Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-23T20:14:27.240Z Has data issue: false hasContentIssue false

Togetherness among Plasmodium falciparum gametocytes: interpretation through simulation and consequences for malaria transmission

Published online by Cambridge University Press:  17 October 2003

F.-O. GAILLARD
Affiliation:
Institut de Recherche pour le Développement (IRD), UR 79, Geodes, Bondy, France
C. BOUDIN
Affiliation:
IRD, UR 77, Paludisme afro-tropical; Laboratoire de Paludologie, B.P. 1386, Dakar, Senegal
N. P. CHAU
Affiliation:
Université Paris 7 and INSERM, U444, Paris, France
V. ROBERT
Affiliation:
IRD, UR 77, Paludisme afro-tropical; Groupe de Recherche sur le Paludisme, Institut Pasteur de Madagascar, B.P. 1274 Antananarivo, Madagascar
G. PICHON
Affiliation:
Institut de Recherche pour le Développement (IRD), UR 79, Geodes, Bondy, France

Abstract

Previous experimental gametocyte infections of Anopheles arabiensis on 3 volunteers naturally infected with Plasmodium falciparum were conducted in Senegal. They showed that gametocyte counts in the mosquitoes are, like macroparasite intakes, heterogeneous (overdispersed). They followed a negative binomial distribution, the overdispersion coefficient seeming constant (k=3·1). To try to explain this heterogeneity, we used an individual-based model (IBM), simulating the behaviour of gametocytes in the human blood circulation and their ingestion by mosquitoes. The hypothesis was that there exists a clustering of the gametocytes in the capillaries. From a series of simulations, in the case of clustering the following results were obtained: (i) the distribution of the gametocytes ingested by the mosquitoes followed a negative binomial, (ii) the k coefficient significantly increased with the density of circulating gametocytes. To validate this model result, 2 more experiments were conducted in Cameroon. Pooled experiments showed a distinct density dependency of the k-values. The simulation results and the experimental results were thus in agreement and suggested that an aggregation process at the microscopic level might produce the density-dependent overdispersion at the macroscopic level. Simulations also suggested that the clustering of gametocytes might facilitate fertilization of gametes.

Type
Research Article
Copyright
2003 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

