Skip to main content

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

  • ANDY FENTON (a1)

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.

Corresponding author
Tel: 0151 795 4473, Fax: 0151 795 4408, Email:
Hide All
Altizer, S., Dobson, A., Hosseini, P., Hudson, P., Pascual, M. and Rohani, P. (2006). Seasonality and the dynamics of infectious diseases. Ecology Letters 9, 467484.
Anderson, R. M. (1980). The dynamics and control of direct life cycle helminth parasites. Lecture Notes in Biomathematics 39, 278322.
Anderson, R. M. and May, R. M. (1978). Regulation and stability of host-parasite population interactions. I. Regulatory processes. Journal of Animal Ecology 47, 219247.
Anderson, R. M. and May, R. M. (1979). Population biology of infectious diseases: Part I. Nature 280, 361367.
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, 451524.
Anderson, R. M. and May, R. M. (1992). Infectious Diseases of Humans: Dynamics and Control, Oxford University Press, Oxford.
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, 11311150.
Begon, M., Harper, J. L. and Townsend, C. R. (1996). Ecology: Individuals, Populations and Communities, 3rd edn. Blackwell Scientific Publications, Oxford, UK.
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, 509517.
Bentwich, Z., Kalinkovich, A. and Weisman, Z. (1995). Immune activation is a dominant factor in the pathogenesis of African AIDS. Immunology Today 16, 187191.
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, 1323.
Bottomley, C., Isham, V. and Basanez, M. G. (2005). Population biology of multispecies helminth infection: interspecific interactions and parasite distribution. Parasitology 131, 417433.
Bottomley, C., Isham, V. and Basanez, M. G. (2007). Population biology of multispecies helminth infection: competition and coexistence. Journal of Theoretical Biology 244, 8195.
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, 247253.
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, 363377.
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, 123132.
Cox, F. E. G. (2001). Concomitant infections, parasites and immune responses. Parasitology (Suppl.) 122, S23S38.
Diekmann, O. and Heesterbeek, J. A. P. (2000). Mathematical Epidemiology of Infectious Diseases: Model Building, Analysis and Interpretation, John Wiley & Sons Ltd., Chichester.
Dobson, A. (2004). Population dynamics of pathogens with multiple host species. American Naturalist 164, S64S78.
Dobson, A. P. (1985). The population-dynamics of competition between parasites. Parasitology 91, 317347.
Druilhe, P., Tall, A. and Sokhna, C. (2005). Worms can worsen malaria: towards a new means to roll back malaria? Trends in Parasitology 21, 359362.
Elliott, J. M. (1977). Some Methods for theStatistical Analysis of Samples of Benthic Invertebrates, 2nd Edition, Titus Wilson & Son Ltd., Cumbria.
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, 5664.
Gatto, M. and De Leo, G. A. (1998). Interspecific competition among macroparasites in a density-dependent host population. Journal of Mathematical Biology 37, 467490.
Gog, J. R. and Grenfell, B. T. (2002). Dynamics and selection of many-strain pathogens. Proceedings of the National Academy of Sciences. USA 99, 1720917214.
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, 129135.
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, 840844.
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, 244248.
May, R. M. (1974). Stability and Complexity in Model Ecosystems, Princeton University Press.
May, R. M. and Anderson, R. M. (1978). Regulation and stability of host-parasite population interactions. II. Destabilizing processes. Journal of Animal Ecology 47, 249267.
May, R. M. and Anderson, R. M. (1979). Population biology of infectious diseases: Part II. Nature 280, 455461.
Mosmann, T. R. and Sad, S. (1996). The expanding universe of T-cell subsets: Th1, Th2 and more. Immunology Today 17, 138146.
Pedersen, A. B. and Fenton, A. (2007). Emphasising the ecology in parasite community ecology. Trends in Ecology and Evolution 22, 133139.
Perkins, S. E. and Fenton, A. (2006). Helminths as vectors of pathogens in vertebrate hosts: A theoretical approach. International Journal for Parasitology 36, 887894.
Petney, T. N. and Andrews, R. H. (1998). Multiparasite communities in animals and humans: frequency, structure and pathogenic significance. International Journal for Parasitology 28, 377393.
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, 12351243.
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, S33S44.
Pugliese, A. (2000). Coexistence of macroparasites without direct interactions. Theoretical Population Biology 57, 145165.
Pugliese, A. (2002). On the evolutionary coexistence of parasite strains. Mathematical Biosciences 177, 355375.
Roberts, M. G. (1999). The immunoepidemiology of nematode parasites of farmed animals: a mathematical approach. Parasitology Today 15, 246251.
Roberts, M. G. and Dobson, A. P. (1995). The population dynamics of communities of parasitic helminths. Mathematical Biosciences 126, 191214.
Rohani, P., Green, C. J., Mantilla-Beniers, N. B. and Grenfell, B. T. (2003). Ecological interference between fatal diseases. Nature 422, 885888.
Romagnani, S. (1996). TH1 and TH2 in Human Diseases. Chemical Immunology 80, 225235.
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, 198199.
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, 517523.
Woolhouse, M. E. J. (1992). A theoretical framework for the immunoepidemiology of helminth infection. Parasite Immunology 14, 563578.
Recommend this journal

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

  • 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? *



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