Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-26T20:16:06.036Z Has data issue: false hasContentIssue false
  • English
  • Français

Parasite interactions in natural populations: insights from longitudinal data

Published online by Cambridge University Press:  12 May 2008

S. TELFER ,
R. BIRTLES ,
M. BENNETT ,
X. LAMBIN ,
S. PATERSON  and
M. BEGON
S. TELFER*
Affiliation:
School of Biological Sciences, University of Liverpool, Biosciences Building, Liverpool L69 7LB, UK
R. BIRTLES
Affiliation:
Centre for Comparative Infectious Diseases, Department of Veterinary Pathology, University of Liverpool, Leahurst, Neston CH64 7TE, UK
M. BENNETT
Affiliation:
Centre for Comparative Infectious Diseases, Department of Veterinary Pathology, University of Liverpool, Leahurst, Neston CH64 7TE, UK
X. LAMBIN
Affiliation:
School of Biological Sciences, University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, UK
S. PATERSON
Affiliation:
School of Biological Sciences, University of Liverpool, Biosciences Building, Liverpool L69 7LB, UK
M. BEGON
Affiliation:
School of Biological Sciences, University of Liverpool, Biosciences Building, Liverpool L69 7LB, UK
*
*Corresponding author: School of Biological Sciences, University of Liverpool, Biosciences Building, Liverpool L69 7LB, UK. Tel: +44 151 795 4528; Fax: +44 151 794 6005; E-mail: stelfer@liv.ac.uk
Get access Rights & Permissions [Opens in a new window]

Summary

The physiological and immunological state of an animal can be influenced by current infections and infection history. Consequently, both ongoing and previous infections can affect host susceptibility to another parasite, the biology of the subsequent infection (e.g. infection length) and the impact of infection on host morbidity (pathology). In natural populations, most animals will be infected by a succession of different parasites throughout the course of their lives, with probably frequent concomitant infections. The relative timing of different infections experienced by a host (i.e. the sequence of infection events), and the effects on factors such as host susceptibility and host survival, can only be derived from longitudinal data on individual hosts. Here we review some of the evidence for the impact of co-infection on host susceptibility, infection biology and pathology focusing on insights obtained from both longitudinal studies in humans and experiments that explicitly consider the sequence of infection. We then consider the challenges posed by longitudinal infection data collected from natural populations of animals. We illustrate their usefulness using our data of microparasite infections associated with field vole (Microtus agrestis) populations to examine impacts on susceptibility and infection length. Our primary aim is to describe an analytical approach that can be used on such data to identify interactions among the parasites. The preliminary analyses presented here indicate both synergistic and antagonistic interactions between microparasites within this community and emphasise that such interactions could have significant impacts on host-parasite fitness and dynamics.

Keywords

Concomitant infectionsmixed infectionslongitudinal datainfection lengthBartonellaBabesiacowpoxAnaplasma
Type
Original Articles
Information
Parasitology , Volume 135 , Special Issue 7: Parasitic co-infections: challenges and solutions , June 2008 , pp. 767 - 781
Copyright
Copyright © 2008 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

