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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)

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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ADLER, F. R. & KRETZSCHMAR, M. ( 1992). Aggregation and stability in parasite-host models. Parasitology 104, 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. Parasitology 85, 373398.
ANDERSON, R. M. & MAY, R. M. ( 1978). Regulation and stability of host-parasite population interactions. I. Regulatory processes. Journal of Animal Ecology 47, 219247.
ANDERSON, R. M. & MAY, R. M. ( 1985) Helminth infections of humans. Mathematical models, population dynamics, and control. Advances in Parasitology 24, 1101.
ANDERSON, R. M. & MAY, R. M. ( 1992). Infectious Disease in Humans: Dynamics and Control. Oxford University Press, Oxford.
ANDERSON, R. M. & MEDLEY, G. F. ( 1985). Community control of helminth infections of man by mass and selective chemotherapy. Parasitology 90, 629660.
BASÁÑEZ, M.-G. & BOUSSINESQ, M. ( 1999). Population biology of human onchocerciasis. Philosophical Transactions of the Royal Society of London, Series B Biological Sciences 354, 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. Parasitology 108, 115127.
BASÁÑEZ, M.-G., COLLINS, R. C., PORTER, C. H., LITTLE, M. P. & BRANDLING-BENNETT, D. ( 2002). Transmission intensity and the patterns of Onchocerca volvulus infection in human communities. American Journal of Tropical Medicine and Hygiene 67, 669679.
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. Parasitology 110, 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. Parasitology 113, 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 Parasitology 76, 561568.
CROFTON, H. D. ( 1971). A quantitative approach to parasitism. Parasitology 62, 179194.
CROMPTON, D. W. T. ( 1989). Biology of Ascaris lumbricoides. In Ascariasis and its Prevention and Control (ed. Crompton, D. W. T., Nesheim, M. C. & Pawlowski, Z. S.), pp. 944. Taylor and Francis, London and Philadelphia.
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 Parasitology 97, 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 Parasitology 2, 401407.
DIETZ, K. ( 1988). Density-dependence in parasite transmission dynamics. Parasitology Today 4, 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 Hygiene 97, 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 Parasitology 34, 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 Parasitology 62, 95106.
DUKE, B. O. L. ( 1993). The population dynamics of Onchocerca volvulus in the human host. Tropical Medicine and Parasitology 44, 6168.
DUKE, B. O. L., ANDERSON, J. & FUGLSANG, H. ( 1975). The Onchocerca volvulus transmission potential and associated patterns of onchocerciasis at four Cameroon Sudan-savanna villages. Tropenmedizin und Parasitologie 26, 143154.
ELLIOTT, J. M. ( 1977). Some Methods for the Statistical Analysis of Samples of Benthic Invertebrates, 2nd edn. Freshwater biological Association, Scientific Publication 25, Titus Wilson, Cumbria.
GALVANI, A. P. ( 2003). Immunity, antigenic heterogeneity, and aggregation of helminth parasites. Journal of Parasitology 89, 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. Parasitology 111, 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. Parasitology 101, 139143.
HALL, A. & HOLLAND, C. ( 2000). Geographical variation in Ascaris lumbricoides fecundity and its implications for helminth control. Parasitology Today 16, 540544.
HARTLEY, S. & SHORROCKS, B. ( 2002). A general framework for the aggregation model of coexistence. Journal of Animal Ecology 71, 651662.
ISHAM, V. ( 1995). Stochastic models of host-macroparasite interaction. Annals of Applied Probability 5, 720740.
KEYMER, A. ( 1982). Density-dependent mechanisms in the regulation of intestinal helminth populations. Parasitology 84, 573587.
KLÄGER, S. L., WHITWORTH, J. A. G., POST, R. J., CHAVASSE, D. C. & DOWNHAM, M. D. ( 1993). How long do the effects of ivermectin on adult Onchocerca volvulus persist. Parasitology 44, 305310.
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 Health 1, 581589.
KRETZSCHMAR, M. & ADLER, F. R. ( 1993). Aggregated distributions in models for patchy populations. Theoretical Population Biology 43, 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. Lancet 363, 15141521.
MACDONALD, G. ( 1965). The dynamics of helminth infections, with special reference to schistosomes. Transactions of the Royal Society of Tropical Medicine and Hygiene 59, 489506.
MAY, R. M. ( 1977). Togetherness in schistosomes: its effects on the dynamics of infection. Mathematical Biosciences 35, 301343.
