Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-26T05:09:22.714Z Has data issue: false hasContentIssue false
  • English
  • Français

Changes in parasite aggregation with age: a discrete infection model

Published online by Cambridge University Press:  06 April 2009

R. J. Quinnell ,
A. Grafen  and
M. E. J. Woolhouse
R. J. Quinnell
Affiliation:
Department of Medical Parasitology, London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT
A. Grafen
Affiliation:
Department of Plant Sciences, University of Oxford, South Parks Road, Oxford OX1 3PS
M. E. J. Woolhouse
Affiliation:
Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS
Get access Rights & Permissions [Opens in a new window]

Summary

We present a discrete time model for age-related changes in the mean and variance of the number of helminth parasites per host. We assess the degree of aggregation as the negative binomial parameter, k, and use the model to examine the influence of various factors on changes in aggregation with host age: discrete versus continuous infection; the degree of predisposition to infection; infection rate; parasite survival rate; and the variance in exposure to infective stages. The model can produce both increases and decreases in k with host age. However, with parameter values typical of many human helminth infections, a monotonic increase in k (decrease in aggregation) with age is predicted. With an age-dependent infection rate, convex relationships between k and age are possible. These predictions are consistent with data from field studies, but differ from those of previous models which have suggested that k is independent of host age in the absence of density dependence in parasite population dynamics. Differences between the models, and some difficulties in the interpretation of field data, are discussed.

Keywords

aggregationdensity-dependencehelminthmathematical modelsnegative binomial
Type
Research Article
Information
Parasitology , Volume 111 , Issue 5 , December 1995 , pp. 635 - 644
Copyright
Copyright © Cambridge University Press 1995