Akaike, H. (1973). Information theory and an extension of the maximum likelihood principle. In International Symposium on Information Theory (ed. Petran, B. N. and Csaki, F.), pp. 267–281. Akademiai Kiadi, Budapest.Google Scholar
Alcami, A., Symons, J. A., Khanna, A. and Smith, G. L. (1998). Poxviruses: Capturing cytokines and chemokines. Seminars in Virology 8, 419–427.CrossRefGoogle Scholar
Arvand, M., Ignatius, R., Regnath, T., Hahn, H. and Mielke, M. A. (2001). Bartonella henselae-specific cell-mediated immune responses display a predominantly Th1 phenotype in experimentally infected C57BL/6 mice. Infection and Immunity 69, 6427–6433.CrossRefGoogle ScholarPubMed
Baxby, D. and Bennet, M. (1999). Cowpox virus (Poxviridae). In Encyclopaedia of Virology (ed. Webster, R. G. and Granoff, A.), pp. 298–304. Academic Press, London.CrossRefGoogle Scholar
Behnke, J. M., Bajer, A., Sinski, E. and Wakelin, D. (2001). Interactions involving intestinal nematodes of rodents experimental and field studies. Parasitology 122, S39–S49.CrossRefGoogle ScholarPubMed
Behnke, J. M., Gilbert, F. S., Abu-Madi, M. A. and Lewis, J. W. (2005). Do the helminth parasites of wood mice interact? Journal of Animal Ecology 74, 982–993.CrossRefGoogle Scholar
Bennett, M., Crouch, A. J., Begon, M., Duffy, B., Feore, S., Gaskell, R. M., Kelly, D. F., McCracken, C. M., Vicary, L. and Baxby, D. (1997). Cowpox in British Voles and Mice. Comparative Pathology 116, 35–44.CrossRefGoogle ScholarPubMed
Bennett, M., Smith, G. L. and Baxby, D. (2008). Cowpox. In Encyclopedia of Virology (ed. Mahy, B. and van Regenmortel, M.), (in press).Google Scholar
Birtles, R. (2005 a). Bartonellosis. In Arthropod-borne Infectious Diseases of the Dog and Cat (ed. Shaw, S. E. and Day, M. J.), pp. 110–119. Manson Publishing, London.CrossRefGoogle Scholar
Birtles, R. J. (2005 b). Bartonellae as elegant hemotropic parasites. In Rickettsioses: From Genome to Proteome, Pathobiology, and Rickettsiae as an International Threat (ed. Oteo, J. A., Hechemy, K. E., Raoult, D. A., Silverman, D. J. and Blanco, J. R.), pp. 270–279.Google Scholar
Birtles, R. J., Hazel, S. M., Bennett, M., Bown, K., Raoult, D. and Begon, M. (2001). Longitudinal monitoring of the dynamics of infections due to Bartonella species in UK woodland rodents. Epidemiology and Infection 126, 323–329.CrossRefGoogle ScholarPubMed
Booth, M. (2006). The role of residential location in apparent helminth and malaria associations. Trends in Parasitology 22, 359–362.CrossRefGoogle ScholarPubMed
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
Brouqui, P., Stein, A., Dupont, H. T., Gallian, P., Badiaga, S., Rolain, J. M., Mege, J. L., La Scola, B., Berbis, P. and Raoult, D. (2005). Ectoparasitism and vector-borne diseases in 930 homeless people from Marseilles. Medicine 84, 61–68.CrossRefGoogle ScholarPubMed
Brown, S. P. and Grenfell, B. T. (2001). An unlikely partnership: parasites, concomitant immunity and host defence. Proceedings of the Royal Society B-Biological Sciences 268, 2543–2549.CrossRefGoogle ScholarPubMed
Brown, S. P., Hochberg, M. E. and Grenfell, B. T. (2002). Does multiple infection select for raised virulence? Trends in Microbiology 10, 401–405.CrossRefGoogle ScholarPubMed
Burthe, S., Bennet, M., Kipar, A., Lambin, X., Smith, A., Telfer, S. and Begon, M. (2008 a). Tuberculosis (Mycobacterium microti) in wild field vole populations. Parasitology 135, 309–317.CrossRefGoogle ScholarPubMed
Burthe, S., Telfer, S., Begon, M., Bennet, M., Smith, A. and Lambin, X. (2008 b). Cowpox virus infection in natural field vole, Microtus agrestis, populations: significant negative impacts on survival. Journal of Animal Ecology 77, 110–119.CrossRefGoogle ScholarPubMed
