Skip to main content Accessibility help
×
×
Home

Co-feeding transmission in Lyme disease pathogens

  • MAARTEN J. VOORDOUW (a1)

Summary

This review examines the phenomenon of co-feeding transmission in tick-borne pathogens. This mode of transmission is critical for the epidemiology of several tick-borne viruses but its importance for Borrelia burgdorferi sensu lato, the causative agents of Lyme borreliosis, is still controversial. The molecular mechanisms and ecological factors that facilitate co-feeding transmission are therefore examined with particular emphasis on Borrelia pathogens. Comparison of climate, tick ecology and experimental infection work suggests that co-feeding transmission is more important in European than North American systems of Lyme borreliosis, which potentially explains why this topic has gained more traction in the former continent than the latter. While new theory shows that co-feeding transmission makes a modest contribution to Borrelia fitness, recent experimental work has revealed new ecological contexts where natural selection might favour co-feeding transmission. In particular, co-feeding transmission might confer a fitness advantage in the Darwinian competition among strains in mixed infections. Future studies should investigate the ecological conditions that favour the evolution of this fascinating mode of transmission in tick-borne pathogens.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Co-feeding transmission in Lyme disease pathogens
      Available formats
      ×

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Co-feeding transmission in Lyme disease pathogens
      Available formats
      ×

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Co-feeding transmission in Lyme disease pathogens
      Available formats
      ×

Copyright

This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.

Corresponding author

* Corresponding author. Institute of Biology, Laboratory of Ecology and Evolution of Parasites, University of Neuchâtel, Emile Argand 11, 2000 Neuchâtel, Switzerland. E-mail: maarten.voordouw@unine.ch

References

Hide All
Alekseev, A. N. and Chunikhin, S. P. (1990). The exchange of the tick-borne encephalitis virus between ixodid ticks feeding jointly on animals with a subthreshold level of viremia. Meditsinskaia Parazitologiia (Mosk) 2, 4850.
Andersson, M., Scherman, K., Raberg, L. and Råberg, L. (2013). Multiple-strain infections of Borrelia afzelii: a role for within-host interactions in the maintenance of antigenic diversity? The American Naturalist 181, 545554.
Baranton, G., Seinost, G., Theodore, G., Postic, D. and Dykhuizen, D. (2001). Distinct levels of genetic diversity of Borrelia burgdorferi are associated with different aspects of pathogenicity. Research in Microbiology 152, 149156.
Barthold, S. W. (1999). Specificity of infection-induced immunity among Borrelia burgdorferi sensu lato species. Infection and Immunity 67, 3642.
Brisson, D. and Dykhuizen, D. E. (2004). ospC diversity in Borrelia burgdorferi: different hosts are different niches. Genetics 168, 713722.
Brossard, M. and Wikel, S. K. (2004). Tick immunobiology. Parasitology 129(Suppl), S161176.
Brunner, J. L. and Ostfeld, R. S. (2008). Multiple causes of variable tick burdens on small-mammal hosts. Ecology 89, 22592272.
Bunikis, J., Tsao, J., Luke, C. J., 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, 15151523.
Burri, C., Bastic, V., Maeder, G., Patalas, E. and Gern, L. (2011). Microclimate and the zoonotic cycle of tick-borne encephalitis virus in Switzerland. Journal of Medical Entomology 48, 615627.
Charon, N., Cockburn, A., Li, C., Liu, J., Miller, K., Miller, M., Motaleb, M. and Wolgemuth, C. (2012). The unique paradigm of spirochete motility and chemotaxis. Annual Review of Microbiology 66, 349370.
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.
Daniels, T. J. and Fish, D. (1990). Spatial distribution and dispersal of unfed larval Ixodes dammini (Acari, Ixodidae) in southern New York. Environmental Entomology 19, 10291033.
Derdakova, M., Dudioak, 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, 67836788.
