocytophilum ecotypes in coexisting, discrete enzootic cycles. Emerging Infectious Diseases 15, 19481954.
Bown K. J., Lambin X., Ogden N. H., Petrovec M., Shaw S. E., Woldehiwet Z. and Birtles R. J. (2007). High-resolution genetic fingerprinting of European strains of Anaplasma phagocytophilum by use of multilocus variable-number tandem-repeat analysis. Journal of Clinical Microbiology 45, 17711776.
Caraco T., Glavanakov S., Chen G., Flaherty J. E., Ohsumi T. K. and Szymanski B. K. (2002). Stage-structured infection transmission and a spatial epidemic: a model for Lyme disease. The American Naturalist 160, 348359.
Courtney J. W., Kostelnik L. M., Zeidner N. S. and Massung R. F. (2004). Multiplex real-time PCR for detection of Anaplasma phagocytophilum and Borrelia burgdorferi. Journal of Clinical Microbiology 42, 31643168.
Craine N. G., Nuttall P. A., Marriott A. C. and Randolph S. E. (1997). Role of grey squirrels and pheasants in the transmission of Borrelia burgdorferi sensu lato, the Lyme disease spirochaete, in the U.K. Folia Parasitologica 44, 155160.
Craine N. G., Randolph S. E. and Nuttall P. A. (1995). Seasonal variation in the role of grey squirrels as hosts of Ixodes ricinus, the tick vector of the Lyme disease spirochaete, in a British woodland. Folia Parasitologica 42, 7380.
De La Fuente J., Massung R. F., Wong S. J., Chu F. K., Lutz H., Meli M., Von Loewenich F. D., Grzeszczuk A., Torina A. and Caracappa S. (2005). Sequence analysis of the msp4 gene of Anaplasma phagocytophilum strains. Journal of Clinical Microbiology 43, 13091317.
Diekmann O., Heesterbeek J. A. P. and Metz J. A. J. (1990). On the definition and the computation of the basic reproduction ratio R0 in models for infectious diseases in heterogeneous populations. Journal of Mathematical Biology 28, 365382.
Duh D., Petrovec M. and Avsic-Zupanc T. (2001). Diversity of Babesia infecting European sheep ticks (Ixodes ricinus). Journal of Clinical Microbiology 39, 33953397.
Gern L., Estrada-Pena A., Frandsen F., Gray J. S., Jaenson T. G., Jongejan F., Kahl O., Korenberg E., Mehl R. and Nuttall P. A. (1998). European reservoir hosts of Borrelia burgdorferi sensu lato. Zentralblatt fur Bakteriologie: International Journal of Medical Microbiology 287, 196204.
Gern L. and Rais O. (1996). Efficient transmission of Borrelia burgdorferi between cofeeding Ixodes ricinus ticks (Acari: Ixodidae). Journal of Medical Entomology 33, 189192.
Ghosh M. and Pugliese A. (2004). Seasonal population dynamics of ticks, and its influence on infection transmission: A semi-discrete approach. Bulletin of Mathematical Biology 66, 16591684.
Gigon F. (1985). Biologie d'Ixodes ricinus L. sur le Plateau Suisse-Une contribution à l'écologie de ce vecteur. Unpublished Ph.D. thesis, University of Neuchatel, France.
Gray J., von Stedingk L. V., Gurtelschmid M. and Granstrom M. (2002). Transmission studies of Babesia microti in Ixodes ricinus ticks and gerbils. Journal of Clinical Microbiology 40, 12591263.
Gray J. S. (2002). Biology of Ixodes species ticks in relation to tick-borne zoonoses. Wiener klinische Wochenschrift 114, 473478.
Gray J. S., Kahl O., Janetzki C. and Stein J. (1992). Studies on the ecology of Lyme disease in a deer forest in County Galway, Ireland. Journal of Medical Entomology 29, 915920.
Gray J. S., Kirstein F., Robertson J. N., Stein J. and Kahl O. (1999). Borrelia burgdorferi sensu lato in Ixodes ricinus ticks and rodents in a recreational park in south-western Ireland. Experimental and Applied Acarology 23, 717729.
Gray J. S., Robertson J. N. and Key S. (2000). Limited role of rodents as reservoirs of Borrelia burgdorferi sensu lato in Ireland. European Journal of Epidemiology 16, 101103.
Harrison A., Scantlebury M. and Montgomery W. I. (2010). Body mass and sex-biased parasitism in wood mice Apodemus sylvaticus. Oikos 119, 10991104.
