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The epidemiological consequences of optimisation of the individual host immune response

Published online by Cambridge University Press:  29 May 2003

G. F. MEDLEY
Affiliation:
Ecology & Epidemiology Group, Department of Biological Sciences, University of Warwick, Coventry CV4 7AL

Abstract

We present a simple unscaled, quantitative framework that addresses the optimum use of resources throughout a host's lifetime based on continuous exposure to parasites (rather than evolutionary, genetically explicit trade-offs). The principal assumptions are that a host's investment of resources in growth increases its survival and reproduction, and that increasing parasite burden reduces survival. The host reproductive value is maximised for a given combination of rates of parasite exposure, host resource acquisition and pathogenicity, which results in an optimum parasite burden (for the host). Generally, results indicate that the optimum resource allocation is to tolerate some parasite infection. The lower the resource acquisition, the lower the proportion of resources that should be devoted to immunity, i.e. the higher the optimum parasite burden. Increases in pathogenicity result in reduced optimum parasite burdens, whereas increases in exposure result in increasing optimum parasite burdens. Simultaneous variation in resource acquisition, pathogenicity and exposure within a community of hosts results in overdispersed parasite burdens, with the degree of heterogeneity decreasing as mean burden increases. The relationships between host condition and parasite burden are complicated, and could potentially confound data analysis. Finally, the value of this approach for explaining epidemiological patterns, immunological processes and the possibilities for further work are discussed.