Devevey, G. and Brisson, D. (2012). The effect of spatial heterogeneity on the aggregation of ticks on white-footed mice. Parasitology 139, 915925.
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, 9296.
Gatewood, A. G., Liebman, K. A., Vourc'h, G., Bunikis, J., Hamer, S. A., Cortinas, R., Melton, F., Cislo, P., Kitron, U., Tsao, J., Barbour, A. G., Fish, D. and Diuk-Wasser, M. A. (2009). Climate and tick seasonality are predictors of Borrelia burgdorferi genotype distribution. Applied and Environmental Microbiology 75, 24762483.
Gern, L. and Humair, P. F. (1998). Natural history of Borrelia burgdorferi sensu lato. Wiener Klinische Wochenschrift 110, 856858.
Gern, L. and Humair, P.-F. (2002). Ecology of Borrelia burgdorferi sensu lato in Europe. In Lyme Borreliosis: Biology, Epidemiology, and Control (ed. Gray, J. S., Kahl, O., Lane, R. S. and Stanek, G.), pp. 149174. CABI Publishing, Wallingford, Oxfordshire, UK.
Gern, L. and Rais, O. (1996). Efficient transmission of Borrelia burgdorferi between cofeeding Ixodes ricinus ticks (Acari: Ixodidae). Journal of Medical Entomology 33, 189192.
Gern, L., Schaible, U. E. and Simon, M. M. (1993). Mode of inoculation of the Lyme disease agent Borrelia burgdorferi influences infection and immune responses in inbred strains of mice. Journal of Infectious Diseases 167, 971975.
Gern, L., Siegenthaler, M., Hu, C. M., Leuba-Garcia, S., Humair, P. F. and Moret, J. (1994). Borrelia burgdorferi in rodents (Apodemus flavicollis and A. sylvaticus): duration and enhancement of infectivity for Ixodes ricinus ticks. European Journal of Epidemiology 10, 7580.
Gern, L., Estrada-Pena, A., Frandsen, F., Gray, J. S., Jaenson, T. G. T., 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 Virology Parasitology and Infectious Diseases 287, 196204.
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.
Guo, X., Booth, C., Paley, M., Wang, X., DePonte, K., Fikrig, E., Narasimhan, S. and Montgomery, R. (2009). Inhibition of neutrophil function by two tick salivary proteins. Infection and Immunity 77, 23202329.
Hanincova, K., Schafer, S. M., Etti, S., Sewell, H. S., Taragelova, V., Ziak, D., Labuda, M. and Kurtenbach, K. (2003 a). Association of Borrelia afzelii with rodents in Europe. Parasitology 126, 1120.
Hanincova, K., Taragelova, V., Koci, J., Schafer, S. M., Hails, R., Ullmann, A. J., Piesman, J., Labuda, M. and Kurtenbach, K. (2003 b). Association of Borrelia garinii and B. valaisiana with songbirds in Slovakia. Applied and Environmental Microbiology 69, 28252830.
Hanincova, K., Ogden, N. H., Diuk-Wasser, M., Pappas, C. J., Iyer, R., Fish, D., Schwartz, I. and Kurtenbach, K. (2008). Fitness variation of Borrelia burgdorferi sensu stricto strains in mice. Applied and Environmental Microbiology 74, 153157.
Harrison, A. and Bennett, N. (2012). The importance of the aggregation of ticks on small mammal hosts for the establishment and persistence of tick-borne pathogens: an investigation using the R(0) model. Parasitology 139, 16051613.
Harrison, A., Montgomery, W. I. and Bown, K. J. (2011). Investigating the persistence of tick-borne pathogens via the R-0 model. Parasitology 138, 896905.
Hartemink, N. A., Randolph, S. E., Davis, S. A. and Heesterbeek, J. A. P. (2008). The basic reproduction number for complex disease systems: defining R-0 for tick-borne infections. American Naturalist 171, 743754.
Hasle, G. (2013). Transport of ixodid ticks and tick-borne pathogens by migratory birds. Frontiers in Cellular and Infection Microbiology 3, 48.
