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Population biology of multispecies helminth infection: interspecific interactions and parasite distribution

Published online by Cambridge University Press:  23 May 2005

C. BOTTOMLEY ,
V. ISHAM  and
M.-G. BASÁÑEZ
C. BOTTOMLEY
Affiliation:
Centre for Mathematics and Physics in the Life Sciences and Experimental Biology (CoMPLEX), Wolfson House, 4 Stephenson Way, London NW1 2HE
V. ISHAM
Affiliation:
Department of Statistical Science, University College London, Gower Street, London WC1E 6BT
M.-G. BASÁÑEZ
Affiliation:
Department of Infectious Disease Epidemiology, Imperial College London, St Mary's Campus, Norfolk Place, London W2 1PG
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Abstract

Despite evidence for the existence of interspecific interactions between helminth species, there has been no theoretical exploration of their effect on the distribution of the parasite species in a host population. We use a deterministic model for the accumulation and loss of adult worms of 2 interacting helminth species to motivate an individual-based stochastic model. The mean worm burden and variance[ratio ]mean ratio (VMR) of each species, and the correlation between the two species are used to describe the distribution within different host age classes. We find that interspecific interactions can produce convex age-intensity profiles and will impact the level of aggregation (as measured by the VMR). In the absence of correlated exposure, the correlation in older age classes may be close to zero when either intra- or interspecific synergistic effects are strong. We therefore suggest examining the correlation between species in young hosts as a possible means of identifying interspecific interaction. The presence of correlation between the rates of exposure makes the interpretation of correlations between species more difficult. Finally we show that in the absence of interaction, strong positive correlations are generated by averaging across most age classes.

Keywords

helminthsinterspecific interactionsstochastic modelcorrelationoverdispersion
Type
Research Article
Information
Parasitology , Volume 131 , Issue 3 , September 2005 , pp. 417 - 433
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