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

Anderson, R. M. (1974). Mathematical models of host-helminth parasite interactions. In Ecological Stability (ed. Usher, M. B. & Williamson, M. H.), pp. 43–69. London: Chapman and Hall.CrossRefGoogle Scholar
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. (1985). Mathematical models in the study of the epidemiology and control of ascariasis in man. In Ascariasis and its Public Health Importance (ed. Crompton, D. W. T., Nesheim, M. C. & Pawlowski, Z. S.), pp. 39–67. London: Taylor & Francis.Google Scholar
Anderson, R. M. & Gordon, D. M. (1982). Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortalities. Parasitology 85, 373–98.CrossRefGoogle ScholarPubMed
Anderson, R. M. & May, R. M. (1985 a). Helminth infections of humans: mathematical models population dynamics and control. Advances in Parasitology 24, 1–101.CrossRefGoogle ScholarPubMed
Anderson, R. M. & May, R. M. (1985 b). Herd immunity to helminth infection and implications for parasite control. Nature, London 315, 493–6.CrossRefGoogle ScholarPubMed
Anderson, R. M. & May, R. M. (1991). Infectious Diseases of Humans: Dynamics and Control. Oxford: Oxford University Press.CrossRefGoogle Scholar
Bradley, D. J. & McCullough, F. S. (1973). Egg Output stability and the epidemiology of Schistosoma haematobium. Part II. An analysis of the epidemiology of S. haematobium. Transactions of the Royal Society of Tropical Medicine and Hygiene 67, 491–500.CrossRefGoogle ScholarPubMed
Brattey, J. & I-Hsun, ni (1992). Ascaridoid nematodes from the stomach of harp seals, Phoca groenlandica, from Newfoundland and Labrador. Canadian Journal of Fisheries and Aquatic Science 49, 956–66.CrossRefGoogle Scholar
Bundy, D. A. P., Cooper, E. S., Thompson, D. E., Anderson, R. M. & Didier, J. M. (1987). Age-related prevalences and intensity of Trichuris trichiura infection in a St. Lucian community. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 85–94.CrossRefGoogle Scholar
Bundy, D. A. P., Kan, S. P. & Rose, R. (1988). Age-related prevalence, intensity and frequency distribution of gastrointestinal helminth infection in urban slum children from Kuala Lumpur Malaysia. Transactions of the Royal Society of Tropical Medicine and Hygiene 82, 289–94.CrossRefGoogle ScholarPubMed
Chandiwana, S. K. (1987). Analysis of the Dynamics of Transmission of Human Schistosomiasis in Two Rural Communities in Zimbabwe. Ph.D. thesis, University of Zimbabwe.Google Scholar
Chandiwana, S. K. (1990). Hookworm population ecology in Zimbabwe. In Hookworm Disease: Current Status and New Directions (ed. Schad, G. A. & Warren, K. S.), pp. 165–176. London: Taylor & Francis.Google Scholar
Chandiwana, S. K., Christensen, N. O. & Frandsen, F. (1987). Seasonal patterns in the transmission of Schistosoma haematobium, S. mattheei and S. mansoni in the highveld region of Zimbabwe. Acta Tropica 44, 433–44.Google ScholarPubMed
Chandiwana, S. K. & Woolhouse, M. E. J. (1991). Heterogeneities in water contact patterns and the epidemiology of Schistosoma haematobium. Parasitology 103, 363–70.CrossRefGoogle ScholarPubMed
Croll, N. A., Anderson, R. M., Gyarkos, T. W. & Ghadirian, E. (1982). The population biology and control of Ascaris lumbricoides in a rural community in Iran. Transactions of the Royal Society of Tropical Medicine and Hygiene 76, 187–97.CrossRefGoogle Scholar
de Vlas, S. J., Gryseels, B., Van Oortmarssen, G. J., Polderman, A. M. & Habbema, J. D. F. (1992). A model for variations in single and repeated egg counts in Schistosoma mansoni infections. Parasitology 104, 451–60.CrossRefGoogle Scholar
Dietz, K. (1988). Mathematical models. In Malaria, Vol. 2 (ed. Wernsdorfer, W. H. & McGregor, I.), pp. 1091–134 Edinburgh: Churchill-Livingstone.Google Scholar
Dobson, A. P., Pacala, S. V., Roughgarden, J. D., Carper, E. R. & Harris, E. A. (1992). The parasites of anolis lizards in the northern Lesser Antilles. 1. Patterns of distribution and abundance. Oecologia 91, 110–17.CrossRefGoogle ScholarPubMed
Elkins, D. B., Haswell-Elkins, M. R. & Anderson, R. M. (1988). The importance of host age and sex to patterns of reinfection with Ascaris lumbricoides following mass anthelminthic treatment in a South Indian fishing community. Parasitology 96, 171–84.CrossRefGoogle Scholar
Fulford, A. J. C., Butterworth, A. E., Sturrock, R. F. & Ouma, J. H. (1992). On the use of age-intensity data to detect immunity to parasitic infections with special reference to Schistosoma mansoni in Kenya. Parasitology 105, 219–28.CrossRefGoogle ScholarPubMed
Grafen, A. & Woolhouse, M. E. J. (1993). Does the negative binomial distribution add up ? Parasitology Today 9, 475–7.CrossRefGoogle ScholarPubMed