Burthe, S., Telfer, S., Lambin, X., Bennett, M., Carslake, D., Smith, A. and Begon, M. (2006). Cowpox virus infection in natural field vole Microtus agrestis populations: delayed density dependence and individual risk. Journal of Animal Ecology 75, 1416–1425.CrossRefGoogle ScholarPubMed
Cam, E., Link, W. A., Cooch, E. G., Monnat, J. Y. and Danchin, E. (2002). Individual covariation in life-history traits: Seeing the trees despite the forest. American Naturalist 159, 96–105.CrossRefGoogle ScholarPubMed
Cavanagh, R. D., Lambin, X., Ergon, T., Bennett, M., Graham, I. M., van Soolingen, D. and Begon, M. (2004). Disease dynamics in cyclic populations of field voles (Microtus agrestis): cowpox virus and vole tuberculosis (Mycobacterium microti). Proceedings of the Royal Society of London Series B-Biological Sciences 271, 859–867.CrossRefGoogle ScholarPubMed
Chantrey, J., Meyer, H., Baxby, D., Begon, M., Bown, K., Feore, S., Jones, T., Montgomery, W. I. and Bennett, M. (1999). Cowpox: reservoir hosts and geographic range. Epidemiology and Infection 122, 455–460.CrossRefGoogle ScholarPubMed
Chu, C. M., Yeh, C. T. and Liaw, W. F. (1998). Low-level viremia and intracellular expression of hepatitis B surface antigen (HBsAg) in HBsAg carriers with concurrent hepatitis C virus infection. Journal of Clinical Microbiology 36, 2084–2086.CrossRefGoogle ScholarPubMed
Coleman, J. L., LeVine, D., Thill, C., Kuhlow, C. and Benach, J. L. (2005). Babesia microti and Borrelia burgdorferi follow independent courses of infection in mice. Journal of Infectious Diseases 192, 1634–1641.CrossRefGoogle ScholarPubMed
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
Cox, F. E. G. (2001). Concomitant infections, parasites and immune responses. Parasitology 122, S23–S38.CrossRefGoogle ScholarPubMed
Crespo, J., Lozano, J. L., Delacruz, F., Rodrigo, L., Rodriguez, M., Sanmiguel, G., Artinano, E. and Ponsromero, F. (1994). Prevalence and significance of Hepatitis-C Viremia in chronic active Hepatitis-B. American Journal of Gastroenterology 89, 1147–1151.Google ScholarPubMed
Crouch, A. C., Baxby, D., McCracken, C. M., Gaskell, R. M. and Bennett, M. (1995). Serological evidence for the reservoir hosts of cowpox virus in British wildlife. Epidemiology and Infection 115, 185–191.CrossRefGoogle ScholarPubMed
Curry, A. J., Else, K. J., Jones, F., Bancroft, A., Grencis, R. K. and Dunne, D. W. (1995). Evidence that cytokine-mediated immune interactions induced by Schistosoma mansoni alter disease outcome in mice concurrently infected with Trichuris muris. Journal of Experimental Medicine 181, 769–774.CrossRefGoogle ScholarPubMed
Dehio, C. (2004). Molecular and cellular basis of Bartonella pathogenesis. Annual Review of Microbiology 58, 365–390.CrossRefGoogle ScholarPubMed
Gokce, H. I. and Woldehiwet, Z. (1999). Ehrlichia (Cytoecetes) phagocytophila predisposes to severe contagious ecthyma (Orf) in lambs. Journal of Comparative Pathology 121, 227–240.CrossRefGoogle Scholar
Graham, A. L. (2002). When T-helper cells don't help: Immunopathology during concomitant infection. Quarterly Review of Biology 77, 409–434.CrossRefGoogle ScholarPubMed
Graham, A. L., Cattadori, I. M., Lloyd-Smith, J. O., Ferrari, M. J. and Bjornstad, O. N. (2007). Transmission consequences of coinfection: cytokines writ large? Trends in Parasitology 23, 284–291.CrossRefGoogle ScholarPubMed
Graham, A. L., Lamb, T. J., Read, A. F. and Allen, J. E. (2005). Malaria-filaria coinfection in mice makes malarial disease more severe unless filarial infection achieves patency. Journal of Infectious Diseases 191, 410–421.CrossRefGoogle ScholarPubMed