Herrmann, C., Gern, L. and Voordouw, M. (2013). Species co-occurrence patterns among Lyme borreliosis pathogens in the tick vector Ixodes ricinus . Applied and Environmental Microbiology, 79, 72737280.
Higgs, S., Schneider, B. S., Vanlandingham, D. L., Klingler, K. A. and Gould, E. A. (2005). Nonviremic transmission of West Nile virus. Proceedings of the National Academy of Sciences of the United States of America 102, 88718874.
Hu, C. M., Cheminade, Y., Perret, J. L., Weynants, V., Lobet, Y. and Gern, L. (2003). Early detection of Borrelia burgdorferi sensu lato infection in Balb/c mice by co-feeding Ixodes ricinus ticks. International Journal of Medical Microbiology 293, 421426.
Huegli, D., Hu, C. M., Humair, P. F., Wilske, B. and Gern, L. (2002). Apodemus species mice are reservoir hosts of Borrelia garinii OspA serotype 4 in Switzerland. Journal of Clinical Microbiology 40, 47354737.
Hughes, V. L. and Randolph, S. E. (2001). Testosterone depresses innate and acquired resistance to ticks in natural rodent hosts: a force for aggregated distributions of parasites. The Journal of Parasitology 87, 4954.
Humair, P. F. and Gern, L. (1998). Relationship between Borrelia burgdorferi sensu lato species, red squirrels (Sciurus vulgaris) and Ixodes ricinus in enzootic areas in Switzerland. Acta Tropica 69(3), 213227.
Humair, P. F. and Gern, L. (2000). The wild hidden face of Lyme borreliosis in Europe. Microbes and Infection 2, 915922.
Humair, P. F., Péter, O., Wallich, R. and Gern, L. (1995). Strain variation of Lyme disease spirochetes isolated from Ixodes ricinus ticks and rodents collected in two endemic areas in Switzerland. Journal of Medical Entomology 32, 433438.
Humair, P. F., Postic, D., Wallich, R. and Gern, L. (1998). An avian reservoir (Turdus merula) of the Lyme borreliosis spirochetes. Zentralblatt Fur Bakteriologie – International Journal of Medical Microbiology Virology Parasitology and Infectious Diseases 287, 521538.
Jaenson, T. G. T. and Talleklint, L. (1992). Incompetence of roe deer as reservoirs of the Lyme borreliosis spirochete. Journal of Medical Entomology 29, 813817.
Johnson, R. C., Kodner, C. and Russell, M. (1986 a). Active immunization of hamsters against experimental infection with Borrelia burgdorferi . Infection and Immunity 54, 897898.
Johnson, R. C., Kodner, C. and Russell, M. (1986 b). Passive immunization of hamsters against experimental infection with the Lyme disease spirochete. Infection and Immunity 53, 713714.
Jones, L. D., Davies, C. R., Steele, G. M. and Nuttall, P. A. (1987). A novel mode of arbovirus transmission involving a nonviremic host. Science 237, 775777.
Keesing, F., Brunner, J., Duerr, S., Killilea, M., LoGiudice, K., Schmidt, K., Vuong, H. and Ostfeld, R. S. (2009). Hosts as ecological traps for the vector of Lyme disease. Proceedings of the Royal Society Biological Sciences Series B 267, 39113919.
Kiffner, C., Lodige, C., Alings, M., Vor, T. and Ruhe, F. (2011). Attachment site selection of ticks on roe deer, Capreolus capreolus . Experimental and Applied Acarology 53, 7994.
Kimura, K., Isogai, E., Isogai, H., Kamewaka, Y., Nishikawa, T., Ishii, N. and Fujii, N. (1995). Detection of Lyme disease spirochetes in the skin of naturally infected wild sika deer (Cervus nippon yesoensis) by PCR. Applied and Environmental Microbiology 61, 16411642.