Hartemink N. A., Randolph S. E., Davis S. A. and Heesterbeek J. A. P. (2008). The basic reproduction number for complex disease systems: Defining R0 for tick-borne infections. The American Naturalist 171, 743754.
Hodzic E., Borjesson D. L., Feng S. and Barthold S. W. (2001). Acquisition dynamics of Borrelia burgdorferi and the agent of human granulocytic ehrlichiosis at the host-vector interface. Vector-Borne and Zoonotic Diseases 1, 149158.
Hubálek Z. and Halouzka J. (1998). Prevalence rates of Borrelia burgdorferi sensu lato in host-seeking Ixodes ricinus ticks in Europe. Parasitology Research 84, 167172.
Humair P. F., Douet V., Cadenas F. M., Schouls L. M., Van De Pol I. and Gern L. (2007). Molecular identification of bloodmeal source in Ixodes ricinus ticks using 12S rDNA as a genetic marker. Journal of Medical Entomology 44, 869880.
Humair P. F., Rais O. and Gern L. (1999). Transmission of Borrelia afzelii from Apodemus mice and Clethrionomys voles to Ixodes ricinus ticks: differential transmission pattern and overwintering maintenance. Parasitology 118, 3342.
Humair P. F., Turrian N., Aeschilimann A. and Gern L. (1993). Borrelia burgdorferi in a focus of Lyme borreliosis: epizootiologic contribution of small mammals. Folia Parasitologica 40, 6570.
Jones L. D., Davies C. R., Steele G. M. and Nuttall P. A. (1987). A novel mode of arbovirus transmission involving a nonviraemic host. Science 237, 775777.
Karbowiak G. (2004). Zoonotic reservoir of Babesia microti in Poland. Polish Journal of Microbiology 53, 6165.
Kirstein F., Rijpkema S., Molkenboer M. and Gray J. S. (1997). Local variations in the distribution and prevalence of Borrelia burgdorferi sensu lato genomospecies in Ixodes ricinus ticks. Applied and Environmental Microbiology 63, 11021106.
Kurtenbach K., De Michelis S., Etti S., Schäfer S. M., Sewell H. S., Brade V. and Kraiczy P. (2002). Host association of Borrelia burgdorferi sensu lato–the key role of host complement. Trends in Microbiology 10, 7479.
Kurtenbach K., Dizij A., Seitz H. M., Margos G., Moter S. E., Kramer M. D., Wallich R., Schaible U. E. and Simon M. M. (1994). Differential immune responses to Borrelia burgdorferi in European wild rodent species influence spirochete transmission to Ixodes ricinus L. (Acari: Ixodidae). Infection and Immunity 62, 53445352.
Kurtenbach K., Kampen H., Dizij A., Arndt S., Seitz H., Schaible U. E. and Simon M. M. (1995). Infestation of rodents with larval Ixodes ricinus (Acari: Ixodidae) is an important factor in the transmission cycle of Borrelia burgdorferi sl in German woodlands. Journal of Medical Entomology 32, 807817.
Liz J. S., Anderes L., Sumner J. W., Massung R. F., Gern L., Rutti B. and Brossard M. (2000). PCR detection of granulocytic ehrlichiae in Ixodes ricinus ticks and wild small mammals in western Switzerland. Journal of Clinical Microbiology 38, 10021007.
Matuschka F. R., Fischer P., Musgrave K., Richter D. and Spielman A. (1991). Hosts on which nymphal Ixodes ricinus most abundantly feed. The American Journal of Tropical Medicine and Hygiene 44, 100107.
Milne A. (1949). The ecology of the sheep tick, Ixodes ricinus L. Host relationships of the tick, Part 2 Observations on hill and moorland grazings in northern England. Parasitology 39, 173197.
Nilsson A. and Lundqvist L. (1978). Host selection and movements of Ixodes ricinus (Acari) larvae on small mammals. Oikos 31, 313322.
Norman R., Bowers R. G., Begon M. and Hudson P. J. (1999). Persistence of tick-borne virus in the presence of multiple host species: tick reservoirs and parasite mediated competition. Journal of Theoretical Biology 200, 111118.
Ogden N. H., Bown K., Horrocks B. K., Woldehiwet Z. and Bennett M. (1998). Granulocytic Ehrlichia infection in ixodid ticks and mammals in woodlands and uplands of the UK. Medical and Veterinary Entomology 12, 423429.
