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Prevalence of schistosome infections within molluscan populations: observed patterns and theoretical predictions

Published online by Cambridge University Press:  06 April 2009

R. M. Anderson  and
R. M. May
R. M. Anderson
Affiliation:
Zoology Department, Imperial College, London University, Prince Consort Road, London SW7
R. M. May
Affiliation:
Biology Department, Princeton University, Princeton, NJ 08540
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Summary

The paper draws together a large and scattered body of empirical evidence concerning the prevalence of snail infection with schistosome parasites in field situations, the duration of the latent period of infection in snails (and its dependence on temperature), and the mortality rates of infected and uninfected snails in field and laboratory conditions. A review and synthesis of quantitative data on the population biology of schistosome infections within the molluscan host is attempted and observed patterns of infection are compared with predictions of a schistosomiasis model developed by May (1977) which incorporates differential snail mortality (between infected and uninfected snails) and latent periods of infection. It is suggested that the low levels of prevalence within snail populations in endemic areas of schistosomiasis are closely associated with high rates of infected snail mortality and the duration of the latent period of infection within the mollusc. In certain instances, the expected life-span of an infected snail may be less than the duration of the latent period of infection. Such patterns generate very low levels of parasite prevalence. A new age prevalence model for schistosome infections within snail populations is developed and its predictions compared with observed patterns.

The implications of this study of observed and predicted patterns of snail infection within molluscan populations are discussed in relation to the overall transmission dynamics of schistosomiasis.

Type
Research Article
Information
Parasitology , Volume 79 , Issue 1 , August 1979 , pp. 63 - 94
Copyright
Copyright © Cambridge University Press 1979