Kjelland, V., Ytrehus, B., Vikoren, T., Stuen, S., Skarpaas, T., Vikørren, T. and Slettan, A. (2011). Borrelia burgdorferi sensu lato detected in skin of Norwegian mountain hares (Lepus timidus) without signs of dissemination. Journal of Wildlife Diseases 47, 293299.
Kocan, K. and de la Fuente, J. (2003). Co-feeding studies of ticks infected with Anaplasma marginale . Veterinary Parasitology 112, 295305.
Kurtenbach, K., Peacey, M., Rijpkema, S. G. T., Hoodless, A. N., Nuttall, P. A. and Randolph, S. E. (1998 a). Differential transmission of the genospecies of Borrelia burgdorferi sensu lato by game birds and small rodents in England. Applied and Environmental Microbiology 64, 11691174.
Kurtenbach, K., Sewell, H. S., Ogden, N. H., Randolph, S. E. and Nuttall, P. A. (1998 b). Serum complement sensitivity as a key factor in Lyme disease ecology. Infection and Immunity 66, 12481251.
Kurtenbach, K., De Michelis, S., Sewell, H. S., Etti, S., Schafer, S. M., Hails, R., Collares-Pereira, M., Santos-Reis, M., Hanincova, K., Labuda, M., Bormane, A. and Donaghy, M. (2001). Distinct combinations of Borrelia burgdorferi sensu lato genospecies found in individual questing ticks from Europe. Applied and Environmental Microbiology 67, 49264929.
Kurtenbach, K., De Michelis, S., Etti, S., Schafer, S. M., Sewell, H. S., Brade, V. and Kraiczy, P. (2002 a). Host association of Borrelia burgdorferi sensu lato – the key role of host complement. Trends in Microbiology 10, 7479.
Kurtenbach, K., Schafer, S. M., Sewell, H. S., Peacey, M., Hoodless, A., Nuttall, P. A. and Randolph, S. E. (2002 b). Differential survival of Lyme borreliosis spirochetes in ticks that feed on birds. Infection and Immunity 70, 58935895.
Kurtenbach, K., Hanincova, K., Tsao, J. I., Margos, G., Fish, D. and Ogden, N. H. (2006). Fundamental processes in the evolutionary ecology of Lyme borreliosis. Nature Reviews Microbiology 4, 660669.
Kuthejlová, M., Kopecky, J., Stepanova, G., Macela, A., Kopecký, J. and Stepánová, G. (2001). Tick salivary gland extract inhibits killing of Borrelia afzelii spirochetes by mouse macrophages. Infection and Immunity 69, 575578.
Labuda, M., Kozuch, O., Eleckova, E., Williams, T., Nuttall, P. A., Elecková, E., Zuffová, E. and Sabó, A. (1993 a). Non-viraemic transmission of tick-borne encephalitis virus: a mechanism for arbovirus survival in nature. Experientia 49, 802805.
Labuda, M., Williams, T., Danielova, V., Jones, L. D. and Nuttall, P. A. (1993 b). Efficient transmission of tick-borne encephalitis virus between cofeeding ticks. Journal of Medical Entomology 30, 295299.
Labuda, M., Williams, T., Jones, L. D. and Nuttall, P. A. (1993 c). Enhancement of tick-borne encephalitis virus transmission by tick salivary gland extracts. Medical and Veterinary Entomology 7, 193196.
Labuda, M., Zuffova, E., Kozuch, O., Fuchsberger, N., Austyn, J. M., Lysy, J. and Nuttall, P. A. (1996). Importance of localized skin infection in tick-borne encephalitis virus transmission. Virology 219, 357366.
Labuda, M., Kozuch, O., Zuffova, E., Eleckova, E., Hails, R. S. and Nuttall, P. A. (1997). Tick-borne encephalitis virus transmission between ticks cofeeding on specific immune natural rodent hosts. Virology 235, 138143.
Levin, M. L. and Fish, D. (2000). Immunity reduces reservoir host competence of Peromyscus leucopus for Ehrlichia phagocytophila . Infection and Immunity 68, 15141518.
