Hostname: page-component-848d4c4894-2pzkn Total loading time: 0 Render date: 2024-05-31T16:27:53.490Z Has data issue: false hasContentIssue false
  • English
  • Français

Vector seasonality, host infection dynamics and fitness of pathogens transmitted by the tick Ixodes scapularis

Published online by Cambridge University Press:  11 October 2006

N. H. OGDEN ,
M. BIGRAS-POULIN ,
C. J. O'CALLAGHAN ,
I. K. BARKER ,
K. KURTENBACH ,
L. R. LINDSAY  and
D. F. CHARRON
N. H. OGDEN
Affiliation:
Faculté de médecine vétérinaire, Université de Montréal, C.P. 5000, Saint-Hyacinthe, QC, J2S 7C6 Public Health Agency of Canada, Foodborne, Waterborne and Zoonotic Infections Division, Canada
M. BIGRAS-POULIN
Affiliation:
Faculté de médecine vétérinaire, Université de Montréal, C.P. 5000, Saint-Hyacinthe, QC, J2S 7C6
C. J. O'CALLAGHAN
Affiliation:
Department of Community Health and Epidemiology, Queen's University, Kingston, ON, Canada
I. K. BARKER
Affiliation:
Canadian Cooperative Wildlife Health Centre, Department of Pathobiology, University of Guelph, ON, Canada
K. KURTENBACH
Affiliation:
Department of Biology and Biochemistry, University of Bath, UK
L. R. LINDSAY
Affiliation:
Public Health Agency of Canada, Zoonotic Diseases and Special Pathogens Section, National Microbiology Laboratory, Canada
D. F. CHARRON
Affiliation:
Public Health Agency of Canada, Foodborne, Waterborne and Zoonotic Infections Division, Canada
Get access Rights & Permissions [Opens in a new window]

Abstract

Fitness of tick-borne pathogens may be determined by the degree to which their infection dynamics in vertebrate hosts permits transmission cycles if infective and uninfected tick stages are active at different times of the year. To investigate this hypothesis we developed a simulation model that integrates the transmission pattern imposed by seasonally asynchronous nymphal and larval Ixodes scapularis ticks in northeastern North America, with a model of infection in white-footed mice (Peromyscus leucopus) reservoir hosts, using the bacteria Borrelia burgdorferi and Anaplasma phagocytophilum as examples. In simulations, survival of microparasites, their sensitivity to reduced rodent and tick abundance, and to ‘dilution’ by a reservoir-incompetent host depended on traits that allowed (i) highly efficient transmission from acutely-infected hosts, (ii) long-lived acute or ‘carrier’ host infections, and/or (iii) transmission amongst co-feeding ticks. Minimum values for transmission efficiency to ticks, and duration of host infectivity, necessary for microparasite persistence, were always higher when nymphal and larval ticks were seasonally asynchronous than when these instars were synchronous. Thus, traits influencing duration of host infectivity, transmission efficiency to ticks and co-feeding transmission are likely to be dominant determinants of fitness in I. scapularis-borne microparasites in northeastern North America due to abiotic forcings influencing I. scapularis seasonality.

Keywords

Ixodes scapularisPeromyscus leucopuswhite-footed mousemodelfitnessBorrelia burgdorferiAnaplasma phagocytophilum
Type
Research Article
Information
Parasitology , Volume 134 , Issue 2 , February 2007 , pp. 209 - 227
Copyright
2006 Cambridge University Press

