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Density dependence and overdispersion in the transmission of helminth parasites

  • T. S. CHURCHER (a1), N. M. FERGUSON (a1) and M.-G. BASÁÑEZ (a1)
Abstract

The influence of density-dependent processes on the transmission of parasitic helminths is determined by both the severity of the regulatory constraints and the degree of parasite overdispersion among the host population. We investigate how overdispersed parasite distributions among humans influence transmission levels in both directly- and indirectly-transmitted nematodes (Ascaris lumbricoides and Onchocerca volvulus). While past work has assumed, for simplicity, that density dependence acts on the average worm load, here we model density-dependence as acting on individual parasite burdens before averaging across hosts. A composite parameter, which we call the effective transmission contribution, is devised to measure the number of transmission stages contributed by a given worm burden after incorporating overdispersion in adult worm mating probabilities and other density-dependent mechanisms. Results indicate that the more overdispersed the parasite population, the greater the effect of density dependence upon its transmission dynamics. Strong regulation and parasite overdispersion make the relationship between mean worm burden and its effective contribution to transmission highly non-linear. Consequently, lowering the intensity of infection in a host population using chemotherapy may produce only a small decline in transmission (relative to its initial endemic level). Our analysis indicates that when parasite burden is low, intermediate levels of parasite clustering maximize transmission. Implications are discussed in relation to existing control programmes and the spread of anthelmintic resistance.

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Tel: +44 (0) 20 75943229. Fax: +44 (0)20 74023927. E-mail: thomas.churcher@imperial.ac.uk
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ADLER, F. R. & KRETZSCHMAR, M. ( 1992). Aggregation and stability in parasite-host models. Parasitology104, 199205.

ANDERSON, R. M. ( 1982). The population dynamics and control of hookworm and roundworm infections. In Population Dynamics of Infectious Diseases (ed. Anderson, R. M.), pp. 67108. Chapman and Hall, London.

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. Parasitology85, 373398.

ANDERSON, R. M. & MAY, R. M. ( 1978). Regulation and stability of host-parasite population interactions. I. Regulatory processes. Journal of Animal Ecology47, 219247.

ANDERSON, R. M. & MAY, R. M. ( 1985) Helminth infections of humans. Mathematical models, population dynamics, and control. Advances in Parasitology24, 1101.

ANDERSON, R. M. & MEDLEY, G. F. ( 1985). Community control of helminth infections of man by mass and selective chemotherapy. Parasitology90, 629660.

BASÁÑEZ, M.-G. & BOUSSINESQ, M. ( 1999). Population biology of human onchocerciasis. Philosophical Transactions of the Royal Society of London, Series B Biological Sciences354, 809826.

BASÁÑEZ, M.-G., BOUSSINESQ, M., PRODHON, J., FRONTADO, H., VILLAMIZAR, N. J., MEDLEY, G. F. & ANDERSON, R. M. ( 1994). Density-dependent processes in the transmission of human onchocerciasis: intensity of microfilariae in the skin and their uptake by the simuliid host. Parasitology108, 115127.

BASÁÑEZ, M.-G., REMME, J. H. F., ALLEY, E. S., BAIN, O., SHELLEY, A. J., MEDLEY, G. F. & ANDERSON, R. M. ( 1995). Density-dependent processes in the transmission of human onchocerciasis: relationship between the numbers of microfilariae ingested and successful larval development in the simuliid vector. Parasitology110, 409427.

BASÁÑEZ, M.-G., TOWNSON, H., WILLIAMS, J. R., FRONTADO, H., VILLAMIZAR, N. J. & ANDERSON, R. M. ( 1996). Density-dependent processes in the transmission of human onchocerciasis: relationship between microfilarial intake and mortality of the simuliid vector. Parasitology113, 331355.

BORSBOOM, G. J. J. M., BOATIN, B., NAGELKERKE, N. J. D., AGOUA, H., AKPOBOUA, K. L. B., SOUMBEY ALLEY, E. W., BISSAN, Y., RENZ, A., YAMÉOGO, L., REMME, H. & HABBEMA, J. D. F. ( 2003). Impact of ivermectin on onchocerciasis transmission: assessing the empirical evidence that repeated ivermectin mass treatment may lead to the elimination/eradication in West-Africa. Filaria Journal, 2.