Anderson, R. M. and Gordon, D. M. ( 1982). Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortalities. Parasitology 85, 373–398.CrossRefGoogle Scholar
Anderson, R. M. and May, R. M. ( 1985 a). Helminth infections of humans: mathematical models, population dynamics, and control. Advances in Parasitology 24, 1–101.Google Scholar
Anderson, R. M. and May, R. M. ( 1985 b). Herd immunity to helminth infection and implications for parasite control. Nature 315, 493–496.Google Scholar
Anderson, R. M. and May, R. M. ( 1991). Infectious Diseases of Humans: Dynamics and Control. Oxford University Press, Oxford.
Behnke, J. M., Bajer, A., Sinski, E. and Wakelin, D. ( 2001). Interactions involving intestinal nematodes of rodents: experimental and field studies. Parasitology 122 (Suppl.), S39–S49.CrossRefGoogle Scholar
Behnke, J. M., Gilbert, F., Abu-Madi, M. and Lewis, J. ( 2005). Do helminth parasites of wood mice interact? Journal of Animal Ecology (in the Press).Google Scholar
Booth, M., Vennervald, B. J., Butterworth, A. E., Kariuki, H. C., Amaganga, C., Kimani, G., Mwatha, J. K., Otedo, A., Ouma, J. H. and Dunne, D. W. ( 2004 a). Exposure to malaria affects the regression of hepatosplenomegaly after treatment for Schistosoma mansoni infection in Kenyan children. BMC Medicine 2, 36.Google Scholar
Booth, M., Vennervald, B. J., Kenty, L., Butterworth, A. E., Kariuki, H. C., Kadzo, H., Ireri, E., Amaganga, C., Kimani, G., Mwatha, J. K., Otedo, A., Ouma, J. H., Muchiri, E. and Dunne, D. W. ( 2004 b). Micro-geographical variation in exposure to Schistosoma mansoni and malaria, and exacerbation of splenomegaly in Kenyan school-aged children. BMC Infectious Diseases 4, 13.Google Scholar
Bundy, D., Sher, A. and Michael, E. ( 2000). Good worms or bad worms: do worm infections affect the epidemiological patterns of other diseases? Parasitology Today 16, 273–274.Google Scholar
Bush, A. O. and Holmes, J. C. ( 1986). Intestinal helminths of lesser scaup ducks: patterns of association. Canadian Journal of Zoology 64, 132–141.CrossRefGoogle Scholar
Byrne, C. J., Holland, C. V., Kennedy, C. R. and Poole, W. R. ( 2003). Interspecific interactions between acanthocephala in the intestine of brown trout: are they more frequent in Ireland? Parasitology 127, 399–409.Google Scholar
Christensen, N. O., Nansen, P., Fagbemi, B. O. and Monrad, J. ( 1987). Heterologous antagonistic and synergistic interactions between helminths and between helminths and protozoans in concurrent experimental infection of mammalian hosts. Parasitology Research 73, 387–410.CrossRefGoogle Scholar
Cox, F. E. G. ( 2001). Concomitant infections, parasites and immune responses. Parasitology 122 (Suppl.), S23–S38.CrossRefGoogle Scholar
Dobson, A. P. ( 1985). The population dynamics of competition between parasites. Parasitology 91, 317–347.CrossRefGoogle Scholar
Duerr, H. P., Dietz, K. and Eichner, M. ( 2003). On the interpretation of age-intensity profiles and dispersion patterns in parasitological surveys. Parasitology 126, 87–101.CrossRefGoogle Scholar
Esch, G. and Fernandez, J. ( 1993). A Functional Biology of Parasitism: Ecological and Evolutionary Implications. Chapman and Hall, London.CrossRef
Faulkner, H., Turner, J., Behnke, J., Kamgno, J., Rowlinson, M.-C., Bradley, J. and Boussinesq, M. ( 2005). Associations between filarial and gastrointestinal nematodes. Transactions of the Royal Society of Tropical Medicine and Hygiene 99, 301–312.CrossRefGoogle Scholar
Fenwick, A., Savioli, L., Engels, D., Bergquist, N. R. and Todd, M. H. ( 2003). Drugs for the control of parasitic diseases: current status and development in schistosomiasis. Trends in Parasitology 19, 509–515.CrossRefGoogle Scholar
Fulford, A. J., Butterworth, A. E., Sturrock, R. F. and Ouma, J. H. ( 1992). On the use of age-intensity data to detect immunity to parasitic infections, with special reference of Schistosoma mansoni in Kenya. Parasitology 105, 219–227.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
Geiger, S., Hoffmann, W., Rapp, J., Schulz-Key, H. and Eisenbeiss, W. ( 1996). Filariidae: cross-protection in filarial infections. Experimental Parasitology 83, 352–356.CrossRefGoogle Scholar
Gems, D. ( 2000). Longevity and ageing in parasitic and free-living nematodes. Biogerontology 1, 289–307.CrossRefGoogle Scholar
Hall, A. and Holland, C. ( 2000). Geographical variation in Ascaris lumbricoides fecundity and its implications for helminth control. Parasitology Today 16, 540–544.CrossRefGoogle Scholar
Harms, G. and Feldmeier, H. ( 2002). HIV infection and tropical diseases-deleterious interactions in both directions? Tropical Medicine and International Health 7, 479–488.Google Scholar
Haukisalmi, V. and Henttonen, H. ( 1998). Analyzing interspecific associations in parasites: alternative methods and effects of sampling heterogeneity. Oecologia 116, 565–574.CrossRefGoogle Scholar
Hayward, C. J., Perera, K. M. and Rohde, K. ( 1998). Assemblages of ectoparasites of a pelagic fish, slimy mackerel (Scomber australasicus), from south-eastern Australia. International Journal for Parasitology 28, 263–273.CrossRefGoogle Scholar
Herbert, J. and Isham, V. ( 2000). Stochastic host-parasite interaction models. Journal of Mathematical Biology 40, 343–371.CrossRefGoogle Scholar
Isham, V. ( 1995). Stochastic models of host-macroparasite interaction. The Annals of Applied Probability 5, 720–740.CrossRefGoogle Scholar
Jackson, J. A., Tinsley, R. C. and Hinkel, H. H. ( 1998). Mutual exclusion of congeneric monogenean species in a space-limited habitat. Parasitology 117, 563–569.CrossRefGoogle Scholar
Kennedy, C. ( 1975). Ecological Animal Parasitology. Blackwell Scientific Publications, Oxford.
Kleinbaum, D. G., Kupper, L. L., Muller, K. E. and Nizam, A. ( 1998). Applied Regression Analysis and other Multivariable Methods, 3rd Edn. Duxbury Press, Pacific Grove, USA.