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

Adelson, M. E., Rao, R. V., Tilton, R. C., Cabets, K., Eskow, E., Fein, L., Occi, J. L. and Mordechai, E. ( 2004). Prevalence of Borrelia burgdorferi, Bartonella spp., Babesia microti, and Anaplasma phagocytophila in Ixodes scapularis ticks collected in Northern New Jersey. Journal of Clinical Microbiology 42, 2799–2801.Google Scholar
Alizon, S. and van Baalen, M. ( 2005). Emergence of a convex trade-off between transmission and virulence. American Naturalist 165, 155–167.CrossRefGoogle Scholar
Anderson, J. F., Johnson, R. C. and Magnarelli, L. A. ( 1987). Seasonal prevalence of Borrelia burgdorferi in natural populations of white-footed mice, Peromyscus leucopus. Journal of Clinical Microbiology 25, 1564–1566.Google Scholar
Barbet, A. F., Meeus, P. F., Belanger, M., Bowie, M. V., Yi, J., Lundgren, A. M., Alleman, A. R., Wong, S. J., Chu, F. K., Munderloh, U. G. and Jauron, S. D. ( 2003). Expression of multiple outer membrane protein sequence variants from a single genomic locus of Anaplasma phagocytophilum. Infection and Immunity 71, 1706–1718.CrossRefGoogle Scholar
Begon, M. ( 2006). Effects of host diversity on disease dynamics. In Ecology of Infectious Diseases: Effects of Ecosystems on Disease and of Disease on Ecosystems ( ed. Ostfeld, R. S., Keesing, F. and Eviner, V.). Princeton University Press (in the Press).
Brisson, D. and Dykhuizen, D. E. ( 2004). OspC diversity in Borrelia burgdorferi: different hosts are different niches. Genetics 168, 713–722.CrossRefGoogle Scholar
Bunikis, J., Tsao, J., Luke, C. L., Luna, M. G., Fish, D. and Barbour, A. G. ( 2004). Borrelia burgdorferi infection in a natural population of Peromyscus leucopus mice: a longitudinal study in an area where Lyme Borreliosis is highly endemic. Journal of Infectious Diseases 189, 1515–1524.CrossRefGoogle Scholar
Burgdorfer, W. and Schwan, T. G. ( 1991). Lyme borreliosis: a relapsing fever-like disease? Scandinavian Journal of Infectious Diseases Supplements 77, 17–22.Google Scholar
Daniels, T. J., Boccia, T. M., Varde, S., Marcus, J., Le, J., Bucher, D. J., Falco, R. C. and Schwartz, I. ( 1998). Geographic risk for Lyme disease and human granulocytic ehrlichiosis in southern New York State. Applied and Environmental Microbiology 64, 4663–4669.Google Scholar
Derdáková, M., Dudiòák, V., Brei, B., Brownstein, J. S., Schwartz, I. and Fish, D. ( 2004). Interaction and transmission of two Borrelia burgdorferi sensu stricto strains in a tick-rodent maintenance system. Applied and Environmental Microbiology 70, 6783–6788.CrossRefGoogle Scholar
Donahue, J. G., Piesman, J. and Spielman, A. ( 1987). Reservoir competence of white-footed mice for Lyme disease spirochetes. American Journal of Tropical Medicine and Hygiene 36, 92–96.CrossRefGoogle Scholar
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 Scholar
Gilchrist, M. A. and Sasaki, A. ( 2002). Modeling host-parasite coevolution: a nested approach based on mechanistic models. Journal of Theoretical Biology 218, 219–308.CrossRefGoogle Scholar
Gog, J. R. and Grenfell, B. T. ( 2002). Dynamics and selection of many-strain pathogens. Proceedings of the National Academy of Sciences, USA 99, 17209–17214.CrossRefGoogle Scholar
Hanincová, K., Kurtenbach, K., Diuk-Wasser, M., Brei, B. and Fish, D. ( 2006). Epidemic spread of Lyme borreliosis, northeastern United States. Emerging Infectious Diseases 12, 604–611.CrossRefGoogle Scholar
Harland, R. M., Blancher, P. J. and Millar, J. S. ( 1979). Demography of a population of Peromyscus leucopus. Canadian Journal of Zoology-Revue Canadienne de Zoologie 57, 323–328.CrossRefGoogle Scholar
Hofmeister, E. K., Ellis, B. A., Glass, G. E. and Childs, J. E. ( 1999). Longitudinal study of infection with Borrelia burgdorferi in a population of Peromyscus leucopus at a Lyme disease-enzootic site in Maryland. American Journal of Tropical Medicine and Hygiene 60, 598–609.CrossRefGoogle Scholar