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, 766775.
MacQueen, D., Lubelczyk, C., Elias, S., Cahill, B., Mathers, A., Lacombe, E., Rand, P. and Smith, R. (2012). Genotypic diversity of an emergent population of Borrelia burgdorferi at a coastal Maine island recently colonized by Ixodes scapularis . Vector Borne and Zoonotic Diseases 12, 456461.
Matuschka, F. R., Heiler, M., Eiffert, H., Fischer, P., Lotter, H. and Spielman, A. (1993). Diversionary role of hoofed game in the transmission of Lyme disease spirochetes. American Journal of Tropical Medicine and Hygiene 48, 693699.
Mead, D. G., Ramberg, F. B., Besselsen, D. G. and Mare, C. J. (2000). Transmission of vesicular stomatitis virus from infected to noninfected black flies co-feeding on nonviremic deer mice. Science 287, 485487
Mejri, N., Rutti, B. and Brossard, M. (2002). Immunosuppressive effects of Ixodes ricinus tick saliva or salivary gland extracts on innate and acquired immune response of BALB/c mice. Parasitology Research 88, 192197.
Montgomery, R. R., Nathanson, M. H. and Malawista, S. E. (1993). The fate of Borrelia burgdorferi, the agent for Lyme disease, in mouse macrophages. Destruction, survival, recovery. The Journal of Immunology 150, 909915.
Morán Cadenas, F. M., Rais, O., Humair, P. F., Douet, V., Moret, J. and Gern, L. (2007). Identification of host bloodmeal source and Borrelia burgdorferi sensu lato in field-collected Ixodes ricinus ticks in Chaumont (Switzerland). Journal of Medical Entomology 44, 11091117.
Nuttall, P. A. (1999). Pathogen-tick-host interactions: Borrelia burgdorferi and TBE virus. Zentralblatt für Bakteriologie 289, 492505.
Nuttall, P. A. and Labuda, M. (2003). Dynamics of infection in tick vectors and at the tick-host interface. Flaviviruses: Pathogenesis and Immunity 60, 233272.
Nuttall, P. A. and Labuda, M. (2004). Tick-host interactions: saliva-activated transmission. Parasitology 129, S177S189.
Ogden, N. H., Nuttall, P. A. and Randolph, S. E. (1997). Natural Lyme disease cycles maintained via sheep by cofeeding ticks. Parasitology 115, 591599.
Ogden, N. H., Hailes, R. S. and Nuttall, P. A. (1998 a). Interstadial variation in the attachment sites of Ixodes ricinus ticks on sheep. Experimental and Applied Acarology 22, 227232.
Ogden, N. H., Kurtenbach, K. and Nuttall, P. A. (1998 b). Interstadial and infestation level-dependent variation in the transmission efficiency of Borrelia burgdorferi from mice to Ixodes ricinus ticks. Experimental and Applied Acarology 22, 367372.
Ogden, N. H., Bigras-Poulin, M., O'Callaghan, C. J., Barker, I. K., Kurtenbach, K., Lindsay, L. R. and Charron, D. (2007). Vector seasonality, host infection dynamics and fitness of pathogens transmitted by the tick Ixodes scapularis . Parasitology 134, 209227.
Papatheodorou, V. and Brossard, M. (1987). C-3 levels in the sera of rabbits infested and reinfested with Ixodes ricinus L and in midguts of fed ticks. Experimental and Applied Acarology 3, 5359.
Patrican, L. A. (1997). Acquisition of Lyme disease spirochetes by cofeeding Ixodes scapularis ticks. The American journal of tropical medicine and hygiene 57, 589593.
Pechová, J., Stepanova, G., Kovar, L., Kopecky, J., Kovár, L. and Kopecký, J. (2002). Tick salivary gland extract-activated transmission of Borrelia afzelii spirochaetes. Folia Parasitologica 49, 153159.