Harcourt, G. C., Donfield, S., Gomperts, E., Daar, E. S., Goulder, P. J. R., Phillips, R. E. and Klenerman, P. (2005). Longitudinal analysis of CD8 T-cell responses to HIV and hepatitis C virus in a cohort of co-infected haemophiliacs. AIDS 19, 1135–1143.CrossRefGoogle Scholar
Harrus, S., Waner, T., Bjoersdorff, S. and Shaw, S. E. (2005). Ehrlichiosis and anaplasmosis. In Arthropod-borne Infectious Diseases of the Dog and Cat (ed. Shaw, S. E. and Day, M. J.), pp. 120–133. Manson Publishing, London.CrossRefGoogle Scholar
Hodgson, D. J., Hitchman, R. B., Vanbergen, A. J., Hails, R. S., Possee, R. D. and Cory, J. S. (2004). Host ecology determines the relative fitness of virus genotypes in mixed-genotype nucleopolyhedrovirus infections. Journal of Evolutionary Biology 17, 1018–1025.CrossRefGoogle ScholarPubMed
Hoffman, I. F., Jere, C. S., Taylor, T. E., Munthali, P., Dyer, J. R., Wirima, J. J., Rogerson, S. J., Kumwenda, N., Eron, J. J., Fiscus, S. A., Chakraborty, H., Taha, T. E., Cohen, M. S. and Molyneux, M. E. (1999). The effect of Plasmodium falciparum malaria on HIV-1 RNA blood plasma concentration. AIDS 13, 487–494.CrossRefGoogle ScholarPubMed
Hofmann-Lehmann, R., Meli, M. L., Dreher, U. M., Gonczi, E., Deplazes, P., Braun, U., Engels, M., Schupbach, J., Jorger, K., Thoma, R., Griot, C., Stark, K. D. C., Willi, B., Schmidt, J., Kocan, K. M. and Lutz, H. (2004). Concurrent infections with vector-borne pathogens associated with fatal hemolytic anemia in a cattle herd in Switzerland. Journal of Clinical Microbiology 42, 3775–3780.CrossRefGoogle Scholar
Hudson, P. J., Dobson, A. P. and Newborn, D. (1998). Prevention of population cycles by parasite removal. Science 282, 2256–2258.CrossRefGoogle ScholarPubMed
Irwin, P. (2005). Babesiosis and cytauxzoonosis. In Arthropod-borne Infectious Diseases of the Dog and Cat (ed. Shaw, S. E. and Day, M. J.), pp. 63–77. Manson Publishing, London.CrossRefGoogle Scholar
Ishii, T., Takatsuka, J., Nakai, M. and Kunimi, Y. (2002). Growth characteristics and competitive abilities of a nucleopolyhedrovirus and an entomopox virus in larvae of the smaller tea tortrix, Adoxophyes honmai (Lepidoptera: Tortricidae). Biological Control 23, 96–105.CrossRefGoogle Scholar
Jackson, J. A., Pleass, R. J., Cable, J., Bradley, J. E. and Tinsley, R. C. (2006). Heterogenous interspecific interactions in a host-parasite system. International Journal for Parasitology 36, 1341–1349.CrossRefGoogle Scholar
Jacobson, L. P., Jenkins, F. J., Springer, G., Munoz, A., Shah, K. V., Phair, J., Zhang, Z. F. and Armenian, H. (2000). Interaction of human immunodeficiency virus type 1 and human herpesvirus type 8 infections on the incidence of Kaposi's sarcoma. Journal of Infectious Diseases 181, 1940–1949.CrossRefGoogle ScholarPubMed
Johnson, J. B. and Omland, K. S. (2004). Model selection in ecology and evolution. Trends in Ecology & Evolution 19, 101–108.CrossRefGoogle ScholarPubMed
Kabeya, H., Sase, M., Yamashita, M. and Maruyama, S. (2006). Predominant T helper 2 immune responses against Bartonella henselae in naturally infected cats. Microbiology and Immunology 50, 171–178.CrossRefGoogle ScholarPubMed
Kabeya, H., Yamasaki, A., Ikariya, M., Negishi, R., Chomel, B. B. and Maruyama, S. (2007). Characterization of Th1 activation by Bartonella henselae stimulation in BALB/c mice: Inhibitory activities of interleukin-10 for the production of interferon-gamma in spleen cells. Veterinary Microbiology 119, 290–296.CrossRefGoogle ScholarPubMed