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References

REFERENCES

Anderson, R. M. (1974). Population dynamics of the cestode Caryophyllaeus laticeps (Pallas, 1781) in the bream (Abramis brama L.). Journal of Animal Ecology 43, 305–21.Google Scholar
Anderson, R. M. (1978 a). The regulation of host population growth by parasitic species. Parasitology 76, 119–58.Google Scholar
Anderson, R. M. (1978 b). Population dynamics of snail infection by miracidia. Parasitology 77, 201–24.Google Scholar
Anderson, R. M. & May, R. M. (1978). Regulation and stability of host–parasite population interactions. I. Regulatory processes. Journal of Animal Ecology 47, 219–48.Google Scholar
Anderson, R. M., Whitfield, P. J. & Mills, C. A. (1977). An experimental study of the population dynamics of an ectoparasitic digenean Transversotrema patialense (Soparker): the cercarial and adult stages. Journal of Animal Ecology 46, 555–80.Google Scholar
Ansari, N. (1973). Epidemiology and Control of Schistosomiasis (Bilharziasis). Basel: S. Karger.Google Scholar
Barbosa, F. S. (1962). Aspects of the ecology of the intermediate hosts of Schistosoma mansoni interfering with the transmission of bilharziasis in north-eastern Brazil. In Bilharziasis: Ciba Foundation Symposium (ed. Wolslenholme, G. E. and O'Connor, M.), pp. 23–35. London: Churchill.Google Scholar
Barbosa, E. S. & Oliver, L. (1958). Studies on the snail vectors of biharziasis mansoni in north-eastern Brazil. Bulletin of the World Health Organization 18, 895.Google Scholar
Barbour, A. D. (1978). Macdonald's Model and the transmission of bilharzia. Transactions of the Royal Society of Tropical Medicine and Hygiene 72, 6–15.CrossRefGoogle ScholarPubMed
Barlow, C. H. & Muench, H. (1951). Life span and monthly mortality rate of Bulinus truncatus and Planorbis boissyi, the intermediate hosts of schistosomiasis in Egypt. Journal of Parasitology 37, 165–73.CrossRefGoogle Scholar
Bauman, P. M., Bennett, H. J. & Ingalls, J. W. (1948). The molluscan intermediate host and schistosomiasis japonicum. II. Observations on the production and rate of emergence of cercariae of Schistosoma japonicum from the molluscan intermediate host, Oncomelania quadrasi. American Journal of Tropical Medicine 28, 567–75.Google Scholar
Berrie, A. D. (1970). Snail problems in African schistosomiasis. In Advances in Parasitology, vol. 8, (ed. Ben, Dawes), pp. 43–96. London: Academic Press.Google Scholar
Bradley, D. J. (1977). Human pest and disease problems: contrasts between developing and developed countries. In Origins of Pest, Parasite, Disease and Weed Problems (ed. Cherrett, J. M. and Sagar, G. R.), pp. 329–345. Oxford: Blackwell.Google Scholar
Bradley, D. J. & May, R. M. (1978). Consequences of helminth aggregation for the dynamics of schistosomiasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 72, 262–73.Google Scholar
Cheever, A. W. (1977). A quantitative post mortem study of schistosomiasis mansoni in man. American Journal of Tropical Medicine and Hygiene, 17, 38–64.Google Scholar
Chernin, E. & Michelson, E. H. (1957). Studies on the biological control of schistosomebearing snails. III. The effects of population density on growth and fecundity in Australorbis glabratus. American Journal of Hygiene 65, 57–70.Google Scholar
Christensen, B. M. (1978). Dirofilaria immitis: effect on longevity of Aedes trivittatus. Experimental Parasitology 44, 116–23.Google Scholar
Christensen, B. M. & Hollander, A. L. (1978). Effect of temperature on vector-parasite relationships of Aedes trivittatus and Dirofilaria immitis. Proceedings of the Helminthological Society of Washington 45, 115–19.Google Scholar
Christie, J. D. & Upatham, E. S. (1977). Control of Schistosoma mansoni transmission by chemotherapy in St Lucia. II. Biological results. The American Journal of Tropical Medicine and Hygiene 26, 894–9.Google Scholar
Chu, K. Y., Massoud, J. & Arfaa, F. (1967). The survival time and fecundity of Bulinus truncatus after desiccation in mud. Annals of Tropical Medicine and Parasitology 61, 139–43.CrossRefGoogle ScholarPubMed
Chu, K. Y., Massoud, J. & Sabbaghian, H. (1966 a). Host–parasite relationship of Bulinus truncatus and Schistosoma haematobium in Iran. 1. Effect of the ago of B. truncatus on the development of S. haematobium. Bulletin of the World Health Organization 34, 113–19.Google Scholar
Chu, K. Y., Massoud, J. & Sabbaghian, H. (1966 b). Host-parasite relationship of Bulinus truncatus and Schistosoma haematobium in Iran. 3. Effect of water temperature on the ability of miracidia to infect snails. Bulletin of the World Health Organization 34, 131–3.Google Scholar
Chu, K. Y., Sabbaghian, H. & Massoud, J. (1966). Host-parasite relationship of Bulinus truncatus and Schistosoma haematobium in Iran. 2. Effect of exposure dosage of miracidia on the biology of the snail host and the development of the parasites. Bulletin of the World Health Organization 34, 131–3.Google Scholar
Cohen, J. E. (1973). Selective host mortality in a calalytic model applied to schistosomiasis. American Naturalist 107, 199–212.CrossRefGoogle Scholar