MEDLEY, G. F. ( 1992). Which comes first in host-parasite systems: density dependence or parasite distribution? Parasitology Today 8, 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. Parasitology 106, 211221.
MOLYNEUX, D. H. & ZAGARIA, N. ( 2002). Lymphatic filariasis elimination: progress in global programme development. Annals of Tropical Medicine and Parasitology 96, S15S40.
MURDOCH, W. W., BRIGGS, C. J. & NISBET, R. ( 2003). Consumer-Resource Dynamics. Monographs in Population Biology 36, Princeton University Press.
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 Infection 124, 529541.
MACEY, R. I. & OSTER, G. F. ( 2000). Berkeley Madonna. Version 8.0.1 for Windows. 1442-A Walnut Street #392-GO, Berkeley, CA 94709-1405, USA.
PATERSON, S. & VINEY, M. E. ( 2002). Host immune responses are necessary for density dependence in nematode infections. Parasitology 125, 283292.
PLAISIER, A. P., SUBRAMANIAN, S., DAS, P. K., SOUZA, W., LAPA, T., FURTADO, A. F., VAN DER PLOEG, C. P. B., HABBEMA, J. D. F., & VAN OORTMARSSEN, G. J. ( 1998). The LYMFASIM simulation program for modeling lymphatic filariasis and its control. Methods of Information in Medicine 37, 97108.
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 Biomedicine 31, 4356.
PLAISIER, A. P., VAN OORTMARSSEN, G. J., REMME, J., ALLEY, E. S. & HABBEMA, J. D. F. ( 1991). The risk and dynamics of onchocerciasis recrudescence after cessation of vector control. Bulletin of the World Health Organization 69, 169178.
PUGLIESE, A., ROSÀ, R. & DAMAGGIO, M. L. ( 1998). Analysis of a model for macroparasitic infection with variable aggregation and clumped infections. Journal of Mathematical Biology 36, 419447.
QUINNELL, R. J., GRAFEN, A. & WOOLHOUSE, M. E. J. ( 1995). Changes in parasite aggregation with age: a discrete infection model. Parasitology 111, 635644.
QUINNELL, R. J. ( 2003). Genetics of susceptibility to human helminth infection. International Journal for Parasitology 33, 12191231.
RICHARDS, F. O., BOATIN, B., SAUERBREY, M. & SÉKÉTÉLI, A. ( 2001). Control of onchocerciasis today: status and challenges. Trends in Parasitology 17, 558563.
ROBERTS, M.-G. ( 1995). A pocket guide to host-parasite models. Parasitology Today 11, 172177.
ROSÀ, R. & PUGLIESE, A. ( 2002). Aggregation, stability, and oscillations in different models for host-macroparasite interactions. Theoretical Population Biology 61, 319334.
ROSÀ, R., PUGLIESE, A., VILLANI, A. & RIZZOLI, A. ( 2003). Individual-based vs. deterministic models for macroparasites: host cycles and extinction. Theoretical Population Biology 63, 295307.
SCHULZ-KEY, H. & KARAM, M. ( 1986). Periodic reproduction of Onchocerca volvulus. Parasitology Today 10, 284286.
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 Parasitology 96, 1528.
SHAW, D. J., GRENFELL, B. T. & DOBSON, A. P. ( 1998). Patterns of macroparasite aggregation in wildlife host populations. Parasitology 117, 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 Entomology 41, 8394.
TALLIS, G. M. & LEYTON, M. ( 1966). A stochastic approach to the study of parasite populations. Journal of Theoretical Biology 13, 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. Parasitology 104, 247252.
WAKELIN, D. ( 1978). Immunity in intestinal parasites. Nature, London 43, 617620.
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 Hygiene 72, 675676.
WINNEN, M., PLAISIER, A. P., ALLEY, E. S., NAGELKERKE, N. J. D., VAN OORTMARSSEN, G., BOATIN, B. A. & HABBEMA, J. D. F. ( 2002). Can ivermectin mass treatments eliminate onchocerciasis in Africa? Bulletin of the World Health Organization 80, 384390.
WOOLHOUSE, M. E. J. ( 1992). A theoretical framework for the immunoepidemiology of helminth infection. Parasite Immunology 14, 563578.
WORLD HEALTH ORGANIZATION ( 1995). Onchocerciasis and its Control. WHO Technical Report Series. No. 852. WHO, Geneva.
WORLD HEALTH ORGANIZATION ( 1998). Guidelines for the Evaluation of Soil-Transmitted Helminthiasis and Schistosomiasis at the Community Level. WHO, Geneva.
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