Kamya, M. R., Gasasira, A. F., Yeka, A., Bakyaita, N., Nsobya, S. L., Francis, D., Rosenthal, P. J., Dorsey, G. and Havlir, D. (2006). Effect of HIV-1 infection on antimalarial treatment outcomes in Uganda: A population-based study. Journal of Infectious Diseases 193, 9–15.CrossRefGoogle ScholarPubMed
Kellerman, S. E., Hanson, D. L., McNaghten, A. D. and Fleming, P. L. (2003). Prevalence of chronic hepatitis B and incidence of acute hepatitis B infection in human immunodeficiency virus-infected subjects. Journal of Infectious Diseases 188, 571–577.CrossRefGoogle ScholarPubMed
Koblin, B. A., Taylor, P. E., Rubinstein, P. and Stevens, C. E. (1992). Effect of duration of hepatitis-B virus infection on the association between Human-Immunodeficiency-Virus Type-1 and hepatitis-B viral replication. Hepatology 15, 590–592.CrossRefGoogle ScholarPubMed
Koesling, J., Aebischer, T., Falch, C., Schulein, R. and Dehio, C. (2001). Cutting edge: Antibody-mediated cessation of hemotropic infection by the intraerythrocytic mouse pathogen Bartonella grahamii. Journal of Immunology 167, 11–14.CrossRefGoogle ScholarPubMed
Kosoy, M. Y., Regnery, R. L., Kosaya, O. I. and Childs, J. E. (1999). Experimental infection of cotton rats with three naturally occurring Bartonella species. Journal of Wildlife Diseases 35, 275–284.CrossRefGoogle ScholarPubMed
Kosoy, M. Y., Regnery, R. L., Tzianabos, T., Marston, E. L., Jones, D. C., Green, D., Maupin, G. O., Olson, J. G. and Childs, J. E. (1997). Distribution, diversity, and host specificity of Bartonella in rodents from the southeastern United States. American Journal of Tropical Medicine and Hygiene 57, 578–588.CrossRefGoogle ScholarPubMed
Krause, P. J., McKay, K., Thompson, C. A., Sikand, V. K., Lentz, R., Lepore, T., Closter, L., Christianson, D., Telford, S. R., Persing, D., Radolf, J. D. and Spielman, A. (2002). Disease-specific diagnosis of coinfecting tickborne zoonoses: Babesiosis, human granulocytic ehrlichiosis, and Lyme disease. Clinical Infectious Diseases 34, 1184–1191.CrossRefGoogle ScholarPubMed
Krause, P. J., Telford, S. R., Spielman, A., Sikand, V., Ryan, R., Christianson, D., Burke, G., Brassard, P., Pollack, R., Peck, J. and Persing, D. H. (1996). Concurrent lyme disease and babesiosis – Evidence for increased severity and duration of illness. Jama-Journal of the American Medical Association 275, 1657–1660.CrossRefGoogle ScholarPubMed
Lello, J., Boag, B., Fenton, A., Stevenson, I. R. and Hudson, P. J. (2004). Competition and mutualism among the gut helminths of a mammalian host. Nature 428, 840–844.CrossRefGoogle ScholarPubMed
Malakar, R., Elkinton, J. S., Hajek, A. E. and Burand, J. P. (1999). Within–host interaction of Lymantria dispar (Lepidoptera: Lymantriidae) nucleopolyhedrosis virus and Entomophaga maimaiga (Zygomycetes: Entomophthorales). Journal of Invertebrate Pathology 73, 91–100.CrossRefGoogle ScholarPubMed
Maizels, R. M. and Yazdanbakhsh, M. (2003). Immune regulation by helminth parasites: cellular and molecular mechanisms. Nature Reviews Immunology 3, 733–744.CrossRefGoogle ScholarPubMed
May, R. M. and Nowak, M. A. (1994). Superinfection, metapopulation dynamics and the evolution of diversity. Journal of Theoretical Biology 95, 95–114.CrossRefGoogle Scholar
McClelland, E. E., Granger, D. L. and Potts, W. K. (2003). Major histocompatibility complex-dependent susceptibility to Cryptococcus neoformans in mice. Infection and Immunity 71, 4815–4817.CrossRefGoogle ScholarPubMed