Type
Research Article
Copyright
© 2002 Cambridge University Press

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References

ANDERSON, R. M. & MEDLEY, G. F. (1985). Community control of helminth infections of man by mass and selective chemotherapy. Parasitology 90, 629660.CrossRefGoogle Scholar
ANISMAN, H., ZALCMAN, S. & ZACHARKO, R. M. (1993). The impact of stressors on immune and central neurotransmitter activity: bidirectional communication. Reviews in the Neurosciences 4, 147180.CrossRefGoogle Scholar
ANTONOVICS, J. & THRALL, P. H. (1994). The cost of resistance and the maintenance of genetic polymorphism in the host-pathogen systems. Proceedings of the Royal Society of London, Series B 257, 105110.CrossRefGoogle Scholar
BARNARD, C. J., BEHNKE, J. M., GAGE, A. R., BROWN, H. & SMITHURST, P. R. (1997). Immunity costs and behavioural modulation in male laboratory mice (Mus musculus) exposed to the odours of females. Physiology and Behavior 62, 857866.CrossRefGoogle Scholar
BEHNKE, J. M., BARNARD, C. J. & WAKELIN, D. (1992). Understanding chronic nematode infections: evolutionary considerations, current hypotheses and the way forward. International Journal for Parasitology 22, 861907.CrossRefGoogle Scholar
BOES, J., COATES, S., MEDLEY, G. F., VARADY, M., ERIKSEN, L., ROEPSTORFF, A. & NANSEN, P. (1999). The role of material immunity in experimental Ascaris suum infections in young piglets. Parasitology 119, 509520.CrossRefGoogle Scholar
BOES, J., MEDLEY, G. F., ERIKSEN, L., ROEPSTORFF, A. & NANSEN, P. (1998). Distribution of Ascaris suum in experimentally and naturally infected pigs and comparison with Ascaris lumbricoides infections in humans. Parasitology 117, 589596.CrossRefGoogle Scholar
BOOTS, M. & BEGON, M. (1993). Trade-offs with resistance to a granulosis virus in the Indian meal moth, examined by a laboratory evolution experiment. Functional Ecology 7, 528534.CrossRefGoogle Scholar
BOWERS, R. G., BOOTS, M. & 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.CrossRefGoogle Scholar
BUNDY, D. A. P. & MEDLEY, G. F. (1992). Immuno-epidemiology of human geohelminthiasis: ecological and immunological determinants of worm burden. Parasitology 104, S105S119.CrossRefGoogle Scholar
BUNDY, D. A. P., SHER, A. & MICHAEL, E. (2000). Good worms or bad worms: do worm infections affect the epidemiological patterns of other diseases? Parasitology Today 16, 273274.Google Scholar
CARLIER, Y. & TRUYENS, C. (1995). Influence of maternal infection on offspring resistance towards parasites. Parasitology Today 11, 9499.CrossRefGoogle Scholar
CHAN, L., BUNDY, D. A. P. & KAN, S. P. (1994a). Aggregation and predisposition to Ascaris lumbricoides and Trichuris trichiura at the familial level. Transactions of the Royal Society of Tropical Medicine and Hygiene 88, 4648.Google Scholar
CHAN, L., BUNDY, D. A. P. & KAN, S. P. (1994b). Genetic relatedness as a determinant of predisposition to Ascaris lumbricoides and Trichuris trichiura infection. Parasitology 108, 7780.Google Scholar
COOP, R. L. & KYRIAZAKIS, I. (1999). Nutrition-parasite interaction. Veterinary Parasitology 84, 187204.CrossRefGoogle Scholar
FELLOWES, M. D. E., KRAAIJEVELD, A. R. & GODFRAY, H. C. J. (1998). Trade-off associated with selection for increased ability to resist parasitoid attack in Drosophila melanogaster. Proceedings of the Royal Society of London, Series B 265, 15531558.CrossRefGoogle Scholar
GARSIDE, P., KENNEDY, M. W., WAKELIN, D. & LAWRENCE, C. E. (2000). Immunopathology of intestinal helminth infection. Parasite Immunology 22, 605612.CrossRefGoogle Scholar
GRAHAM, A. L. (2001). Use of an optimality model to solve the immunological puzzle of concomitant infection. Parasitology 122, S61S64.CrossRefGoogle Scholar
GUSTAFSSON, L., NORDLING, D., ANDERSSON, M. S., SHELDON, B. C. & QVARNSTROM, A. (1994). Infectious diseases, reproductive effort and the cost of reproduction in birds. Philosophical Transactions of the Royal Society of London, Series B 346, 323331.CrossRefGoogle Scholar
GUYATT, H. L., BUNDY, D. A. P., MEDLEY, G. F. & GRENFELL, B. T. (1990). The relationship between the frequency distribution of Ascaris lumbricoides and the prevalence and intensity of infection in human communities. Parasitology 101, 139143.CrossRefGoogle Scholar
GUYATT, H. L., SMITH, T., GRYSEELS, B., LENGELER, C., MSHINDA, H., SIZIYA, S., SALANAVE, B., MOHOME, N., MAKWALA, J., NGIMBI, K. P. & TANNER, M. (1994). Aggregation in schistosomiasis: comparison of the relationships between prevalence and intensity in different endemic areas. Parasitology 109, 4555.CrossRefGoogle Scholar
HUDSON, P. J. & DOBSON, A. P. (1995). Macroparasites: observed patterns in naturally fluctuating animal populations. In Ecology of Infectious Diseases in Natural Populations (ed. Grenfell, B. T. & Dobson, A. P.). Cambridge, Cambridge University Press.CrossRef
HURD, H. (2001). Host fecundity reduction: a strategy for damage limitation? Trends in Parasitology 17, 363368.Google Scholar