Cohen, J. E. (1976). Schistosomiasis, a human–parasite system. In Theoretical Ecology: Principles and Applications (ed. May, R. M.). Oxford: Blackwell.Google Scholar
Cohen, J. E. (1977). Mathematical models of schistosomiasis. Annual Review of Ecology and Systematics 8, 209–33.Google Scholar
Crofton, H. D. (1971). A quantitative approach to parasitism. Parasitology 62, 179–93.Google Scholar
Dazo, B. C., Hairston, N. G. & Dawood, I. K. (1966). The ecology of Bulinus truncatus and Biomphalaria alexandrina and its implications for the control of bilharziasis in the Egypt-49 project area. Bulletin of the World Health Organization 35, 339–56.Google Scholar
Evans, A. S. & Stirewalt, M. A. (1951). Variations in infectivity of cercariae of Schistosoma mansoni. Experimental Parasitology 1, 19–33.CrossRefGoogle Scholar
Fain, A. (1953). Contribution to the study of the larval forms of helminths in the Belgian Congo, and especially of the larvae of Schistosoma mansoni. Mémoires, Institut Royal Colonial Belge. Section des sciences naturelles et medicales 22, 1–312.Google Scholar
Fine, P. E. M. & Lehman, J. S. (1977). Mathematical models of schistosomiasis: report of a workshop. American Journal of Tropical Medicine and Hygiene 26, 500–4.CrossRefGoogle ScholarPubMed
Goddard, M. J. (1978). On Macdonald's model for schistosomiasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 72, 123–31.CrossRefGoogle ScholarPubMed
Gordon, R. M., Davey, T. H. & Peaston, H. (1934). The transmission of human bilharziasis in Sierra Leone, with an account of the life-cycle of the schistosomes concerned, S. mansoni and S. haematobium. Annals of Tropical Medicine and Parasitology 28, 323–419.Google Scholar
Gretillat, S. (1961). The epidemiology of vesical bilharziasis in eastern Senegal: observations on the ecology of Bulinus guernei and Bulinus senegalensis. Bulletin of the World Health Organization 25, 459–66.Google ScholarPubMed
Hairston, N. G. (1965). An analysis of age-prevalence data by catalytic models. A contribution to the study of bilharziasis. Bulletin of the World Health Organization 33, 163–75.Google Scholar
Harry, H. W. & Aldrich, D. V. (1958). The ecology of Australorbis glabratus in Puerto Rico. Bulletin of the World Health Organization 18, 819–32.Google Scholar
Hsu, H. F., Hsu, S. Y. L. & Ritchie, L. S. (1955). Epidemiological study on schistosomiasis japonica in Formosa. American Journal of Tropical Medicine and Hygiene 4, 1042–8.Google Scholar
Jordan, P. (1977). Schistosomiasis–research to control. American Journal of Tropical Medicine and Hygiene 26, 877–86.Google Scholar
Kennedy, C. R. & Rumpus, A. (1977). Long term changes in the size of the Pomphorhynchus laevis (Acanthocephala) population in the River Avon. Journal of Fish Biology 10, 35–42.Google Scholar
Kuntz, R. E. (1955). Biology of the schistosome complexes. American Journal of Tropical Medicine and Hygiene 4, 383–414.Google Scholar
Lee, K. L. & Lewis, E. R. (1976). Delay time models of population dynamics with application to schistosomiasis control. IEEE Transactions of Biomedical Engineering BME-23, 225–33.Google Scholar
Lewis, T. (1975). A model for the parasitic disease bilharziasis. Advances in Applied Probability 7, 673–704.Google Scholar
Macdonald, G. (1952). The analysis of equilibrium in malaria. Tropical Disease Bulletin 49, 813–28.Google Scholar
Macdonald, G. (1965). The dynamics of helminth infections with special reference to schistosomes. Transactions of the Royal Society of Tropical Medicine and Hygiene 59, 489–506.Google Scholar
May, R. M. (1977). Togetherness among schistosomes: its effects on the dynamics of the infection. Mathematical Biosciences 35, 301–43.CrossRefGoogle Scholar
McMullen, D. B. (1947). The control of schistosomiasis japonica. I. Observations on the habits, ecology, and life cycle of Oncomelania quadrasi the molluscan intermediate host of Schistosoma japonicum in the Philippine Islands. American Journal of Hygiene 45, 259–73.Google ScholarPubMed
McMullen, D. B., Endo-Itabashi, T., Sato, S., Komiyama, S. & Stone, P. R. (1951). Seasonal studies of S. japonicum in the intermediate host, Oncomelania nosophora. American Journal of Hygiene 54, 416–30.Google Scholar
Muench, H. (1959). Catalytic Models in Epidemiology. Cambridge, Massachusetts: Harvard University Press.Google Scholar
Nasell, I. (1976 a). A hybrid model of schistosomiasis. Theoretical Population Biology 10, 47–69.Google Scholar
Nasell, I. (1976 b). On eradication of schistosomiasis. Theoretical Population Biology 10, 133–44.CrossRefGoogle ScholarPubMed
Nasell, I. & Hirsch, W. M. (1973). The transmission dynamics of schistosomiasis. Communications in Pure and Applied Mathematics 26, 395–453.Google Scholar
Pan, C. T. (1965). Studies on the host–parasite relationship between Schistosoma mansoni and the snail Australorbis glabratus. American Journal of Tropical Medicine and Hygiene 14, 931–76.Google Scholar
Pellegrino, J. & De Maria, M. (1966). Results of exposing mice to natural pond water harbouring a colony of Australorbis glabratus highly infected with Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 15, 333–6.Google Scholar