Moro, M. H., Zegarra-Moro, O. L., Bjornsson, J., Hofmeister, E. K., Bruinsma, E., Germer, J. J. and Persing, D. H. (2002). Increased arthritis severity in mice coinfected with Borrelia burgdorferi and Babesia microti. Journal of Infectious Diseases 186, 428–431.CrossRefGoogle ScholarPubMed
Ohkawa, K., Hayashi, N., Yuki, N., Hagiwara, H., Kato, M., Yamamoto, K., Eguchi, H., Fusamoto, H., Masuzawa, M. and Kamada, T. (1994). Hepatitis-C virus-antibody and hepatitis-C virus-replication in chronic hepatitis-B patients. Journal of Hepatology 21, 509–514.CrossRefGoogle ScholarPubMed
Pearce, L. K., Radecki, S. V., Brewer, M. and Lappin, M. R. (2006). Prevalence of Bartonella henselae antibodies in serum of cats with and without clinical signs of central nervous system disease. Journal of Feline Medicine and Surgery 8, 315–320.CrossRefGoogle ScholarPubMed
Pedersen, A. B. and Fenton, A. (2007). Emphasizing the ecology in parasite community ecology. Trends in Ecology & Evolution 22, 133–139.CrossRefGoogle ScholarPubMed
Petney, T. N. and Andrews, R. H. (1998). Multiparasite communities in animals and humans: frequency, structure and pathogenic significance. International Journal for Parasitology 28, 377–393.CrossRefGoogle ScholarPubMed
Raimondo, G., Brunetto, M. R., Pontisso, P., Smedile, A., Maina, A. M., Saitta, C., Squadrito, G. and Tono, N. (2006). Longitudinal evaluation reveals a complex spectrum of virological profiles in hepatitis B virus hepatitis C virus-coinfected patients. Hepatology 43, 100–107.CrossRefGoogle ScholarPubMed
Read, A. F. and Taylor, L. H. (2001). The ecology of genetically diverse infections. Science 292, 1099–1102.CrossRefGoogle ScholarPubMed
Reid, H. W., Buxton, D., Pow, I., Brodie, T. A., Holmes, P. H. and Urquhart, G. M. (1986). Response of sheep to experimental concurrent infection with tick-borne fever (Cytoecetes phagocytophila) and Louping-Ill Virus. Research in Veterinary Science 41, 56–62.CrossRefGoogle ScholarPubMed
Resto-Ruiz, S., Burgess, A. and Anderson, B. E. (2003). The role of the host immune response in pathogenesis of Bartonella henselae. DNA and Cell Biology 22, 431–440.CrossRefGoogle ScholarPubMed
Sato, S., Fujiyama, S., Tanaka, M., Yamasaki, K., Kuramoto, I., Kawano, S., Sato, T., Mizuno, K. and Nonaka, S. (1994). Coinfection of hepatitis-C virus in patients with chronic hepatitis-B infection. Journal of Hepatology 21, 159–166.CrossRefGoogle ScholarPubMed
Signorini, L., Simeone, F., Tonegatti, L., Colombini, P., Cadeo, B., Cristini, F., Matteeli, A. and Viale, P. (2002). Co-infection with Epstein-Barr virus and Bartonella henselae resulting in systemic bartonellosis. Journal of Infection 45, 206–207.CrossRefGoogle ScholarPubMed
Smith, A., Telfer, S., Burthe, S., Bennett, M. and Begon, M. (2005). Trypanosomes, fleas and field voles: ecological dynamics of a host-vector-parasite interaction. Parasitology 131, 355–365.CrossRefGoogle ScholarPubMed
Swanson, S. J., Neitzel, D., Reed, K. D. and Belongia, E. A. (2006). Coinfections acquired from Ixodes ticks. Clinical Microbiology Reviews 19, 708–727.CrossRefGoogle ScholarPubMed
Telfer, S., Begon, M., Bennett, M., Bown, K. J., Burthe, S., Lambin, X., Telford, G. and Birtles, R. (2007 a). Contrasting dynamics of Bartonella spp. in cyclic field vole populations: the impact of vector and host dynamics. Parasitology 134, 413–425.CrossRefGoogle ScholarPubMed
Telfer, S., Bennett, M., Bown, K., Cavanagh, R., Crespin, L., Hazel, S., Jones, T. and Begon, M. (2002). The effects of cowpox virus on survival in natural rodent populations: increases and decreases. Journal of Animal Ecology 71, 558–568.CrossRefGoogle Scholar