Jones, C. G., Ostfeld, R. S., Richard, M. P., Schauber, E. M. and Wolff, J. O. ( 1998). Chain reactions linking acorns to gypsy moth outbreaks and Lyme disease risk. Science 279, 1023–1026.CrossRefGoogle Scholar
Keeling, M. J. and Gilligan, C. A. ( 2000). Bubonic plague: a metapopulation model of a zoonosis. Proceedings of the Royal Society of London, B 267, 2219–2230.CrossRefGoogle Scholar
Kilpatrick, H. J., Spohr, S. M. and Lima, K. K. ( 2001). Effects of population reduction on home ranges of female white-tailed deer at high densities. Canadian Journal of Zoology-Revue Canadienne De Zoologie 79, 949–954.CrossRefGoogle Scholar
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 Scholar
Lederer, S., Brenner, C., Stehle, T., Gern, L., Wallich, R. and Simon, M. M. ( 2005). Quantitative analysis of Borrelia burgdorferi gene expression in naturally (tick) infected mouse strains. Medical Microbiology and Immunology 194, 81–90.CrossRefGoogle Scholar
Levene, H. ( 1953). Genetic equilibrium when more than one ecological niche is available. American Naturalist 87, 331–333.CrossRefGoogle Scholar
Levin, M. L. and Fish, D. ( 2000). Immunity reduces reservoir host competence of Peromyscus leucopus for Ehrlichia phagocytophila. Infection and Immunity 68, 1514–1518.CrossRefGoogle Scholar
Levin, M. L. and Ross D. E. ( 2004). Acquisition of different isolates of Anaplasma phagocytophilum by Ixodes scapularis from a model animal. Vector Borne Zoonotic Diseases 4, 53–59.CrossRefGoogle Scholar
Levin, M. L., des Vignes, F. and Fish, D. ( 1999). Disparity in the natural cycles of Borrelia burgdorferi and the agent of human granulocytic ehrlichiosis. Emerging Infectious Diseases 5, 204–208.CrossRefGoogle Scholar
Levine, J. F., Wilson, M. L. and Spielman, A. ( 1985). Mice as reservoirs of the Lyme disease spirochete. American Journal of Tropical Medicine and Hygiene 34, 355–360.CrossRefGoogle Scholar
Lewellen, R. H. and Vessey, S. H. ( 1998). The effect of density dependence and weather on population size of a polyvoltine species. Ecological Monographs 68, 571–594.CrossRefGoogle Scholar
Liang, F. T., Yan, J., Mbow, M. L., Sviat, S. L., Gilmore, R. D., Mamula, M. and Fikrig, E. ( 2004). Borrelia burgdorferi changes its surface antigenic expression in response to host immune responses. Infection and Immunity 72, 5759–5767.CrossRefGoogle Scholar
Lindsay, L. R., Barker, I. K., Surgeoner, G. A., McEwen, S. A. and Campbell, G. D. ( 1997). Duration of Borrelia burgdorferi infectivity in white-footed mice for the tick vector Ixodes scapularis under laboratory and field conditions in Ontario. Journal of Wildlife Diseases 33, 766–775.CrossRefGoogle Scholar
Lindsay, L. R., Mathison, S. W., Barker, I. K., McEwen, S. A., Gillespie, T. J. and Surgeoner, G. A. ( 1999). Microclimate and habitat in relation to Ixodes scapularis (Acari: Ixodidae) populations on Long Point, Ontario, Canada. Journal of Medical Entomology 36, 255–262.CrossRefGoogle Scholar
Linzey, A. V. and Kesner, M. H. ( 1991). Population regulation in white-footed mice (Peromyscus leucopus) in a suboptimal habitat. Canadian Journal of Zoology-Revue Canadienne de Zoologie 69, 76–81.CrossRefGoogle Scholar
Liveris, D., Wang, G., Girao, G., Byrne, D. W., Nowakowski, J., McKenna, D., Nadelman, R., Wormser, G. P. and Schwartz, I. ( 2002). Quantitative detection of Borrelia burgdorferi in 2-millimeter skin samples of erythema migrans lesions: correlation of results with clinical and laboratory findings. Journal of Clinical Microbiology 40, 1249–1253.CrossRefGoogle Scholar
LoGiudice, K., Ostfeld, R. S., Schmidt, K. A. and Keesing, F. ( 2003). The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. Proceedings of the National Academy of Sciences, USA 100, 567–571.CrossRefGoogle Scholar
Massung, R. F., Priestly, R. A. and Levin, M. L. ( 2004). Transmission route and kinetics of Anaplasma phagocytophilum infection in the white-footed mouse Peromyscus leucopus. Vector-Borne Zoonotic Diseases 4, 310–318.CrossRefGoogle Scholar