CHEKE, R. A., GARMS, R. & KERNER, M. ( 1982). The fecundity of Simulium damnosum s.l. in northern Togo and infections with Onchocerca spp. Annals of Tropical Medicine and Parasitology76, 561568.

CROFTON, H. D. ( 1971). A quantitative approach to parasitism. Parasitology62, 179194.

DEMANOU, M., ENYONG, P., PION, S. D. S., BASÁŇEZ, M.-G. & BOUSSINESQ, M. ( 2003). Experimental studies on the transmission of Onchocerca volvulus by its vector in the Sanaga valley (Cameroon): Simulium squamosum B. Intake of microfilariae and their migration to the haemocoel of the vector. Annals of Tropical Medicine and Parasitology97, 381402.

DENHAM, D. A., PONNUDURAI, T., NELSON, G. S., ROGERS, R. & GUY, F. ( 1972). Studies with Brugia pahangi. II. The effect of repeatedly infection on parasite levels in cats. International Journal for Parasitology2, 401407.

DIETZ, K. ( 1988). Density-dependence in parasite transmission dynamics. Parasitology Today4, 9197.

DUERR, H. P., DIETZ, K., SCHULZ-KEY, H., BÜTTNER, D. W. & EICHNER, M. ( 2003). Density-dependent parasite establishment suggests infection-associated immunosuppression as an important mechanism for parasite density regulation in onchocerciasis. Transactions of the Royal Society of Tropical Medicine and Hygiene97, 242250.

DUERR, H. P., DIETZ, K., SCHULZ-KEY, H., BÜTTNER, D. W. & EICHNER, M. ( 2004). The relationships between the burden of adult parasites, host age and the microfilarial density in human onchocerciasis. International Journal for Parasitology34, 463473.

DUKE, B. O. L. ( 1968). Studies on factors influencing the transmission of onchocerciasis. IV. The biting cycles, infective biting density and transmission potential of ‘forest’ Simulium damnosum. Annals of Tropical Medicine and Parasitology62, 95106.

GALVANI, A. P. ( 2003). Immunity, antigenic heterogeneity, and aggregation of helminth parasites. Journal of Parasitology89, 232241.

GRENFELL, B. T., WILSON, K., ISHAM, V. S., BOYD, H. E. G. & DIETZ, K. ( 1995). Modelling patterns of parasite aggregation in natural populations: trichostrongylid nematode-ruminant interactions as a case study. Parasitology111, S135S151.

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. Parasitology101, 139143.

HALL, A. & HOLLAND, C. ( 2000). Geographical variation in Ascaris lumbricoides fecundity and its implications for helminth control. Parasitology Today16, 540544.

HARTLEY, S. & SHORROCKS, B. ( 2002). A general framework for the aggregation model of coexistence. Journal of Animal Ecology71, 651662.

ISHAM, V. ( 1995). Stochastic models of host-macroparasite interaction. Annals of Applied Probability5, 720740.

KEYMER, A. ( 1982). Density-dependent mechanisms in the regulation of intestinal helminth populations. Parasitology84, 573587.

KLÄGER, S. L., WHITWORTH, J. A. G. & DOWNHAM, M. D. ( 1996). Viability and fertility of adult Onchocerca volvulus after 6 years of treatment with ivermectin. Tropical Medicine and International Health1, 581589.

KRETZSCHMAR, M. & ADLER, F. R. ( 1993). Aggregated distributions in models for patchy populations. Theoretical Population Biology43, 130.

LITTLE, M. P., BREITLING, L. P., BASÁÑEZ, M.-G., ALLEY, E. S. & BOATIN, B. ( 2004). Association between microfilarial load and excess mortality in onchocerciasis: an epidemiological study. Lancet363, 15141521.

MACDONALD, G. ( 1965). The dynamics of helminth infections, with special reference to schistosomes. Transactions of the Royal Society of Tropical Medicine and Hygiene59, 489506.

MAY, R. M. ( 1977). Togetherness in schistosomes: its effects on the dynamics of infection. Mathematical Biosciences35, 301343.

MEDLEY, G. F. ( 1992). Which comes first in host-parasite systems: density dependence or parasite distribution? Parasitology Today8, 321322.

