Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-28T05:43:34.822Z Has data issue: false hasContentIssue false
  • English
  • Français

Worms and germs: the population dynamic consequences of microparasite-macroparasite co-infection

Published online by Cambridge University Press:  10 December 2007

ANDY FENTON
ANDY FENTON*
Affiliation:
School of Biological Sciences, University of Liverpool, Crown Street, Liverpool, L69 7ZB, UK
*
Tel: 0151 795 4473, Fax: 0151 795 4408, Email: a.fenton@liverpool.ac.uk
Get access Rights & Permissions [Opens in a new window]

Summary

Hosts are typically simultaneously co-infected by a variety of microparasites (e.g. viruses and bacteria) and macroparasites (e.g. parasitic helminths). However, the population dynamical consequences of such co-infections and the implications for the effectiveness of imposed control programmes have yet to be fully realised. Mathematical models may provide an important framework for exploring such issues and have proved invaluable in helping to understand the factors affecting the epidemiology of single parasitic infections. Here the first population dynamic model of microparasite-macroparasite co-infection is presented and used to explore how co-infection alters the predictions of the existing single-species models. It is shown that incorporating an additional parasite species into existing models can greatly stabilise them, due to the combined density-dependent impacts on the host population, but co-infection can also restrict the region of parameter space where each species could persist alone. Overall it is concluded that the dynamic feedback between host, microparasite and macroparasite means that it is difficult to appreciate the factors affecting parasite persistence and predict the effectiveness of control by just studying one component in isolation.

Keywords

Basic reproduction ratiodisease controlepidemiologyhost-parasite communitymathematical modelparasitic helminthpopulation dynamicsvirus
Type
Research Article
Information
Parasitology , Volume 135 , Special Issue 13: Mathematical modelling of parasitic infections: from data and parameter estimation to evolutionary implications , November 2008 , pp. 1545 - 1560
Copyright
Copyright © 2007 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