Mather, T. N., Wilson, M. L., Moore, S. I., Ribeiro, J. M. and Spielman, A. ( 1989). Comparing the relative potential of rodents as reservoirs of the Lyme disease spirochete (Borrelia burgdorferi). American Journal of Epidemiology 130, 143–150.CrossRefGoogle Scholar
Mather, T. N., Telford, S. R. 3rd, Moore, S. I. and Spielman, A. ( 1990). Borrelia burgdorferi and Babesia microti: efficiency of transmission from reservoirs to vector ticks (Ixodes dammini). Experimental Parasitology 70, 55–61.CrossRefGoogle Scholar
Millar, J. S. and Gyug, L. W. ( 1981). Initiation of breeding by northern Peromyscus in relation to temperature. Canadian Journal of Zoology-Revue Canadienne de Zoologie 59, 1094–1098.CrossRefGoogle Scholar
Nadeau, J. H., Lombardi, R. T. and Tamarin, R. H. ( 1981). Population-structure and dispersal of Peromyscus leucopus on Muskeget island. Canadian Journal of Zoology-Revue Canadienne de Zoologie 59, 793–799.CrossRefGoogle Scholar
Nelson, D. E., Virok, D. P., Wood, H., Roshick, C., Johnson, R. M., Whitmire, W. M., Crane, D. D., Steele-Mortimer, O., Kari, L., McClarty, G. and Caldwell, H. D. ( 2005). Chlamydial IFN-gamma immune evasion is linked to host infection tropism. Proceedings of the National Academy of Sciences, USA 102, 10658–10663.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 Scholar
O'Callaghan, C. J., Medley, G. F., Peter, T. F. and Perry, B. D. ( 1998). Investigating the epidemiology of heartwater (Cowdria ruminantium infection) by means of a transmission dynamics model. Parasitology 117, 49–61.CrossRefGoogle Scholar
Ogden, N. H., Nuttall, P. A. and Randolph, S. E. ( 1997). Natural Lyme disease cycles maintained via sheep by cofeeding ticks. Parasitology 115, 591–599.CrossRefGoogle Scholar
Ogden, N. H., Casey, A. N. J., Woldehiwet, Z. and French, N. P. ( 2003). Transmission of Anaplasma phagocytophilum to Ixodes ricinus ticks from sheep in the acute and post-acute phase of infection. Infection and Immunity 71, 2071–2078.CrossRefGoogle Scholar
Ogden, N. H., Lindsay, L. R., Beauchamp, G., Charron, D., Maarouf, A., O'Callaghan, C. J., Waltner-Toews D. and Barker, I. K. ( 2004). Investigation of the relationships between temperature and development rates of the tick Ixodes scapularis (Acari: Ixodidae) in the laboratory and field. Journal of Medical Entomology 41, 622–633.CrossRefGoogle Scholar
Ogden, N. H., Bigras-Poulin, M., O'Callaghan, C. J., Barker, I. K., Lindsay, L. R., Maarouf, A., Smoyer-Tomic, K. E., Waltner-Toews, D. and Charron, D. ( 2005). A dynamic population model to investigate effects of climate on geographic range and seasonality of the tick Ixodes scapularis. International Journal for Parasitology 35, 375–389.CrossRefGoogle Scholar
Ogden, N. H., Maarouf, A., Barker, I. K., Bigras-Poulin, M., Lindsay, L. R., Morshed M. G., O'Callaghan, C. J., Ramay, F., Waltner-Toews, D. and Charron, D. F. ( 2006). Projections for range expansion of the Lyme disease vector Ixodes scapularis, in response to climate change. International Journal for Parasitology 36, 63–70.CrossRefGoogle Scholar
Pancholi, P., Kolbert, C. P., Mitchell, P. D., Reed, K. D. Jr, Dumler, J. S., Bakken, J. S., Telford, S. R. 3rd and Persing, D. H. ( 1995). Ixodes dammini as a potential vector of human granulocytic ehrlichiosis. Journal of Infectious Diseases 172, 1007–1012.CrossRefGoogle Scholar
Peterson, S. and Richmond, B. ( 1997). Stella Technical Documentation, High Performance Systems, Inc., 13.2–13.5.
Porco, T. C. ( 1999). A mathematical model of the ecology of Lyme disease. IMA Journal of Mathematics Applied in Medicine and Biology 16, 261–296.CrossRefGoogle Scholar
Randolph, S. E. ( 2001). The shifting landscape of tick-borne zoonoses: tick-borne encephalitis and Lyme borreliosis in Europe. Philosophical Transactions of the Royal Society, B. 356, 1045–1056.CrossRefGoogle Scholar