Telfer, S., Clough, H., Birtles, R., Bennett, M., Carslake, D., Helyar, S. and Begon, M. (2007 b). Ecological differences and coexistence in a guild of microparasites: Bartonella in wild rodents. Ecology 88, 1841–1849.CrossRefGoogle Scholar
Thomas, M. B., Watson, E. L. and Valverde-Garcia, P. (2003). Mixed infections and insect-pathogen interactions. Ecology Letters 6, 183–188.CrossRefGoogle Scholar
Tompkins, D. M., Dobson, A. P., Arneberg, P., Begon, M. E., Cattadori, I. M., Greenman, J. V., Heesterbeek, J. A. P., Hudson, P. J., Newborn, D., Pugliese, A., Rizzoli, A. P., Rosa, R., Rosso, F. and Wilson, K. (2002). Parasites and host population dynamics. In The Ecology of Wildlife Diseases (ed. Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. and Dobson, A. P.), pp. 45–62. Oxford University Press, Oxford.CrossRefGoogle Scholar
van Soolingen, D., van der Zanden, A. G. M., de Haas, P. E. W., Noordhoek, G. T., Kiers, A., Foudraine, N. A., Portaels, F., Kolk, A. H. J., Kremer, K. and van Embden, J. D. A. (1998). Diagnosis of Mycobacterium microti infections among humans by using novel genetic markers. Journal of Clinical Microbiology 36, 1840–1845.CrossRefGoogle ScholarPubMed
Wang, T. J., Liang, M. H., Sangha, O., Phillips, C. B., Lew, R. A., Wright, E. A., Berardi, V., Fossel, A. H. and Shadick, N. A. (2000). Coexposure to Borrelia burgdorferi and Babesia microti does not worsen the long-term outcome of Lyme disease. Clinical Infectious Diseases 31, 1149–1154.CrossRefGoogle Scholar
Wells, A. Q. (1946). The murine type of tubercle bacillus (the vole acid-fast bacillus). Special Report Series in Medicine, Council of London 259, 1–48.Google Scholar
Whitworth, J., Morgen, D., Quigley, M., Smith, A., Mayanja, S., Eotu, H., Omoding, N., Okongo, M., Malamba, S. and Ojwiya, A. (2000). Effect of HIV-1 and increasing immunosuppression on malaria parasitaemia and clinical episodes in adults in rural Uganda: a cohort study. Lancet 356, 1051–1056.CrossRefGoogle ScholarPubMed
Wintrebert, C. M. A., Zwinderman, A. H., Cam, E., Pradel, R. and van Houwelingen, J. C. (2005). Joint modelling of breeding and survival in the kittiwake using frailty models. Ecological Modelling 181, 203–213.CrossRefGoogle Scholar
Yacob, H. T., Dorchies, P., Jacquiet, P., Bleuart, C., Prevot, F., Grisez, C., Bergeaud, J. P. and Hoste, H. (2004). Concurrent parasitic infections of sheep: depression of Trichostrongylus colubriformis populations by a subsequent infection with Oestrus ovis. Veterinary Parasitology 121, 297–306.CrossRefGoogle ScholarPubMed
Yacob, H. T., Duranton-Grisez, C., Prevot, F., Bergeaud, J. P., Bleuart, C., Jacquiet, P., Dorchies, P. and Hoste, H. (2002). Experimental concurrent infection of sheep with Oestrus ovis and Trichostrongylus colubriformis: negative interactions between parasite populations and related changes in the cellular responses of nasal and digestive mucosae. Veterinary Parasitology 104, 307–317.CrossRefGoogle ScholarPubMed
Yamamoto, K., Chomel, B. B., Kasten, R. W., Hew, C. M., Weber, D. K., Lee, W. I., Koehler, J. E. and Pedersen, N. C. (2003). Infection and re-infection of domestic cats with various Bartonella species or types: B-henselae type I is protective against heterologous challenge with B-henselae type II. Veterinary Microbiology 92, 73–86.CrossRefGoogle ScholarPubMed
Yirrell, D. L., Wright, E., Shafer, L. A., Campbell, E., Van der Paall, L., Kaleebu, P., Grosskurth, H. and Whitworth, J. A. (2007). Association between active GB virus-C (hepatitis G) infection and HIV-1 disease in Uganda. International Journal of STD & Aids 18, 244–249.CrossRefGoogle ScholarPubMed