JANKOVIC, D., LIU, Z. & GAUSE, W. C. (2001). Th1- and Th2-cell commitment during infectious disease: asymmetry in divergent pathways. Trends in Immunology 22, 450457.CrossRefGoogle Scholar
KAITALA, V., HEINO, M. & GETZ, W. M. (1997). Host-parasite dynamics and the evolution of host immunity and parasite fecundity strategies. Bulletin of Mathematical Biology 59, 427450.CrossRefGoogle Scholar
keymer, a. e. & pagel, m. (1990). Predisposition to hookworm infection. In Hookworm Infection: Current Status and New Directions (ed. Schad, G. A. & Warren, K. S.). London, Taylor and Francis.
KEYMER, A. E. & PAGEL, M. (1990). Predisposition to hookworm infection. In Hookworm Infection: Current Status and New Directions (ed. Schad, G. A. & Warren, K. S.). London, Taylor and Francis.
LOCHMILLER, R. L. & DEERENBERG, C. (2000). Trade-offs in evolutionary immunology: just what are the costs of immunity? Oikos 88, 8798.Google Scholar
LWAMBO, N. J. S., BUNDY, D. A. P. & MEDLEY, G. F. H. (1992). A new approach to morbidity risk assessment in hookworm endemic communities. Epidemiology and Infection 108, 469481.CrossRefGoogle Scholar
MATARESE, G., LA CAVA, A., SANNA, V., LORD, G. M., LECHLER, R. I., FONTANA, S. & ZAPPACOSTA, S. (2002). Balancing susceptibility to infection and autoimmunity: a role for leptin? Trends in Immunology 23, 182187.Google Scholar
MEDLEY, G. F. & BUNDY, D. A. P. (1996). Dynamic modelling of epidemiological patterns of schistosomiasis morbidity. American Journal of Tropical Medicine and Hygiene 55, 149158.CrossRefGoogle Scholar
MEDLEY, G. F., SINDEN, R. E., FLECK, S., BILLINGSLEY, P. F., TIRAWANCHAI, N. & RODRIGUEZ, M. H. (1993). Heterogeneity in patterns of malarial oocyst infections in the mosquito vector. Parasitology 106, 441449.CrossRefGoogle Scholar
METCALFE, N. B. & MONAHAN, P. (2001). Compensation of a bad start: grow now, pay later? Trends in Ecology and Evolution 16, 254260.Google Scholar
MICHAEL, E. & BUNDY, D. A. P. (1992a). Nutrition, immunity and helminth infection: effects of dietary protein in the dynamics of the primary antibody response to Trichuris muris (Nematoda) in CBA/Ca mice. Parasite Immunology 14, 169183.Google Scholar
MICHAEL, E. & BUNDY, D. A. P. (1992b). Protein content of CBA/Ca mouse diet: relationship with host antibody responses and the population dynamics of Trichuris muris (Nematoda) in repeated infection. Parasitology 105, 139150.Google Scholar
MORET, Y. & SCHMID-HEMPEL, P. (2000). Survival for immunity: the price of immune system activation for bumblebee workers. Science 290, 11661168.CrossRefGoogle Scholar
NELSON, R. J. & DEMAS, G. E. (1996). Seasonal changes in immune function. The Quarterly Review of Biology 71, 511548.CrossRefGoogle Scholar
PACALA, S. W. & DOBSON, A. P. (1988). The relation between the number of parasites/host and host age: population dynamic causes and maximum likelihood estimation. Parasitology 96, 197210.CrossRefGoogle Scholar
PARKER, G. A. & MAYNARD SMITH, J. (1990). Optimality theory in evolutionary biology. Nature 348, 2733.CrossRefGoogle Scholar
PETKEVICIUS, S., BJORN, H., ROEPSTORFF, A., NANSEN, P., BACH KNUDSEN, K. E., BARNES, E. H. & JENSEN, K. (1995). The effect of two types of diet on populations of Ascaris suum and Oesophagostomum dentatum in experimentally infected pigs. Parasitology 111, 395402.CrossRefGoogle Scholar
QUINNELL, R. J., MEDLEY, G. F. & KEYMER, A. E. (1990). The regulation of gastro-intestinal helminth populations. Proceedings of the Royal Society of London, Series B 330, 191201.CrossRefGoogle Scholar
READ, A. F. & ALLEN, E. A. (2000). The economics of immunity. Science 290, 11041105.CrossRefGoogle Scholar
ROEPSTORFF, A., ERIKSEN, L., SLOTVED, H. C. & NANSEN, P. (1997). Experimental Ascaris suum infection in the pig: worm population kinetics following single inoculations with three doses of infective eggs. Parasitology 115, 443452.CrossRefGoogle Scholar
SHELDON, B. C. & VERHULST, S. (1996). Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology and Evolution 11, 317321.CrossRefGoogle Scholar
VAN BAALEN, M. (1998). Coevolution of recovery ability and virulence. Proceedings of the Royal Society of London, Series B 265, 317325.CrossRefGoogle Scholar
WILLIAMS-BLANGERO, S., SUBEDI, J., UPADHAYAY, R. P., MANRAL, D. B., RAI, D. R., JHA, B., ROBINSON, E. S. & BLANGERO, J. (1999). Genetic analysis of susceptibility to infection with Ascaris lumbricoides. American Journal of Tropical Medicine & Hygiene 60, 921926.CrossRefGoogle Scholar
WOOLHOUSE, M. E. J. (1992). A theoretical framework for the immunoepidemiology of helminth infection. Parasite Immunology 14, 563578.CrossRefGoogle Scholar
YAZDANBAKHSH, M., VAN DEN BIGGELAAR, A. & MAIZELS, R. M. (2001). Th2 responses without atopy: immunoregulation in chronic helminth infections and reduced allergic disease. Trends in Immunology 22, 372377.CrossRefGoogle Scholar