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 Scholar
Randolph, S. E., Mikslová, D., 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 Scholar
Randolph, S. E., Green, R. M., Peacey, M. F. and Rogers, D. J. ( 2000). Seasonal synchrony: the key to tick-borne encephalitis foci identified by satellite data. Parasitology 121, 15–23.CrossRefGoogle Scholar
Richter, D., Allgower, R. and Matuschka, F. R. ( 2002). Cofeeding transmission and its contribution to the perpetuation of the lyme disease spirochete Borrelia afzelii. Emerging Infectious Diseases 8, 1421–1425.CrossRefGoogle Scholar
Rintamaa, D. L., Mazur, P. A. and Vessey, S. H. ( 1976). Reproduction during two annual cycles in a population of Peromyscus leucopus noveboracensis. Journal of Mammalogy 57, 593–595.CrossRefGoogle Scholar
Schauber, E. M. and Ostfeld, R. S. ( 2002). Modeling the effects of reservoir competence decay and demographic turnover in Lyme disease ecology. Ecological Applications 12, 1142–1162.CrossRefGoogle Scholar
Schmidt, K. A., Ostfeld, R. S. and Schauber, E. M. ( 1999). Infestation of Peromyscus leucopus and Tamias striatus by Ixodes scapularis (Acari: Ixodidae) in relation to the abundance of hosts and parasites. Journal of Medical Entomology 36, 749–757.CrossRefGoogle Scholar
Schug, M. D., Vessey, S. H. and Korytko, A. I. ( 1991). Longevity and survival in a population of white-footed mice (Peromyscus leucopus). Journal of Mammalogy 72, 360–366.CrossRefGoogle Scholar
Schwan, T. G., Kime, K. K., Schrumpf, M. E., Coe, J. E. and Simpson, W. J. ( 1989). Antibody response in white footed mice (Peromyscus leucopus) experimentally infected with the Lyme disease spirochaete (Borrelia burgdorferi). Infection and Immunity 57, 3445–3451.Google Scholar
Stafford, K. C. 3rd, Massung, R. F., Magnarelli, L. A., Ijdo, J. W. and Anderson, J. F. ( 1999). Infection with agents of human granulocytic ehrlichiosis, Lyme disease, and babesiosis in wild white-footed mice (Peromyscus leucopus) in Connecticut. Journal of Clinical Microbiology 37, 2887–2892.Google Scholar
Steere, A. C., Coburn, J. and Glickstein, L. ( 2004). The emergence of Lyme disease. Journal of Clinical Investigation 113, 1093–1101.CrossRefGoogle Scholar
Terman, C. R. and Terman, J. R. ( 1999). Early summer reproductive hiatus in wild adult white-footed mice. Journal of Mammalogy 80, 1251–1256.CrossRefGoogle Scholar
Thompson, C., Spielman, A. and Krause, P. J. ( 2001). Coinfecting deer-associated zoonoses: Lyme disease, babesiosis, and ehrlichiosis. Clinical Infectious Diseases 33, 676–685.CrossRefGoogle Scholar
Tsao, J. I., Wootton, J. T., Bunikis, J., Luna, M. G., Fish, D. and Barbour, A. G. ( 2004). An ecological approach to preventing human infection: vaccinating wild mouse reservoirs intervenes in the Lyme disease cycle. Proceedings of the National Academy of Sciences, USA 101, 18159–18164.CrossRefGoogle Scholar
Wang, G., Ojaimi, C., Wu, H., Saksenberg, V., Iyer, R., Liveris, D., McClain, S. A., Wormser, G. P. and Schwartz, I. ( 2002). Disease severity in a murine model of Lyme borreliosis is associated with the genotype of the infecting Borrelia burgdorferi sensu stricto strain. Journal of Infectious Diseases 186, 782–791.CrossRefGoogle Scholar
Wilson, M. L. and Spielman, A. ( 1985). Seasonal activity of immature Ixodes dammini (Acari: Ixodidae). Journal of Medical Entomology 26, 408–414.CrossRefGoogle Scholar
Wolff, J. O. ( 1985). Comparative population ecology of Peromyscus leucopus and Peromyscus maniculatus. Canadian Journal of Zoology-Revue Canadienne de Zoologie 63, 1548–1555.CrossRefGoogle Scholar
Yunger, J. A. ( 2002). Response of two low-density populations of Peromyscus leucopus to increased food availability. Journal of Mammalogy 83, 267–279.2.0.CO;2>CrossRefGoogle Scholar
Yuval, B. and Spielman, A. ( 1990). Duration and regulation of the developmental cycle of Ixodes dammini (Acari: Ixodidae). Journal of Medical Entomology 27, 196–201.CrossRefGoogle Scholar