Pérez, D., Kneubühler, Y., Rais, O., Jouda, F. and Gern, L. (2011). Borrelia afzelii ospC genotype diversity in Ixodes ricinus questing ticks and ticks from rodents in two Lyme borreliosis endemic areas: contribution of co-feeding ticks. Ticks and Tick-borne Diseases 2, 137142.
Perkins, S. E., Cattadori, I. M., Tagliapietra, V., Rizzoli, A. P. and Hudson, P. J. (2003). Empirical evidence for key hosts in persistence of a tick-borne disease. International Journal for Parasitology 33, 909917.
Pichon, B., Gilot, B. and Perez-Eid, C. (2000). Detection of spirochaetes of Borrelia burgdorferi complex in the skin of cervids by PCR and culture. European Journal of Epidemiology 16, 869873.
Pichon, B., Egan, D., Rogers, M. and Gray, J. (2003). Detection and identification of pathogens and host DNA in unfed host-seeking Ixodes ricinus L. (Acari: Ixodidae). Journal of Medical Entomology 40, 723731.
Pichon, B., Rogers, M., Egan, D. and Gray, J. (2005). Blood-meal analysis for the identification of reservoir hosts of tick-borne pathogens in Ireland. Vector-Borne and Zoonotic Diseases 5, 172180.
Piesman, J. and Happ, C. M. (2001). The efficacy of co-feeding as a means of maintaining Borrelia burgdorferi: a North American model system. Journal of Vector Ecology 26, 216220.
Piesman, J., Dolan, M. C., Happ, C. M., Luft, B. J., Rooney, S. E., Mather, T. N. and Golde, W. T. (1997). Duration of immunity to reinfection with tick-transmitted Borrelia burgdorferi in naturally infected mice. Infection and Immunity 65, 40434047.
Qiu, W. G., Bosler, E. M., Campbell, J. R., Ugine, G. D., Wang, I. N., Luft, B. J. and Dykhuizen, D. E. (1997). A population genetic study of Borrelia burgdorferi sensu stricto from eastern Long Island, New York, suggested frequency-dependent selection, gene flow and host adaptation. Hereditas 127, 203216.
Qiu, W. G., Dykhuizen, D. E., Acosta, M. S. and Luft, B. J. (2002). Geographic uniformity of the Lyme disease spirochete (Borrelia burgdorferi) and its shared history with tick vector (Ixodes scapularis) in the northeastern United States. Genetics 160, 833849.
Raberg, L. (2012). Infection intensity and infectivity of the tick-borne pathogen Borrelia afzelii . Journal of Evolutionary Biology 25, 14481453.
Ramamoorthi, N., Narasimhan, S., Pal, U., Bao, F. K., Yang, X. F. F., Fish, D., Anguita, J., Norgard, M. V., Kantor, F. S., Anderson, J. F., Koski, R. A. and Fikrig, E. (2005). The Lyme disease agent exploits a tick protein to infect the mammalian host. Nature 436, 573577.
Randolph, S. E. (1975). Patterns of distribution of the tick Ixodes trianguliceps Birula on its host. Journal of Animal Ecology 44, 451474.
Randolph, S. E. (1998). Ticks are not insects: consequences of contrasting vector biology for transmission potential. Parasitology Today 14, 186192.
Randolph, S. E. (2009). Tick-borne disease systems emerge from the shadows: the beauty lies in molecular detail, the message in epidemiology. Parasitology 136, 14031413.
Randolph, S. E. (2011). Transmission of tick-borne pathogens between co-feeding ticks: Milan Labuda's enduring paradigm. Ticks and Tick-borne Diseases 2, 179182.
Randolph, S. E. and Gern, L. (2003). Co-feeding transmission and its contribution to the perpetuation of the Lyme disease spirochete Borrelia afzelii . Emerging Infectious Diseases 9, 893894.
Randolph, S. E. and Rogers, D. J. (2000). Fragle transmission cycles of tick-borne encephalitis virus may be disrupted by predicted climate change. Proceedings of the Royal Society Biological Sciences Series B 267, 17411744.
