Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-23T20:31:26.609Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  26 April 2011

A. HARRISON ,
W. I. MONTGOMERY  and
K. J. BOWN
A. HARRISON*
Affiliation:
School of Biological Sciences, Queen's University Belfast, MBC, 97 Lisburn Road, Belfast BT9 7BL, UK
W. I. MONTGOMERY
Affiliation:
School of Biological Sciences, Queen's University Belfast, MBC, 97 Lisburn Road, Belfast BT9 7BL, UK
K. J. BOWN
Affiliation:
Department of Veterinary Pathology, University of Liverpool, Leahurst Campus, Chester High Road, Neston CH64 7TE, UK
*
*Corresponding author and present address: Department of Zoology and Entomology, University of Pretoria, Pretoria, 0002, South Africa. Tel: +0027 (0)713815103. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

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.

Keywords

tick-borne diseasezoonosisbasic reproduction numberIxodes ricinus
Type
Research Article
Information
Parasitology , Volume 138 , Issue 7 , June 2011 , pp. 896 - 905
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Anderson, R. M. and May, R. M. (1990). Modern vaccines: Immunisation and herd immunity. Lancet 335, 641–645.CrossRefGoogle Scholar
Arthur, D. R. (1963). British Ticks. 1st Edn. Butterworths, London.Google Scholar
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, 63–70.CrossRefGoogle Scholar
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, 1948–1954.CrossRefGoogle ScholarPubMed
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, 1771–1776.CrossRefGoogle ScholarPubMed
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, 348–359.CrossRefGoogle Scholar
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, 3164–3168.CrossRefGoogle ScholarPubMed
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, 155–160.Google ScholarPubMed
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, 73–80.Google Scholar
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, 1309–1317.CrossRefGoogle ScholarPubMed
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, 365–382.CrossRefGoogle ScholarPubMed
Duh, D., Petrovec, M. and Avsic-Zupanc, T. (2001). Diversity of Babesia infecting European sheep ticks (Ixodes ricinus). Journal of Clinical Microbiology 39, 3395–3397.CrossRefGoogle ScholarPubMed
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, 196–204.CrossRefGoogle ScholarPubMed
Gern, L. and Rais, O. (1996). Efficient transmission of Borrelia burgdorferi between cofeeding Ixodes ricinus ticks (Acari: Ixodidae). Journal of Medical Entomology 33, 189–192.CrossRefGoogle ScholarPubMed
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, 1659–1684.CrossRefGoogle ScholarPubMed
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.Google Scholar
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, 1259–1263.CrossRefGoogle ScholarPubMed
Gray, J. S. (2002). Biology of Ixodes species ticks in relation to tick-borne zoonoses. Wiener klinische Wochenschrift 114, 473–478.Google ScholarPubMed
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, 915–920.CrossRefGoogle Scholar
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, 717–729.CrossRefGoogle Scholar
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, 101–103.CrossRefGoogle ScholarPubMed
Harrison, A., Scantlebury, M. and Montgomery, W. I. (2010). Body mass and sex-biased parasitism in wood mice Apodemus sylvaticus. Oikos 119, 1099–1104.CrossRefGoogle Scholar
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, 743–754.CrossRefGoogle ScholarPubMed
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, 149–158.CrossRefGoogle ScholarPubMed
Hubálek, Z. and Halouzka, J. (1998). Prevalence rates of Borrelia burgdorferi sensu lato in host-seeking Ixodes ricinus ticks in Europe. Parasitology Research 84, 167–172.Google ScholarPubMed
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, 869–880.CrossRefGoogle ScholarPubMed
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, 33–42.CrossRefGoogle ScholarPubMed
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, 65–70.Google Scholar
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, 775–777.CrossRefGoogle Scholar
Karbowiak, G. (2004). Zoonotic reservoir of Babesia microti in Poland. Polish Journal of Microbiology 53, 61–65.Google ScholarPubMed
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, 1102–1106.CrossRefGoogle ScholarPubMed
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, 74–79.CrossRefGoogle ScholarPubMed
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, 5344–5352.CrossRefGoogle ScholarPubMed
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, 807–817.CrossRefGoogle ScholarPubMed
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, 1002–1007.CrossRefGoogle ScholarPubMed
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, 100–107.CrossRefGoogle ScholarPubMed
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, 173–197.CrossRefGoogle Scholar
Nilsson, A. and Lundqvist, L. (1978). Host selection and movements of Ixodes ricinus (Acari) larvae on small mammals. Oikos 31, 313–322.CrossRefGoogle Scholar
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, 111–118.CrossRefGoogle ScholarPubMed
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, 423–429.CrossRefGoogle Scholar
Parola, P. (2004). Tick-borne rickettsial diseases: emerging risks in Europe. Comparative Immunology, Microbiology and Infectious Diseases 27, 297–304.CrossRefGoogle ScholarPubMed
Parola, P. and Raoult, D. (2001). Ticks and tick-borne bacterial diseases in humans: an emerging infectious threat. Clinical Infectious Diseases 32, 897–928. doi: 10.1086/319347.CrossRefGoogle ScholarPubMed
Randolph, S. E. (1995). Quantifying parameters in the transmission of Babesia microti by the tick Ixodes trianguliceps amongst voles (Clethrionomys glareolus). Parasitology 110, 287–295.CrossRefGoogle ScholarPubMed
Randolph, S. E. (1998). Ticks are not insects: consequences of contrasting vector biology for transmission potential. Parasitology Today 14, 186–192.CrossRefGoogle Scholar
Randolph, S. E. (2004). Tick ecology: processes and patterns behind the epidemiological risk posed by ixodid ticks as vectors. Parasitology 129, 37–65.CrossRefGoogle ScholarPubMed
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, 765–777.CrossRefGoogle ScholarPubMed
Randolph, S. E., Gern, L. and Nuttall, P. A. (1996). Co-feeding ticks: epidemiological significance for tick-borne pathogen transmission. Parasitology Today 12, 472–479.CrossRefGoogle ScholarPubMed
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, 177–186.CrossRefGoogle ScholarPubMed
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, 741–748.CrossRefGoogle ScholarPubMed
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, 3091–3095.CrossRefGoogle ScholarPubMed
Rosą, R. and Pugliese, A. (2007). Effects of tick population dynamics and host densities on the persistence of tick-borne infections. Mathematical Biosciences 208, 216–240.CrossRefGoogle ScholarPubMed
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, 359–376.CrossRefGoogle ScholarPubMed
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, 442–446.CrossRefGoogle ScholarPubMed
Snow, K. R. (1978). Identification of Larval Ticks Found on Small Mammals in Britain. 1st Edn. The Mammal Society, Reading, Berks, UK.Google Scholar
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, 109–114.Google Scholar
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, 880–886.CrossRefGoogle Scholar
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, 6209–6214.CrossRefGoogle Scholar
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, 429–430.Google Scholar
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, 1721–1728. doi: 10.1086/382965.CrossRefGoogle ScholarPubMed