AIKAWA, M. (1988). Human cerebral malaria. American Journal of Tropical Medicine and Hygiene 39, 310.CrossRefGoogle Scholar
ANDERSON, R. M. & MAY, R. M. (1985). Helminth infections of humans: mathematical models, population dynamics, and control. Advances in Parasitology 24, 1101.CrossRefGoogle Scholar
ANSCOMBE, F. J. (1950). Sampling theory of the negative binomial and logarithmic series distributions. Biometrika 37, 358.CrossRefGoogle Scholar
ANTOLISEI, E. & ANGELINI, A. (1890). Osservazioni sopra alcuni casi d'infezione malarica con forme semilunari. Rivista Clinica – Archivio italiano di Clinica Medica 29, 123.Google Scholar
BLISS, C. I. & FISHER, R. A. (1953). Fitting the negative binomial distribution to biological data, with a note on the efficient fitting. Biometrics 9, 176200.CrossRefGoogle Scholar
CARLSON, J., HELMBY, H., HILL, A. V. S., BREWSTER, D., GREENWOOD, B. M. & WAHLGREN, M. (1990). Human cerebral malaria: association with erythrocyte rosetting and lack of anti-rosetting antibodies. Lancet 336, 14571460.CrossRefGoogle Scholar
COHEN, J. E. (1971). Casual Groups of Monkeys and Men: Stochastic Models of Elemental Social Systems. Harvard University Press, Cambridge, Mass.CrossRef
CRANS, W. J. (1973). Experimental infection of Anopheles gambiae and Culex pipiens fatigans with Wuchereria bancrofti in coastal East Africa. Journal of Medical Entomology 10, 189193.CrossRefGoogle Scholar
CROFTON, H. D. (1971 a). A quantitative approach to parasitism. Parasitology 63, 343364.Google Scholar
CROFTON, H. D. (1971 b). A model of host–parasite relationships. Parasitology 63, 365371.Google Scholar
DeANGELIS, D. L., COX, D. C. & COUTANT, C. C. (1979). Cannibalism and size dispersal in young-of-the-year largemouth bass: experiments and model. Ecological Modelling 8, 133148.Google Scholar
DeANGELIS, D. L., ROSE, K. A. & HUSTON, M. A. (1994). Individual-oriented approaches to modelling ecological populations and communities. In Frontiers in Mathematical Biology (ed. Levin, S. A.), pp. 390410. Lecture Notes in Biomathematics 100, Springer Verlag, Berlin.
DIEBNER, H. H., EICHNER, M., MOLINEAUX, L., COLLINS, W. E., JEFFREY, G. M. & DIETZ, K. (2000). Modelling the transition of asexual blood stages of Plasmodium falciparum to gametocytes. Journal of Theoretical Biology 202, 113127.CrossRefGoogle Scholar
FERBER, J. (1995). Les Systèmes Multi-agents. Vers une Intelligence Collective. Inter-Editions, Paris.
GARNHAM, P. C. C. (1966). Malaria Parasites and other Haemosporidia. Blackwell Scientific Publications, Oxford.
GORDON, R. M. & LUMSDEN, W. H. R. (1939). A study of the behaviour of the mouth-parts of mosquitoes when taking up blood from living tissue; together with some observations on the ingestion of microfilariae. Annals of Tropical Medicine and Parasitology 46, 311319.CrossRefGoogle Scholar
MAY, R. M. (1977). Togetherness among schistosomes: its effect on the dynamics on the infection. Mathematical Bioscience 35, 301343.CrossRefGoogle Scholar
McPHERSON, G. G., WARRELL, M. J., WHITE, N. J., LOOAREESUWAN, S. & WARELL, D. A. (1985). Human cerebral malaria. A quantitative ultrastructural analysis of parasitized erythrocyte sequestration. American Journal of Pathology 119, 385401.Google Scholar
OKUBO, A. (1986). Dynamical aspects of animal grouping: swarms, schools, flocks, and herds. Advances in Biophysics 22, 194.CrossRefGoogle Scholar
PETIT, G. (1985). Ingestion des hématozoaires par le vecteur. Analyse de quatre filaires parasites d'un Saïmiri. Annales de Parasitologie Humaine et Comparée 60, 247297, 455497.CrossRefGoogle Scholar
PICHON, G., AWONO, P. & ROBERT, V. (2000). High heterogeneity in the number of Plasmodium falciparum gametocytes in the bloodmeal of mosquitoes fed on the same host. Parasitology 121, 115120.CrossRefGoogle Scholar
PICHON, G. & MULLON, C. (1991). Les distributions rencontrées en parasitologie; Introduction: la Filariose de Bancroft, prototype des relations hôte-parasites. In SEMINFOR 5 Statistique Impliquée (ed. ORSTOMed, Paris), pp. 289301.