Randolph, S. E. and Sumilo, D. (2007). Tick-borne encephalitis in Europe: dynamics of changing risk. In Emerging Pests and Vector-borne Diseases in Europe (ed. Takken, W. and Knols, B. G. J.), pp. 187206. Wageningen Academic Publishers, Wageningen.
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.
Rechav, Y. and Nuttall, P. A. (2000). The effect of male ticks on the feeding performance of immature stages of Rhipicephalus sanguineus and Amblyomma americanum (Acari: Ixodidae). Experimental and Applied Acarology 24, 569578.
Ribeiro, J. M. C. (1987). Ixodes dammini – salivary anti-complement activity. Experimental Parasitology 64, 347353.
Ribeiro, J. M. C. (1995). How ticks make a living. Parasitology Today 11, 9193.
Ribeiro, J. M. C. and Spielman, A. (1986). Ixodes dammini – salivary anaphylatoxin inactivating activity. Experimental Parasitology 62, 292297.
Ribeiro, J. M. C., Weis, J. J. and Telford, S. R. (1990). Saliva of the tick Ixodes dammini inhibits neutrophil function. Experimental Parasitology 70, 382388.
Richter, D., Allgower, R. and Matuschka, F. R. (2002). Co-feeding transmission and its contribution to the perpetuation of the Lyme disease spirochete Borrelia afzelii . Emerging Infectious Diseases 8, 14211425.
Richter, D., Allgower, R. and Matuschka, F. R. (2003). Co-feeding transmission and its contribution to the perpetuation of the Lyme disease spirochete Borrelia afzelii . Emerging Infectious Diseases 9, 895896.
Richter, D., Debski, A., Hubalek, Z. and Matuschka, F. R. (2012). Absence of Lyme disease spirochetes in larval Ixodes ricinus ticks. Vector-Borne and Zoonotic Diseases 12, 2127.
Rollend, L., Fish, D. and Childs, J. E. (2013). Transovarial transmission of Borrelia spirochetes by Ixodes scapularis: a summary of the literature and recent observations. Ticks and Tick-borne Diseases 4, 4651.
Rudolf, I., Hubalek, Z. and Hubálek, Z. (2003). Effect of the salivary gland and midgut extracts from Ixodes ricinus and Dermacentor reticulatus (Acari: Ixodidae) on the growth of Borrelia garinii in vitro. Folia Parasitologica 50, 159160.
Rudolf, I., Sikutova, S., Kopecky, J. and Hubalek, Z. (2010). Salivary gland extract from engorged Ixodes ricinus (Acari: Ixodidae) stimulates in vitro growth of Borrelia burgdorferi sensu lato. Journal of Basic Microbiology 50, 294298.
Sato, Y. and Nakao, M. (1997). Transmission of the Lyme disease spirochete, Borrelia garinii, between infected and uninfected immature Ixodes persulcatus during cofeeding on mice. Journal of Parasitology 83, 547550.
Scheckelhoff, M., Telford, S., Wesley, M. and Hu, L. (2007). Borrelia burgdorferi intercepts host hormonal signals to regulate expression of outer surface protein A. Proceedings of the National Academy of Sciences of the United States of America 104, 72477252.
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, 749757.
Scott, M. C., Harmon, J. R., Tsao, J. I., Jones, C. J. and Hickling, G. J. (2012). Reverse line blot probe design and polymerase chain reaction optimization for bloodmeal analysis of ticks from the eastern United States. Journal of Medical Entomology 49, 697709.
Shaw, M., Keesing, F., McGrail, R. and Ostfeld, R. (2003). Factors influencing the distribution of larval blacklegged ticks on rodent hosts. The American Journal of Tropical Medicine and Hygiene 68, 447452.
Shih, C. M., Spielman, A., Pollack, R. J. and Telford, S. R. (1992). Delayed dissemination of Lyme disease spirochetes from the site of deposition in the skin of mice. The Journal of infectious diseases 166, 827831.