Pesigan, T. P., Hairston, N. G., Jaurequi, J. J., Garcia, E. G., Santos, A. T., Santos, B. C. & Besa, A. A. (1958). Studies on Schistosoma japonicum infection in the Philippines. 2. The molluscan host. Bulletin of the World Health Organization 18, 481–578.Google Scholar
Ritchie, L. S., Radke, M. G. & Ferguson, F. F. (1962). Population dynamics of Australorbis glabratus in Puerto Rico. Bulletin of the World Health Organization 27, 171–81.Google ScholarPubMed
Schreiber, F. G. & Schubert, M. (1949). Experimental infection of the snail Australorbis glabratus with the trematode schistosoma mansoni and the production of cercariae. Journal of Parasitology 35, 91–100.Google Scholar
Scott, J. A. (1942). The epidemiology of schistosomiasis in Venezuela. American Journal of Hygiene 35, 337–66.Google Scholar
Schiff, C. J., Evans, A., Yiannakis, C. & Eardley, M. (1975). Seasonal influence on the production of Schistosoma haematobium and S. mansoni cercariae in Rhodesia. International Journal for Parasitology 5, 119–23.Google Scholar
Smithers, S. R. (1956). On the ecology of schistosome vectors in the Gambia, with evidence of their role in transmission. Transactions of the Royal Society of Tropical Medicine and Hygiene 50, 354–65.CrossRefGoogle ScholarPubMed
Standen, O. D. (1949). Experimental schistosomiasis. II. Maintenance of Schistosoma mansoni in the laboratory, with some notes on experimental infection with S. haematobium. Annals of Tropical Medicine and Parasitology 43, 268–83.Google Scholar
Standen, O. D. (1952). Experimental infection of Australorbis glabratus with Schistosoma mansoni. I. Individual and mass infection of snails, and the relationship to temperature and season. Annals of Tropical Medicine and Parasitology 46, 48–53.Google Scholar
Stirewalt, M. A. (1954). Effect of snail maintenance temperature on development of Schistosoma mansoni. Experimental Parasitology 3, 504–16.Google Scholar
Sturrock, B. M. (1966). The influence of infection with Schistosoma mansoni on the growth rate and reproduction of Biomphalaria pfeifferi. Annals of Tropical Medicine and Parasitology 60, 187–97.CrossRefGoogle ScholarPubMed
Sturrock, B. M. (1967). The effect of infection with Schistosoma haematobium on the growth and reproduction rates of Bulinus (Physopsis) nasutus productus. Annals of Tropical Medicine and Parasitology 61, 321–5.Google Scholar
Sturrock, R. F. (1970). An investigation of some factors influencing the survival of Biomphalaria glabrata deprived of water. Annals of Tropical Medicine and Parasitology 64, 365–71.Google Scholar
Sturrock, R. F. (1973). Field studies on the transmission of Schistosoma mansoni and on the bionomics of its intermediate host, Biomphaloria glabrata, on St Lucia, West Indies. International Journal for Parasitology 3, 175–94.Google Scholar
Sturrock, R. F. & Webbe, G. (1971). The application of catalytic models to schistosomiasis in snails. Journal of Helminthology. 45, 189–200.Google Scholar
Sturrock, B. M. & Sturrock, R. F. (1970). Laboratory studies of the host parasite relationship of Schistosoma mansoni and Biomphaloria glabrata from St Lucia, West Indies. Annals of Tropical Medicine and Parasitology 64, 357–63.Google Scholar
Sturrock, R. F., Cohen, J. E. & Webbe, G. (1975). Catalytic curve analysis of schistosomiasis in snails. Annals of Tropical Medicine and Parasitology 69, 133–4.Google Scholar
Sugiura, S. (1933). Studies on the biology of Oncomelania nosphora, Robson, an intermediate host of schistosomiasis japonica. Niigata Ika Daigaku Byorigaku Kyoshitsu Kenkyu Hokoku 31, 1–18.Google Scholar
Teesdale, C. (1962). Ecological observations on the molluscs of significance in the transmission of bilharziasis in Kenya. Bulletin of the World Health Organization 27, 759–82.Google Scholar
Vogel, H. (1948). Maintenance of Oncomelania hupensis and experimental infection of it with Bilharzia japonicum. Zeitschrift für Parasitologie 14, 70–91.Google Scholar
Warren, K. S. (1973). Regulation of the prevalence and intensity of schistosomiasis in man: immunology or ecology? Journal of Infectious Diseases 127, 595–609.Google Scholar
Webbe, G. (1962 a). Population studies on intermediate hosts in relation to transmission of bilharziasis in East Africa. In Bilharziasis, Ciba Foundation Symposium (ed. Wolslenholme, G. W. E and O'Connor, M.), pp. 7–22. London: Churchill.Google Scholar
Webbe, G. (1962 b). The transmission of Schistosoma haematobium in an area of Lake Province Tanganyika. Bulletin of the World Health Organization 27, 59–85.Google Scholar
Wright, C. A. (1960). The crowding phenomenon in laboratory colonies of freshwater snails. Annals of Tropical Medicine and Parasitology 54, 224–32.Google Scholar
Wright, W. H. (1973). Geographical distribution of schistosomes and their intermediate hosts. In Epidemiology and Control of shistosomiasis (Bilharziasis) (ed. Ansari, N.), pp. 32–249. London: S. Karger.Google Scholar
Wright, W. H., McMullen, D. B., Bennett, H. J., Bauman, P. M. & Ingalls, J. W.(1947). The epidemiology of schistosomiasis japonica in the Philippine Islands and Japan III. Surveys of endemic areas of schistosomiasis japonica in Japan. American Journal of Tropical Medicine 27, 417–47.Google Scholar