PICHON, G. & MULLON, C. (1998). ParaDis version 2.1, software for statistical analysis of parasitic distributions. IRD-GEODES Downloadable Freeware:http://www.bondy.ird.fr/~pichon/paradis
PICHON, G., PROD'HON, J. & RIVIÈRE, F. (1980 a). Hétérogénéité de l'ingestion des parasites sanguicoles par leurs vecteurs: description quantitative et interprétation. Comptes Rendus de l'Académie des Sciences, Paris, série Biologie 18, 10111013.Google Scholar
PICHON, G., PROD'HON, J. & RIVIÈRE, F. (1980 b). Filarioses: surdispersion parasitaire et surinfection de l'hôte invertébré. Cahiers ORSTOM, Série Entomologie Médicale et Parasitologie 18, 2748.Google Scholar
PONGPONRATN, E., RIGANTI, M., PUNPOOWONG, B. & AIKAWA, M. (1991). Microvascular sequestration of parasitized erythrocytes in human falciparum malaria: a pathological study. American Journal of Tropical Medicine and Hygiene 44, 168175.CrossRefGoogle Scholar
READ, A. F., NARARA, A., NEE, S., KEYMER, A. E. & DAY, K. P. (1992). Gametocyte sex ratios as indirect measures of outcrossing rates in malaria. Parasitology 104, 387395.CrossRefGoogle Scholar
RINGWALD, P., LEPERS, J. P., LE BRAS, J., RAKOTOMALALA, C., RABONIRINA, M., VUILLEZ, J. P., RAZANAMPARANY, M., PEYRON, F. & ROUX, J. (1992). Parasite virulence factors during falciparum malaria: Rosetting, cytoadherence, and modulation of cytoadherence by cytokines. Infection and Immunity 61, 51985204.Google Scholar
ROBERT, V., READ, A., ESSONG, F., TCHUINKAM, T., MULDER, B., VERHAVE, J. P. & CARNEVALE, P. (1996). Effect of gametocytes sex ratio on infectivity of Plasmodium falciparum to Anopheles gambiae. Transactions of the Royal Society of Tropical Medicine and Hygiene 90, 621624.CrossRefGoogle Scholar
ROWE, A., OBEIRO, J., NEWBOLD, C. I. & MARSH, K. (1995). Plasmodium falciparum rosetting is associated with malaria severity in Kenya. Infection and Immunity 63, 23232326.Google Scholar
SINDEN, R. E. (1983). The cell biology of sexual development in Plasmodium. Parasitology 86, 728.CrossRefGoogle Scholar
SINDEN, R. E. (1984). The biology of Plasmodium in the mosquito. Experimentia 40, 13301343.CrossRefGoogle Scholar
SINDEN, R. E. (1989). Recent advances in the parasitology of malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene 83 (Suppl.), 39.CrossRefGoogle Scholar
TEMPLETON, J. T., KEISTER, D. B., MURATOVA, O., PROCTER, J. L. & KASLOW, D. C. (1998). Adherence of erythrocytes during exflagellation of Plasmodium falciparum microgametes is dependent on erythrocyte surface sialic acid and glycophorins. Journal of Experimental Medicine 187, 15991609.CrossRefGoogle Scholar
TREUTIGER, C. J., HEDLUND, I., HELMBY, H., CARLSON, J., JEPSON, A., TWUMASI, P., KWIATKOWSKI, D., GREENWOOD, B. M. & WAHLGREN, M. (1992). Rosette formation in Plasmodium falciparum isolates and anti-rosette activity of sera from Gambians with cerebral or uncomplicated malaria. American Journal of Tropical Medicine and Hygiene 46, 503510.CrossRefGoogle Scholar
TURNER, G. D. H., MORRISON, H., JONES, M., DAVIS, T. M. E., LOOAREESUWAN, S., BULEY, I. D., GATTER, K. C., NEWBOLD, C. I., PUKRITAYAKAMEE, S., NAGACHINTA, B., WHITE, N. J. & BERENDT, A. R. (1994). An immunohistochemical study of the pathology of fatal malaria. American Journal of Pathology 145, 10571069.Google Scholar
VAUGHAN, J. A., NODEN, B. H. & BEIER, J. C. (1991). Concentration of human erythrocytes by anopheline mosquitoes (Diptera: Culcidae) during feeding. Journal of Medical Entomology 28, 780786.CrossRefGoogle Scholar
WAHLGREN, M., FERNANDEZ, V., SCHOLANDER, C. & CARLSON, J. (1994). Rosetting. Parasitology Today 2, 7379.CrossRefGoogle Scholar
WEST, S. A., REECE, S. E. & READ, A. F. (2001). Evolution of gametocyte sex ratios in malaria and related apicomplexan (protozoan) parasites. Trends in Parasitology 17, 525531.CrossRefGoogle Scholar
WEST, S. A., SMITH, T. G., NEE, S. & READ, A. F. (2002). Fertility insurance and the sex ratios of malaria and related haemosporin blood parasites. Journal of Parasitology 88, 258263.CrossRefGoogle Scholar
WILLIAMS, C. B. (1964). Patterns in the Balance of Nature and Related Problems in Quantitative Ecology. Academic Press, London.