Altizer, S., Dobson, A., Hosseini, P., Hudson, P., Pascual, M. and Rohani, P. (2006). Seasonality and the dynamics of infectious diseases. Ecology Letters 9, 467–484.CrossRefGoogle ScholarPubMed
Anderson, R. M. (1980). The dynamics and control of direct life cycle helminth parasites. Lecture Notes in Biomathematics 39, 278–322.CrossRefGoogle Scholar
Anderson, R. M. and May, R. M. (1978). Regulation and stability of host-parasite population interactions. I. Regulatory processes. Journal of Animal Ecology 47, 219–247.CrossRefGoogle Scholar
Anderson, R. M. and May, R. M. (1979). Population biology of infectious diseases: Part I. Nature 280, 361–367.CrossRefGoogle ScholarPubMed
Anderson, R. M. and May, R. M. (1981). The population dynamics of microparasites and their invertebrate hosts. Philosophical Transactions of the Royal Society of London, Series B 291, 451–524.Google Scholar
Anderson, R. M. and May, R. M. (1992). Infectious Diseases of Humans: Dynamics and Control, Oxford University Press, Oxford.Google Scholar
Begon, M., Bowers, R. G., Kadiankis, N. and Hodgkinson, D. E. (1992). Disease and community structure: the importance of host self-regulation in a host-host-pathogen model. The American Naturalist 139, 1131–1150.CrossRefGoogle Scholar
Begon, M., Harper, J. L. and Townsend, C. R. (1996). Ecology: Individuals, Populations and Communities, 3rd edn. Blackwell Scientific Publications, Oxford, UK.CrossRefGoogle Scholar
Behnke, J. M., Ali, N. M. H. and Jenkins, S. N. (1984). Survival to patency of low-level infections with Trichuris muris in mice concurrently infected with Nematospiroides dubius. Annals of Tropical Medicine and Parasitology 78, 509–517.CrossRefGoogle ScholarPubMed
Bentwich, Z., Kalinkovich, A. and Weisman, Z. (1995). Immune activation is a dominant factor in the pathogenesis of African AIDS. Immunology Today 16, 187–191.CrossRefGoogle ScholarPubMed
Boots, M. and Bowers, R. G. (1999). Three mechanisms of host resistance to microparasites – avoidance, recovery and tolerance – show different evolutionary dynamics. Journal of Theoretical Biology 201, 13–23.CrossRefGoogle ScholarPubMed
Bottomley, C., Isham, V. and Basanez, M. G. (2005). Population biology of multispecies helminth infection: interspecific interactions and parasite distribution. Parasitology 131, 417–433.CrossRefGoogle ScholarPubMed
Bottomley, C., Isham, V. and Basanez, M. G. (2007). Population biology of multispecies helminth infection: competition and coexistence. Journal of Theoretical Biology 244, 81–95.CrossRefGoogle ScholarPubMed
Bowers, R. G., Boots, M. and Begon, M. (1994). Life-history trade-offs and the evolution of pathogen resistance: competition between host strains. Proceedings of the Royal Society of London, Series B 257, 247–253.Google ScholarPubMed
Bowers, R. G., Hoyle, A., White, A. and Boots, M. (2005). The geometric theory of adaptive evolution: trade-off and invasion plots. Journal of Theoretical Biology 233, 363–377.CrossRefGoogle ScholarPubMed
Correa-Oliveira, R., Golgher, D. B., Oliveira, G. C., Carvalho, O. S., Massara, C. L., Caldas, I. R., Colley, D. G. and Gazzinelli, G. (2002). Infection with Schistosoma mansoni correlates with altered immune responses to Ascaris lumbricoides and hookworm. Acta Tropica 83, 123–132.CrossRefGoogle ScholarPubMed
Cox, F. E. G. (2001). Concomitant infections, parasites and immune responses. Parasitology (Suppl.) 122, S23–S38.CrossRefGoogle ScholarPubMed
Diekmann, O. and Heesterbeek, J. A. P. (2000). Mathematical Epidemiology of Infectious Diseases: Model Building, Analysis and Interpretation, John Wiley & Sons Ltd., Chichester.Google Scholar
Dobson, A. (2004). Population dynamics of pathogens with multiple host species. American Naturalist 164, S64–S78.CrossRefGoogle ScholarPubMed
Dobson, A. P. (1985). The population-dynamics of competition between parasites. Parasitology 91, 317–347.CrossRefGoogle ScholarPubMed
Druilhe, P., Tall, A. and Sokhna, C. (2005). Worms can worsen malaria: towards a new means to roll back malaria? Trends in Parasitology 21, 359–362.CrossRefGoogle ScholarPubMed
Elliott, J. M. (1977). Some Methods for theStatistical Analysis of Samples of Benthic Invertebrates, 2nd Edition, Titus Wilson & Son Ltd., Cumbria.Google Scholar
Fleming, F. M., Brooker, S., Geiger, S. M., Caldas, I. R., Correa-Oliveira, R., Hotez, P. J. and Bethony, J. M. (2006). Synergistic associations between hookworm and other helminth species in a rural community in Brazil. Tropical Medicine and International Health 11, 56–64.CrossRefGoogle Scholar
Gatto, M. and De Leo, G. A. (1998). Interspecific competition among macroparasites in a density-dependent host population. Journal of Mathematical Biology 37, 467–490.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 ScholarPubMed
Kelly-Hope, L. A., Diggle, P. J., Rowlingson, B. S., Gyapong, J. O., Kyelem, D., Coleman, M., Thomson, M. C., Obsomer, V., Lindsay, S. W., Hemingway, J. and Molyneux, D. H. (2006). Negative spatial association between lymphatic filariasis and malaria in West Africa. Tropical Medicine and International Health 11, 129–135.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
Maggi, E., Mazzetti, M., Ravina, A., Annunziato, F., Decarli, M., Piccinni, M. P., Manetti, R., Carbonari, M., Pesce, A. M., Delprete, G. and Romagnani, S. (1994). Ability of HIV to promote a Th1 to Th0 shift and to replicate preferentially in Th2 and Th0 cells. Science 265, 244–248.CrossRefGoogle ScholarPubMed
May, R. M. (1974). Stability and Complexity in Model Ecosystems, Princeton University Press.Google Scholar
May, R. M. and Anderson, R. M. (1978). Regulation and stability of host-parasite population interactions. II. Destabilizing processes. Journal of Animal Ecology 47, 249–267.CrossRefGoogle Scholar
May, R. M. and Anderson, R. M. (1979). Population biology of infectious diseases: Part II. Nature 280, 455–461.CrossRefGoogle ScholarPubMed
Mosmann, T. R. and Sad, S. (1996). The expanding universe of T-cell subsets: Th1, Th2 and more. Immunology Today 17, 138–146.CrossRefGoogle ScholarPubMed
Pedersen, A. B. and Fenton, A. (2007). Emphasising the ecology in parasite community ecology. Trends in Ecology and Evolution 22, 133–139.CrossRefGoogle Scholar
Perkins, S. E. and Fenton, A. (2006). Helminths as vectors of pathogens in vertebrate hosts: A theoretical approach. International Journal for Parasitology 36, 887–894.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
Poulin, R. and Valtonen, E. T. (2002). The predictability of helminth community structure in space: a comparison of fish populations from adjacent lakes. International Journal for Parasitology 32, 1235–1243.CrossRefGoogle ScholarPubMed
Pritchard, D. I., Hewitt, C. and Moqbel, R. (1997). Relationship between immunological responsiveness controlled by T-helper 2 lymphocytes and infections with parasitic helminths. Parasitology 115, S33–S44.CrossRefGoogle ScholarPubMed
Pugliese, A. (2000). Coexistence of macroparasites without direct interactions. Theoretical Population Biology 57, 145–165.CrossRefGoogle ScholarPubMed
Pugliese, A. (2002). On the evolutionary coexistence of parasite strains. Mathematical Biosciences 177, 355–375.CrossRefGoogle ScholarPubMed
Roberts, M. G. (1999). The immunoepidemiology of nematode parasites of farmed animals: a mathematical approach. Parasitology Today 15, 246–251.CrossRefGoogle ScholarPubMed
Roberts, M. G. and Dobson, A. P. (1995). The population dynamics of communities of parasitic helminths. Mathematical Biosciences 126, 191–214.CrossRefGoogle ScholarPubMed
Rohani, P., Green, C. J., Mantilla-Beniers, N. B. and Grenfell, B. T. (2003). Ecological interference between fatal diseases. Nature 422, 885–888.CrossRefGoogle ScholarPubMed
Romagnani, S. (1996). TH1 and TH2 in Human Diseases. Chemical Immunology 80, 225–235.Google ScholarPubMed
Spiegel, A., Tall, A., Raphenon, G., Trape, J. F. and Druilhe, P. (2003). Increased frequency of malaria attacks in subjects co-infected by intestinal worms and Plasmodium falciparum malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene 97, 198–199.CrossRefGoogle ScholarPubMed
Stewart, G. R., Boussinesq, M., Coulson, T., Elson, L., Nutman, T. and Bradley, J. E. (1999). Onchocerciasis modulates the immune response to mycobacterial antigens. Clinical and Experimental Immunology 117, 517–523.CrossRefGoogle ScholarPubMed
Woolhouse, M. E. J. (1992). A theoretical framework for the immunoepidemiology of helminth infection. Parasite Immunology 14, 563–578.CrossRefGoogle ScholarPubMed