Kuris, A. M. and Lafferty, K. D. ( 1994). Community structure: larval trematodes in snail hosts. Annual Review of Ecology and Systematics 25, 189–217.CrossRefGoogle Scholar
Leathwick, D., Miller, C., Brown, A. and Sutherland, I. ( 1999). The establishment rate of Ostertagia circumcincta and Trichostrongylus colubriformis in lactating Romney ewes. International Journal for Parasitology 29, 315–320.CrossRefGoogle Scholar
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 Scholar
Lotz, J. M. and Font, W. F. ( 1994). Excess positive associations in communities of intestinal helminths of bats: a refined null hypothesis and a test of the facilitation hypothesis. Journal of Parasitology 80, 398–413.CrossRefGoogle Scholar
Mariotti, S. P., Pararajasegaram, R. and Resnikoff, S. ( 2003). Trachoma: looking forward to global elimination of trachoma by 2020 (GET 2020). American Journal of Tropical Medicine and Hygiene 69, 33–35.CrossRefGoogle Scholar
Molyneux, D. H. and Zagaria, N. ( 2002). Lymphatic filariasis elimination: progress in global programme development. Annals of Tropical Medicine and Parasitology 96 (Suppl. 2), S15–S40.CrossRefGoogle Scholar
Moore, J. and Simberloff, D. ( 1990). Gastrointestinal helminth communities of bobwhite quail. Ecology 71, 344–359.CrossRefGoogle Scholar
Nacher, M. ( 2001). Malaria vaccine trials in a wormy world. Trends in Parasitology 17, 563–565.CrossRefGoogle Scholar
Nacher, M., Gay, F., Singhasivanon, P., Krudsood, S., Treeprasertsuk, S., Mazier, D., Vouldoukis, I. and Looareesuwan, S. ( 2000). Ascaris lumbricoides infection is associated with protection from cerebral malaria. Parasite Immunology 22, 107–113.CrossRefGoogle Scholar
Pacala, S. W. and 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 Scholar
Petney, T. N. and Ross, A. H. ( 1998). Multiparasite communities in animals and humans: frequency, structure and pathogenic significance. International Journal for Parasitology 28, 377–393.CrossRefGoogle Scholar
Plaisier, A. P., van Oortmarssen, G. J., Remme, J. and Habbema, J. D. ( 1991). The reproductive lifespan of Onchocerca volvulus in West African savanna. Acta Tropica 48, 271–284.CrossRefGoogle Scholar
Poulin, R. ( 1998). Evolutionary Ecology of Parasites. Chapman and Hall, London.
Price, P. W. ( 1980). Evolutionary Biology of Parasites. Princeton University Press, Princeton.
Quinnell, R. J. ( 2003). Genetics of susceptibility to human helminth infection. International Journal of Parasitology 33, 1219–1231.CrossRefGoogle Scholar
Remme, J. H. F., Binka, F. and Nabarro, D. ( 2001). Toward a framework and indicators for monitoring roll back malaria. American Journal of Tropical Medicine and Hygiene 64, 76–84.CrossRefGoogle Scholar
Roberts, M. G. and Dobson, A. P. ( 1995). The population dynamics of communities of parasitic helminths. Mathematical Biosciences 126, 191–214.CrossRefGoogle Scholar
Sékétéli, A., Adeoye, G., Eyamba, A., Nnoruka, E., Drameh, P., Amazigo, U. V., Noma, M., Agboton, F., Aholou, Y., Kale, O. O. and Dadzie, K. Y. ( 2002). The achievements and challenges of the African Programme for Onchocerciasis Control (APOC). Annals of Tropical Medicine and Parasitology 96 (Suppl. 1), S15–S28.CrossRefGoogle Scholar
Sharma, D. K., Chauhan, P. P. and Agrawal, R. D. ( 2000). Interaction between Trypanosoma evansi and Haemonchus contortus infection in goats. Veterinary Parasitology 92, 261–267.CrossRefGoogle Scholar
Simberloff, D. ( 1990). Free-living communities and alimentary tract helminths: hypotheses and pattern analyses. In Parasite Communities: Patterns and Processes (ed. Esch, G. W., Bush, A. O. and Aho, J. M.), pp. 289–319. Chapman and Hall, London.CrossRef
Tallis, G. M. and Leyton, M. ( 1966). A stochastic approach to the study of parasite populations. Journal of Theoretical Biology 13, 251–260.CrossRefGoogle Scholar
Tallis, G. M. and Leyton, M. ( 1969). Stochastic models of populations of helminthic parasites in the definitive host. I. Mathematical Biosciences 4, 39–48.CrossRefGoogle Scholar
Tchuem Tchuenté, L. A., Behnke, J. M., Gilbert, F. S., Southgate, V. R. and Vercruysse, J. ( 2003). Polyparasitism with Schistosoma haematobium and soil-transmitted helminth infections among school children in Loum, Cameroon. Tropical Medicine and International Health 8, 975–986.CrossRefGoogle Scholar
Thomas, J. D. ( 1964). Studies on populations of helminth parasites in brown trout (Salmo trutta L.). Journal of Animal Ecology 33, 83–95.CrossRefGoogle Scholar
Wahl, G., Enyong, P., Ngosso, A., Schibel, J. M., Moyou, R., Tubbesing, H., Ekale, D. and Renz, A. ( 1998). Onchocerca ochengi: epidemiological evidence of cross-protection against Onchocerca volvulus in man. Parasitology 116, 349–362.CrossRefGoogle Scholar
Wilson, K., Bjørnstad, O. N., Dobson, A. P., Merler, S., Poglayen, G., Randolph, S. E., Read, A. F. and Skorping, A. ( 2002). Heterogeneities in macroparasite infections: patterns and processes. In Ecology of Wildlife Diseases (ed. Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. and Dobson, A. P.), chapter 2. Oxford University Press, Oxford.
Wong, M. S., Bundy, D. A. and Golden, M. H. ( 1988). Quantitative assessment of geophagus behaviour as a potential source of exposure to geohelminth infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 82, 621–625.CrossRefGoogle Scholar
Woolhouse, M. E. J. ( 1992 a). A theoretical framework for the immunoepidemiology of helminth infection. Parasite Immunology 14, 563–578.Google Scholar
Woolhouse, M. E. J. ( 1992 b). Immunoepidemiology of intestinal helminths: pattern and process. Parasitology Today 8, 111.Google Scholar
Woolhouse, M. E. J., Ndamba, J. and Bradley, D. ( 1994). The interpretation of intensity and aggregation data for infections of Schistosoma haematobium. Transactions of the Royal Society of Tropical Medicine and Hygiene 88, 520–526.CrossRefGoogle Scholar