Shih, C. M., Chao, L. L. and Yu, C. P. (2002). Chemotactic migration of the Lyme disease spirochete (Borrelia burgdorferi) to salivary gland extracts of vector ticks. American Journal of Tropical Medicine and Hygiene 66, 616621.
Sonenshine, D. E. (2004). Pheromones and other semiochemicals of ticks and their use in tick control. Parasitology 129(Suppl), S405425.
Stearns, S. C. (1992). The Evolution of Life-Histories. Oxford University Press, Oxford.
Steele, G. M. and Randolph, S. E. (1985). An experimental evaluation of conventional control measures against the sheep tick, Ixodes ricinus (L.) (Acari, Ixodidae). I. A unimodal seasonal activity pattern. Bulletin of Entomological Research 75, 489499.
Swanson, K. I. and Norris, D. E. (2008). Presence of multiple variants of Borrelia burgdorferi in the natural reservoir Peromyscus leucopus throughout a transmission season. Vector-Borne and Zoonotic Diseases 8, 397405.
Taragel'ová, V., Koci, J., Hanincova, K., Kurtenbach, K., Derdakova, M., Ogden, N. H., Hanincová, K., Derdáková, M., Literák, I., Kocianová, E. and Labuda, M. (2008). Blackbirds and song thrushes constitute a key reservoir of Borrelia garinii, the causative agent of borreliosis in Central Europe. Applied and Environmental Microbiology 74, 12891293.
Telford, S. R., Mather, T. N., Moore, S. I., Wilson, M. L. and Spielman, A. (1988). Incompetence of deer as reservoirs of the Lyme-disease spirochete. American Journal of Tropical Medicine and Hygiene 39, 105109.
Tonetti, N. and Gern, L. (2011). Dynamic of host-tick-host transmission of Borrelia afzelii osp C groups. In Seventh Ticks and Tick-borne Pathogens International Conference, Zaragoza, Spain.
Tsao, J. (2009). Reviewing molecular adaptations of Lyme borreliosis spirochetes in the context of reproductive fitness in natural transmission cycles. Veterinary Research (Paris) 40, 36.
Wang, G., Ojaimi, C., Iyer, R., Saksenberg, V., McClain, S. A., Wormser, G. P. and Schwartz, I. (2001 a). Impact of genotypic variation of Borrelia burgdorferi sensu stricto on kinetics of dissemination and severity of disease in C3H/HeJ mice. Infection and Immunity 69, 43034312.
Wang, H., Paesen, G. C., Nuttall, P. A. and Barbour, A. G. (1998). Male ticks help their mates to feed. Nature 391, 753754.
Wang, H., Hails, R. S., Cui, W. W. and Nuttall, P. A. (2001 b). Feeding aggregation of the tick Rhipicephalus appendiculatus (Ixodidae): benefits and costs in the contest with host responses. Parasitology 123(Pt 5), 447453.
Wang, I. N., Dykhuizen, D. E., Qiu, W., Dunn, J. J., Bosler, E. M. and Luft, B. J. (1999). Genetic diversity of ospC in a local population of Borrelia burgdorferi sensu stricto. Genetics 151, 1530.
Woolhouse, M. E., Dye, C., Smith, T., Etard, J. F., Charlwood, J. D., Garnett, G. P., Hagan, P., Hii, J. L., Ndhlovu, P. D., Quinnell, R. J., Watts, C. H., Chandiwana, S. K. and Anderson, R. M. (1997). Heterogeneities in the transmission of infectious agents: implications for the design of control programs. Proceedings of the National Academy of Sciences of the United States of America 94, 338342.
Zeidner, N. S., Gern, L., Piesman, J., Schneider, B. S. and Nuncio, M. S. (2002). Coinoculation of Borrelia spp. with tick salivary gland lysate enhances spirochete load in mice and is tick species-specific. The Journal of Parasitology 88, 12761278.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Parasitology
  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed