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Density-dependent processes in the transmission of human onchocerciasis: intensity of microfilariae in the skin and their uptake by the simuliid host

Published online by Cambridge University Press:  06 April 2009

M. G. Basáñez ,
M. Boussinesq ,
J. Prod'hon ,
H. Frontado ,
N. J. Villamizar ,
G. F. Medley  and
R. M. Anderson
M. G. Basáñez
Affiliation:
Instituto de Medicina Tropical, Universidad Central de Venezuela, Caracas, Venezuela Department of Biology, Parasite Epidemiology Research Group, Imperial College, Prince Consort Road, London SW7 2BB, UK
M. Boussinesq
Affiliation:
Antenne ORSTOM auprés du Centre Pasteur, BP 1274, Yaoundé, Cameroon
J. Prod'hon
Affiliation:
Antenne ORSTOM auprés du Centre Pasteur, BP 1274, Yaoundé, Cameroon
H. Frontado
Affiliation:
Centro Amazónico de Investigación y Control de Enfermedades Tropicales (CAICET), Puerto Ayacucho, Amazonas, Venezuela.
N. J. Villamizar
Affiliation:
Centro Amazónico de Investigación y Control de Enfermedades Tropicales (CAICET), Puerto Ayacucho, Amazonas, Venezuela.
G. F. Medley
Affiliation:
Department of Biology, Parasite Epidemiology Research Group, Imperial College, Prince Consort Road, London SW7 2BB, UK
R. M. Anderson
Affiliation:
Department of Biology, Parasite Epidemiology Research Group, Imperial College, Prince Consort Road, London SW7 2BB, UK
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Summary

The transmission success of Onchocerca volvulus is thought to be influenced by a variety of regulatory or density-dependent processes that act at various points in the two-host life-cycle. This paper examines one component of the life-cycle, namely, the ingestion of microfilariae by the simuliid vector, to assess the relationship between intake of larvae and the density of parasites in the skin of the human host. Analysis is based on data from three areas in which onchocerciasis is endemic and includes published information as well as new data collected in field studies. The three areas are: Guatemala (Simulium ochraceum sl.), West and Central Africa (savanna members of the S. damnosum complex), and South Venezuela (S. guianense). The data record experimental studies of parasite uptake by flies captured in the field and fed to repletion on locally infected subjects who harboured varying intensities of dermal microfilarial infection. Regression analyses of log transformed counts of parasite burdens ingested by the flies plotted against log transformed counts of microfilariae per mg of skin revealed little evidence for saturation in parasite uptake by the flies as the intensity in the human host increased. There was a positive and highly significant rank correlation between both variables for the three blackfly species. In an alternative analysis a model was fitted to data on prevalence of flies with ingested microfilariae (mff) versus dermal mean intensities. The model assumed an overdispersed distribution of the number of mff/fly and a given functional relationship between intake and skin load. The results of both approaches were consistent. It is concluded that parasite ingestiossssn by the vector host is not strongly density dependent in the three geographical areas and ranges of dermal loads examined. It therefore appears that this transmission process is of reduced importance as a regulatory mechanism in the dynamics of parasite population growth.

Keywords

Onchocerca volvulussimuliid hostsmicrofilarial intakemicrofilarial concentrationdensity dependence
Type
Research Article
Information
Parasitology , Volume 108 , Issue 1 , January 1994 , pp. 115 - 127
Copyright
Copyright © Cambridge University Press 1994

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References

REFERENCES

Anderson, R. M. (1982 a). The population dynamics and control of hookworm and roundworm infections. In Population Dynamics of Infectious Diseases (ed. Anderson, R. M.), pp. 67–108. London: Chapman and Hall.Google Scholar
Anderson, R. M. (1982 b). Epidemiology. In Modern Parasitology (ed. Cox, F. E. G.), pp. 204–51. Oxford: Blackwell Scientific Publications.Google Scholar
Anderson, R. M. (1987). Determinants of infection in human schistosomiasis. In Bailliére's Clinical Tropical Medicine and Communicable Diseases, Vol. 2, No. 2, (ed. Mahmoud, A. F.), 2nd Edn, pp. 279–300. London: Bailliére Tindall.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.Google Scholar
Anderson, R. M., Gordon, D. M., Crawley, M. J. & Hasell, M. P. (1982). Variability in the abundance of animal and plant species. Nature, London 296, 245–8.Google Scholar
Anderson, R. M. & May, R. M. (1985). Helminth infections of humans: mathematical models, population dynamics, and control. Advances in Parasitology 24, 1–101.Google Scholar
Anderson, R. M. & May, R. M. (1991). Infectious Diseases of Humans. Oxford: Oxford University Press.CrossRefGoogle Scholar
Armitage, P. & Berry, G. (1987). Statistical Methods in Medical Research, 2nd edn.Oxford: Blackwell Scientific Publications.Google Scholar
Bailey, N. T. J. (1981). Statistical Methods in Biology, 2nd edn.London: Hodder and Stoughton.Google Scholar
Bain, O., Vuong, P., Petit, G., Prod'hon, J., Ranque, P. & Chabaud, A. G. (1986). Différences dans la localisation des microfilaires d'O. volvulus en savane et en forêt: Implications cliniques éventuelles. Annates de Parasitologic Humaine et Comparée 61, 125–6.Google Scholar
Basáñez, M. G. & Yarzábal, L. (1988). Onchocerciasis in the Sierra Parima and Upper Orinoco regions, Federal Territory of Amazonas, Venezuela. In Parasitic Diseases: Treatment and Control (ed. Miller, M. J. & Love, E. J.), pp. 231–56. Boca Raton, FL: CRC Press.Google Scholar
Basáñez, M. G., Yarz´bal, L., Takaoka, H., Suzuki, H., Noda, S. & Tada, I. (1988). The vectorial role of several blackfly species (Diptera: Simuliidae) in relation to human onchocerciasis in the Sierra Parima and Upper Orinoco regions of Venezuela. Annals of Tropical Medicine and Parasitology 82, 597–611.Google Scholar
Billingsley, P. F., Medley, G. F., Charlwood, J. D. & Sinden, R. E. (1994). Relationship between prevalence and intensity of Plasmodium falciparum infection in natural populations of Anopheles mosquitoes. American Journal of Tropical Medicine and Hygiene (in the Press).CrossRefGoogle ScholarPubMed
Boussinesq, M. (1991). Etude épidémiologique de I'onchocercose en zone de savane camerounaise. Effets d'un traitement de masse par l'ivermectine. Ph.D. thesis. University of Montpellier II.Google Scholar
Bryan, J. H. & Southgate, B. A. (1988). Factors affecting transmission of Wuchereria bancrofti by anopheline mosquitoes. 1. Uptake of microfilariae. Transactions of the Royal Society of Tropical Medicine and Hygiene 82, 128–37.Google Scholar
Campbell, C. C., Collins, R. C., Huong, A. Y. & Figueroa Marroquin, H. (1980). Quantitative aspects of the infection of Simulium ochraceum by Onchocerca volvulus: the relation of skin microfilarial density to vector infection. Tropenmedizin und Parasitologie 31, 475–8.Google ScholarPubMed
Cohen, J. E. (1976). Schistosomiasis: a human-host parasite system. In Theoretical Ecology (ed. May, R. M.), pp. 237–56. Oxford: Blackwell Scientific Publications.Google Scholar
Collins, R. C., Campbell, C. C., Wilton, D. P. & Newton, L. (1977). Quantitative aspects of the infection of Simulium ochraceum by Onchocerca volvulus. Tropenmedizin und Parasitologie 28, 235–43.Google Scholar
Collins, R. C., Brandling-Bennett, A. D., Hollman, R. B., Campbell, C. C. & Darsie, R. F. (1980). Parasitological diagnosis of onchocerciasis: comparison of incubation media and incubation times for skin snips. American Journal of Tropical Medicine and Hygiene 29, 35–41.Google Scholar
Cox, D. R. & Hinkley, D. V. (1974). Theoretical Statistics. London: Chapman and Hall.CrossRefGoogle Scholar
Cox, D. R. & Oakes, D. (1984). Analysis of Survival Data. London: Chapman and Hall.Google Scholar
Crosskey, R. W. (1990). The Natural History of Blackflies. Chichester: John Wiley & Sons.Google Scholar
Cupp, E. W. (1992). Treatment of onchocerciasis with Ivermectin in Central America. Parasitology Today 8, 212–14.Google Scholar
Dalmat, H. T. (1955). The Blackflies (Diptera, Simuliidae) of Guatemala and their Role as Vectors of Onchocerciasis. Smithsonian Miscellaneous Collection 125. Washington: Smithsonian Institute.Google Scholar
Davies, J. B., Weidhaas, D. E. & Haile, D. G. (1987). Models as aids to understanding onchocerciasis. In Black-flies: Ecology, Population Management and Annotated World List (ed. Kim, K. C. & Merrit, R. W.), pp. 396–407. University Park and London: The Pennsylvania State University.Google Scholar
De León, N. J. & Duke, B. O. L. (1966). Experimental studies on the transmission of Guatemalan and West African strains of Onchocerca volvulus by Simulium ochraceum, S. metallicum and S. callidum. Transactions of the Royal Society of Tropical Medicine and Hygiene 60, 735–52.Google Scholar
Dietz, K. (1982). The population dynamics of onchocerciasis. In Population Dynamics of Infectious Diseases (ed. Anderson, R. M.), pp. 209–41. London: Chapman and Hall.CrossRefGoogle Scholar
Duke, B. O. L. (1962 a). Studies on factors influencing the transmission of onchocerciasis. I. The survival rate of Simulium damnosum under laboratory conditions and the effect upon it of Onchocerca volvulus. Annals of Tropical Medicine and Parasitology 56, 130–5.Google Scholar
Duke, B. O. L. (1962 b). Studies on factors influencing the transmission of onchocerciasis. II. The intake of Onchocerca volvulus microfilariae by Simulium damnosum and the survival of the parasites in the fly under laboratory conditions. Annals of Tropical Medicine and Parasitology 56, 255–63.Google Scholar
Elliot, J. M. (1977). Some Methods for the Statistical Analysis of Samples of Benthic Invertebrates, 2nd edn. Freshwater Biological Association, Sci. Publ. No. 25. Cumbria: Titus Wilson & Son Ltd.Google Scholar
Grenfell, B. T. & Michael, E. (1992). Infection and disease in lymphatic filariasis: an epidemiological approach. Parasitology 104, S81–S90.Google Scholar
Guderian, R. H., Beck, B. J., Stone, D. J., Isabel, K. & Mackenzie, C. D. (1988). Onchocerciasis in Ecuador: recent observations in the province of Esmeraldas. Journal of Tropical Medicine and Hygiene 91, 161–8.Google Scholar
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, 139–43.Google Scholar
Hairston, N. G. & Jachowski, L. A. (1968). Analysis of the Wuchereria bancrofti population in the people of American Samoa. Bulletin of the World Health Organization 38, 29–59.Google Scholar
Kershaw, W. E. (1958). The population dynamics of infection with Onchocerca volvulus in the vector Simulium damnosum. Proceedings of the Xth International Congress of Entomology, Montreal, 1956 3, 499–501.Google Scholar
Kershaw, W. E., Duke, B. O. L. & Budden, F. H. (1954). Distribution of microfilariae of O. volvulus in the skin. Its relation to the skin changes and to eye lesions and blindness. British Medical Journal 2, 724–9.Google Scholar
Kershaw, W. E., Jamison, D. G., Nugent, D. & Duke, B. O. L. (1956). Preliminary observations on the depth distribution of the microfilariae of Onchocerca volvulus in the skin and its relation to the reservoir of infection to the fly. Transactions of the Royal Society of Tropical Medicine and Hygiene 50, 6.Google Scholar
Lwambo, N. J. S., Bundy, D. A. P. & Medley, G. F. H. (1992). A new approach to morbidity risk assessment in hookworm endemic communities. Epidemiology and Infection 108, 469–81.CrossRefGoogle ScholarPubMed
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.Google Scholar
Medley, G. F., Sinden, R. E., Fleck, S., Billingsley, P. F., Tirawanchai, N. & Rodriguez, M. H. (1993). Heterogeneity in patterns of malarial oocyst infections in the mosquito vector. Parasitology 106, 441–9.Google Scholar
Nelson, G. S. (1991). Human onchocerciasis: notes on the history, the parasite and the life cycle. Annals of Tropical Medicine and Parasitology 85, 83–95.Google Scholar
Omar, M. S. & Garms, R. (1975). The fate and migration of microfilariae of a Guatemalan strain of Onchocerca volvulus in Simulium ochraceum and S. metallicum, and the role of the buccopharyngeal armature in the destruction of microfilariae. Tropenmedizin und Parasitologie 26, 183–90.Google Scholar
Omar, M. S. & Garms, R. (1977). Lethal damage to Simulium metallicum following high intakes of Onchocerca volvulus microfilariae in Guatemala. Tropenmedizin und Parasitologie 26, 169–82.Google Scholar
Philippon, B. (1977). Etude de la transmission d'Onchocerca volvulus (Leuckart, 1893) (Nematoda, Onchocercidae) par Simulium damnosum Theobald, 1903 (Diptera, Simuliidae) en Afrique tropicale. Travaux et Documents de l’ORSTOM, (Paris) No. 63.Google Scholar
Philippon, B. & Bain, O. (1972). Transmission de l'onchocercose humaine en zone de savane d’Afrique Occidentale, passage des microfilaires d'Onchocerca volvulus Leuck. dans l'hémocèle de la femelle de Simulium damnosum Th. Cahiers O.R.S.T.O.M., série Entomologie medicale et Parasitologie 10, 251–61.Google Scholar
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, 43–56.Google Scholar
Plaisier, A. P., van Oortmarssen, G. J., Remme, J. & Habbema, J. D. F. (1991 a). The reproductive lifespan of Onchocerca volvulus in West African savana. Acta Tropica 48, 271–84.Google Scholar
Plaisier, A. P., van Oortmarssen, G. J., Remme, J., Alley, E. S. & Habbema, J. D. F. (1991 b). The risk and dynamics of onchocerciasis recrudescence after cessation of vector control. Bulletin of the World Health Organization 69, 169–78.Google Scholar
Prod'hon, J., Hebrard, G., Prud'hom, J. M. & Couret, D. (1986). Action de l'ivermectine (MK-933) sur la transmission de l'onchocercose humaine par le groupe vecteur Simulium soubrense–Simulium sanctipauli en zone forestiere de Côte d’Ivoire. Résultats immédiatement et six mois après traitement. Rapport OCCGE/ORSTOM non publié No. 03/IPR/Rap/86.Google Scholar
Prod'hon, J., Lardeaux, F., Bain, O., Hebrard, G. & Prud'hom, J. M. (1987). Ivermectine et modalites de la reduction de l'infection des simulies dans un foyer forestier d'onchocercose humaine. Annales de Parasitologie Humaine et Comparée 62, 590–8.Google Scholar
Prost, A. & Prod'hon, J. (1978). Le diagnostique de l'onchocercose. Revue critique des méthodes en usage. Médecine Tropical 38, 519–32.Google Scholar
Remme, J., Ba, O., Dadzie, K. Y. & Karam, M. (1986). A force-of-infection model for onchocerciasis and its applications in the epidemiological evaluation of the Onchocerciasis Control Programme in the Volta river basin area. Bulletin of the World Health Organization 64, 667–81.Google Scholar
Rochet, M. -J. (1990). A simple deterministic model for bancroftian filariasis transmission dynamics. Tropical Medicine and Parasitology 41, 225–33.Google Scholar
Rosewell, J., Shorrocks, B. & Edwards, K. (1990). Competition on a divided and ephemeral resource: testing the assumptions. I. Aggregation. Journal of Animal Ecology 59, 977–1001.Google Scholar
Schlotzhauer, S. D. & Litell, R. C. (1987). SAS System for Elementary Statistical Analysis. Cary, NC: SAS Institute Inc.Google Scholar
Shelley, A. J. (1988). Biosystematics and medical importance of the Simulium amazonicum group and the S. exiguum complex in Latin America. In Biosystematics of Haematophagous Insects (ed. Service, M. W.), pp. 203–20. The Systematics Association. Special Volume No. 37. Oxford: Clarendon Press.Google Scholar
Shelley, A. J. (1991). Simuliidae and the transmission and control of human onchocerciasis in Latin America. Cadernos de Saûde Pública 7, 310–27.CrossRefGoogle ScholarPubMed
Shelley, A. J., Finger, R. R., Moraes, M. A. P. & Hayes, J. (1979). Concentration of microfilariae of Onchocerca volvulus by Simulium sanguineum during feeding: use in mapping parasite distribution in the skin. Journal of Medical Entomology 16, 48–51.Google Scholar
Shelley, A. J., Luna Dias, A. P. A., Moraes, M. A. P. & Procunier, W. S. (1987). The status of Simulium oyapockense and S. limbatum as vectors of human onchocerciasis in Brazilian Amazonia. Medical and Veterinary Entomology 1, 219–34.Google Scholar
Sokal, R. R. & Rohlf, F. J. (1981). Biometry. The Principles and Practice of Statistics in Biological Research. New York: W. H. Freeman and Company.Google Scholar
Takaoka, H., Suzuki, H., Noda, S., Tada, I., Basáñez, M. G. & Yarzábal, L. (1984). Development of Onchocerca volvulus larvae in Simulium pintoi in the Amazonas region of Venezuela. American Journal of Tropical Medicine and Hygiene 33, 414–19.Google Scholar
Taylor, H. R., Keyvan-Larijanl, E., Newland, H. S., White, A. T. & Greene, B. M. (1987). Sensitivity of skin snips in the diagnosis of onchocerciasis. Tropical Medicine and Parasitology 38, 145–7.Google Scholar
Taylor, H. R., Munoz, B., Keyvan-Larijanl, E. & Greene, B. M. (1989). Reliability of detection of microfilariae in skin snips in the diagnosis of onchocerciasis. American Journal of Tropical Medicine and Hygiene 41, 467–71.Google Scholar
Vajime, C. G. & Dunbar, R. W. (1975). Chromosomal identification of eight species of the subgenus Edwardsellum near and including Simulium (Edwardsellum) damnosum Theobald (Diptera: Simuliidae). Tropenmedizin und Parasitologie 26, 111–38.Google Scholar
Vuong, P., Bain, O., Cabaret, J., Petit, G., Prod'hon, J., Ranque, P. & Chabaud, A. G. (1988). Forcst and savanna onchocerciasis: comparative morphometric histopathology of skin lesions. Tropical Medicine and Parasitology 39, 105–10.Google Scholar
Wada, Y. (1982). Theoretical approach to the epidemiology of onchocerciasis in Guatemala. Japanese Journal of Medical Science and Biology 35, 183–96.Google Scholar
Wenk, P. (1981). Bionomics of adult blackflies. In Blackflies: The Future for Biological Methods in Integrated Control (ed. Laird, M.), pp. 215–27. London: Academic Press.Google Scholar
Wenk, P. (1991). The vector host link in filariasis. Annals of Tropical Medicine and Parasitology 85, 139–47.Google Scholar
World Health Organization (1985). Ten years of onchocerciasis control in West Africa. WHO Document No. OCP/GVA/85·1B.Google Scholar
World Health Organization (1987). WHO Expert Committee on Onchocerciasis. WHO Technical Report Series No. 752. Geneva.Google Scholar
Williams, C. B. (1937). The use of logarithms in the interpretation of certain entomological problems. Annals of Applied Biology 24, 404–14.Google Scholar
Yarzábal, L., Botto, C., Arango, M., Raga, L. M., Wong, F., Allan, R., Jaimes, J. L. & Sanchez-Beaujon, R. (1985). Epidemiological aspects of onchocerciasis in the Sierra Parima, Federal Territory of Amazonas, Venezuela. In La Oncocercosis en América (ed. Yarzabal, L., Botto, C. & Allan, R.), pp. 43–63. Caracas: Ediciones PROICET-Amazonas.Google Scholar