Parola P. (2004). Tick-borne rickettsial diseases: emerging risks in Europe. Comparative Immunology, Microbiology and Infectious Diseases 27, 297304.
Parola P. and Raoult D. (2001). Ticks and tick-borne bacterial diseases in humans: an emerging infectious threat. Clinical Infectious Diseases 32, 897928. doi: 10.1086/319347.
Randolph S. E. (1995). Quantifying parameters in the transmission of Babesia microti by the tick Ixodes trianguliceps amongst voles (Clethrionomys glareolus). Parasitology 110, 287295.
Randolph S. E. (1998). Ticks are not insects: consequences of contrasting vector biology for transmission potential. Parasitology Today 14, 186192.
Randolph S. E. (2004). Tick ecology: processes and patterns behind the epidemiological risk posed by ixodid ticks as vectors. Parasitology 129, 3765.
Randolph S. E. and Craine N. G. (1995). General framework for comparative quantitative studies on transmission of tick-borne diseases using Lyme borreliosis in Europe as an example. Journal of Medical Entomology 32, 765777.
Randolph S. E., Gern L. and Nuttall P. A. (1996). Co-feeding ticks: epidemiological significance for tick-borne pathogen transmission. Parasitology Today 12, 472479.
Randolph S. E., Miklisova D., Lysy J., Rogers D. J. and Labuda M. (1999). Incidence from coincidence: patterns of tick infestations on rodents facilitate transmission of tick-borne encephalitis virus. Parasitology 118, 177186.
Randolph S. E. and Storey K. (1999). Impact of microclimate on immature tick-rodent host interactions (Acari: Ixodidae): implications for parasite transmission. Journal of Medical Entomology 36, 741748.
Rijpkema S. G., Molkenboer M. J., Schouls L. M., Jongejan F. and Schellekens J. F. (1995). Simultaneous detection and genotyping of three genomic groups of Borrelia burgdorferi sensu lato in Dutch Ixodes ricinus ticks by characterization of the amplified intergenic spacer region between 5S and 23S rRNA genes. Journal of Clinical Microbiology 33, 30913095.
Rosą R. and Pugliese A. (2007). Effects of tick population dynamics and host densities on the persistence of tick-borne infections. Mathematical Biosciences 208, 216240.
Rosą R., Pugliese A., Norman R. and Hudson P. J. (2003). Thresholds for disease persistence in models for tick-borne infections including non-viraemic transmission, extended feeding and tick aggregation. Journal of Theoretical Biology 224, 359376.
Simpson V. R., Panciera R. J., Hargreaves J., McGarry J. W., Scholes S. F. E., Bown K. J. and Birtles R. J. (2005). Myocarditis and myositis due to infection with Hepatozoon species in pine martens (Martes martes) in Scotland. The Veterinary Record 156, 442446.
Snow K. R. (1978). Identification of Larval Ticks Found on Small Mammals in Britain. 1st Edn. The Mammal Society, Reading, Berks, UK.
Stanzak J., Gabre R. M., Kruminis-Lozowska W., Racewicz M. and Kubica-Biernat B. (2004). Ixodes ricinus as a vector of Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum and Babesia microti in urban and suburban forests. Annals of Agriculture and Environmental Medicine 11, 109114.
Talleklint L. and Jaenson T. G. T. (1994). Transmission of Borrelia burgdorferi sl from mammal reservoirs to the primary vector of Lyme borreliosis, Ixodes ricinus (Acari: Ixodidae), in Sweden. Journal of Medical Entomology 31, 880886.
Telford S. R., Dawson J. E., Katavolos P., Warner C. K., Kolbert C. P. and Persing D. H. (1996). Perpetuation of the agent of human granulocytic ehrlichiosis in a deer tick-rodent cycle. Proceedings of the National Academy of Sciences, USA, 93, 62096214.
Telford S. R., Mather T. N., Moore S. I., Wilson M. L. and Spielman A. (2006). Incompetence of Deer as reservoirs of Borrelia burgdorferi. Annals of the New York Academy of Sciences 539, 429430.
Vannier E., Borggraefe I., Telford S. R., Menon S., Brauns T., Spielman A., Gelfand J. A. and Wortis H. H. (2004). Age-associated decline in resistance to Babesia microti is genetically determined. The Journal of Infectious Diseases 189, 17211728. doi: 10.1086/382965.
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