Gregory, R. D. (1992). On the interpretation of host-parasite ecology: Heligmosomoides polygyrus (Nematoda) in wild wood mouse (Apodemus sylvaticus) populations. Journal of Zoology 226, 109–21.CrossRefGoogle Scholar
Gregory, R. D. & Woolhouse, M. E. J. (1993). Quantification of parasite aggregation: a simulation study. Acta Tropica 54, 131–9.CrossRefGoogle ScholarPubMed
Grenfell, B. T., Dietz, K. & Roberts, M. G. (1995). Modelling the immuno-epidemiology of macroparasites in naturally-fluctuating host populations. In Ecology of Infectious Diseases in Natural Populations (ed. Grenfell, B. T. & Dobson, A. P.), pp. 362–383. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Hadeler, K. P. & Dietz, K. (1983). Nonlinear hyperbolic partial differential equations for the dynamics of parasite populations. Computers and Mathematics with Applications 9, 415–30.CrossRefGoogle Scholar
Haswell-Elkins, M. R., Elkins, D. B., Manjula, K., Michael, E. & Anderson, R. M. (1988). An investigation of hookworm infection and reinfection following mass anthelminthic treatment in the South Indian fishing community of Vairavankuppam. Parasitology 96, 565–77.CrossRefGoogle ScholarPubMed
Hominick, W. M., Dean, C. G. & Schad, G. A. (1987). Population biology of hookworms in West Bengal: analysis of infective larvae recovered from damp pads applied to the soil surface at defaecation sites. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 978–86.CrossRefGoogle Scholar
Keymer, A. E. & Pagel, M. (1990). Predisposition to helminth infection. In Hookworm Disease: Current Status and New Directions (ed. Schad, G. A. & Warren, K. S.), pp. 177–209. London: Taylor & Francis.Google 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, 197–210.CrossRefGoogle ScholarPubMed
Quinnell, R. J. (1992). The population dynamics of Heligmosomoides polygyrus in an enclosure population of wood mice. Journal of Animal Ecology 61, 669–79.CrossRefGoogle Scholar
Quinnell, R. J., Slater, A. F. G., Tighe, P., Walsh, E. A., Keymer, A. E. & Pritchard, D. I. (1993). Reinfection with hookworm after chemotherapy in Papua New Guinea. Parasitology 106, 379–85.CrossRefGoogle ScholarPubMed
Srividya, A., Krishnamoorthy, K., Sabesan, S., Panicker, A. N., Grenfell, B. T. & Bundy, D. A. P. (1991). Frequency distribution of Brugia malayi microfilariae in human populations. Parasitology 102, 207–12.CrossRefGoogle ScholarPubMed
Sweet, W. C. (1925). Average egg count per gm faeces per female hookworm in Ceylon. Journal of Parasitology 12, 39–42.CrossRefGoogle Scholar
Taylor, L. R., Woiwod, I. P. & Perry, J. N. (1979). The negative binomial as a dynamic ecological model for aggregation and the density dependence of k. Journal of Animal Ecology 48, 289–304.CrossRefGoogle Scholar
Tinsley, R. C. & Jackson, H. C. (1988). Pulsed transmission of Pseudodiplorchis americanus (Monogenea) between desert hosts (Scaphiopus couchii). Parasitology 97, 437–53.CrossRefGoogle Scholar
Udonsi, J. K. (1990). Human community ecology of urinary schistosomiasis in relation to snail vector bionomics in the Igwun river basin of Nigeria. Tropical Medicine and Parasitology 41, 131–5.Google ScholarPubMed
Warren, K. S., Mahmoud, A. A. F., Cummings, P., Murphy, D. J. & Houser, D. B. (1974). Schistosomiasis mansoni in Yemeni in California: duration of infection, presence of disease and therapeutic management. American Journal of Tropical Medicine and Hygiene 23, 902–9.CrossRefGoogle ScholarPubMed
Wilkins, H. A., Goll, P. H., Marshall, T. F. de C. & Moore, P. J. (1984). Dynamics of Schistosoma haematobium infection in a Gambian community. III. The acquisition and loss of infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 78, 227–32.CrossRefGoogle Scholar
Wong, M. S., Bundy, D. A. P. & Golden, M. H. N. (1988). Quantitative assessment of geographic behaviour as a potential source of exposure to geohelminth infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 82, 621–5.CrossRefGoogle Scholar
Woolhouse, M. E. J. (1992). A theoretical framework for the immunoepidemiology of human helminth infection. Parasite Immunology 14, 563–78.CrossRefGoogle Scholar
Woolhouse, M. E. J. & Chandiwana, S. K. (1989). Spatial and temporal heterogeneity in the population dynamics of Bulinus globosus and Biomphalaria pfeifferi and in the epidemiology of their infection with schistosomes. Parasitology 98, 21–34.CrossRefGoogle ScholarPubMed
Woolhouse, M. E. J., Ndamba, J. & Bradley, D. J. (1994). On the interpretation of intensity of infection data for Schistosoma haematobium. Transactions of the Royal Society of Tropical Medicine and Hygiene 88, 520–6.CrossRefGoogle ScholarPubMed