MEDLEY, G. F., GUYATT, H. L. & BUNDY, D. A. P. ( 1993). A quantitative framework for evaluating the effect of community treatment on the morbidity due to ascariasis. Parasitology106, 211221.

MOLYNEUX, D. H. & ZAGARIA, N. ( 2002). Lymphatic filariasis elimination: progress in global programme development. Annals of Tropical Medicine and Parasitology96, S15S40.

NORMAN, R. A., CHAN, M. S., SRIVIDYA, A., PANI, S. P., RAMAIAH, K. D., VANAMAIL, P., MICHAEL, E., DAS, P. K. & BUNDY, D. A. P. ( 2000). EPIFIL: The development of an age-structured model for describing the transmission dynamics and control of lymphatic filariasis. Epidemiology and Infection124, 529541.

PATERSON, S. & VINEY, M. E. ( 2002). Host immune responses are necessary for density dependence in nematode infections. Parasitology125, 283292.

PLAISIER, A. P., VAN OORTMARSSEN, G. J., HABBEMA, J. D. F., REMME, J. & ALLEY, E. S. ( 1990). ONCHOSIM – A model and computer-simulation program for the transmission and control of onchocerciasis. Computer Methods and Programs in Biomedicine31, 4356.

QUINNELL, R. J., GRAFEN, A. & WOOLHOUSE, M. E. J. ( 1995). Changes in parasite aggregation with age: a discrete infection model. Parasitology111, 635644.

QUINNELL, R. J. ( 2003). Genetics of susceptibility to human helminth infection. International Journal for Parasitology33, 12191231.

RICHARDS, F. O., BOATIN, B., SAUERBREY, M. & SÉKÉTÉLI, A. ( 2001). Control of onchocerciasis today: status and challenges. Trends in Parasitology17, 558563.

ROBERTS, M.-G. ( 1995). A pocket guide to host-parasite models. Parasitology Today11, 172177.

ROSÀ, R. & PUGLIESE, A. ( 2002). Aggregation, stability, and oscillations in different models for host-macroparasite interactions. Theoretical Population Biology61, 319334.

ROSÀ, R., PUGLIESE, A., VILLANI, A. & RIZZOLI, A. ( 2003). Individual-based vs. deterministic models for macroparasites: host cycles and extinction. Theoretical Population Biology63, 295307.

SÉKÉTÉLI, A., ADEOYE, G., EYAMBA, A., NNORUKA, E., DRAMEH, P., AMAZIGO, U. V., NOMA, M., AGBOTON, F., AHOLOU, Y., KALE, O. O. & DADZIE, K. Y. ( 2002). The achievements and challenges of the African Programme for Onchocerciasis Control (APOC). Annals of Tropical Medicine and Parasitology96, 1528.

SHAW, D. J., GRENFELL, B. T. & DOBSON, A. P. ( 1998). Patterns of macroparasite aggregation in wildlife host populations. Parasitology117, 597610.

SOUMBEY-ALLEY, E., BASÁÑEZ, M.-G., BISSAN, Y., BOATIN, B. A., REMME, J. H. F., NAGELKERKE, N. J. D., DE VLAS, S. J., BORSBOOM, G. J. J. M. & HABBEMA, J. D. F. ( 2004). Uptake of Onchocerca volvulus (Nematoda: Onchocercidae) by Simulium (Diptera: Simuliidae) is not strongly dependent on the density of skin microfilariae in the human host. Journal of Medical Entomology41, 8394.

TALLIS, G. M. & LEYTON, M. ( 1966). A stochastic approach to the study of parasite populations. Journal of Theoretical Biology13, 251260.

TREES, A. J., WAHL, G., KLÄGER, S. & RENZ, A. ( 1992). Age-related diffrences in parasitosis may indicate acquired immunity against microfilariae in cattle naturally infected with Onchocerca ochengi. Parasitology104, 247252.

WALSH, J. F., DAVIES, J. B., LE BERRE, R. & GARMS, R. ( 1978). Standardization of criteria for assessing the effects of Simulium control in onchocerciasis control programmes. Transactions of the Royal Society of Tropical Medicine and Hygiene72, 675676.

WOOLHOUSE, M. E. J. ( 1992). A theoretical framework for the immunoepidemiology of helminth infection. Parasite Immunology14, 563578.

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