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Heterogeneity in patterns of malarial oocyst infections in the mosquito vector

  • G. F. Medley (a1), R. E. Sinden (a1), S. Fleck (a1), P. F. Billingsley (a1), N. Tirawanchap (a1) and M. H. Rodriguez (a2)...


Oocyst prevalence and intensity have been recorded in 349 laboratory infections of Anopheles stephensi with Plasmodium berghei. Intensity and prevalence of infection are shown to be predictably related. The structure and heterogeneity in the infections has been analysed with the objective of describing the biological mechanisms by which the observed negative binomial oocyst distributions are generated. The analysis has revealed that the most likely processes lie within the population dynamic events of malaria within the mosquito, namely gametogenesis, fertilization and mortality. The distribution is similar in all Plasmodium – mosquito combinations examined so far, whether they are of laboratory (P. gallinaceum in Aedes aegypti) or field (P. vivax in An. albimanus and P. falciparum in An. gambiae s.l. and An. funestus) origin. Further we conclude that there is competition between parasites in the vector. Oocyst frequency distribution analysis shows that under natural conditions of transmission intensity, and even under the best laboratory conditions, significant numbers (> 10%) of fully susceptible mosquitoes will not be infected under conditions where the mean infection is as high as 250 oocysts. Failure to infect is not therefore an absolute indicator of refractoriness. In assessing transmission data it is shown that sample sizes should not be less than 50, and ideally 100 mosquitoes, if reliable data are to be obtained. In the field it is suggested that difficulties in determining the low natural intensity of oocyst infections indicate that prevalence estimates are a useful and accessible parameter to measure. In determining the impact of transmission blocking mechanisms we predict that under conditions where high oocyst intensities prevail, large reductions in intensity will be required before a reduction in prevalence can be expected i.e. here it will be necessary to measure intensity of infection. Conversely, under conditions where low oocyst intensities prevail, a rapid reduction in prevalence will occur with little concurrent reduction in intensity i.e. prevalence determination will be the more sensitive estimate.



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Anderson, R. M. & Gordon, D. (1982). Processes influencing the distribution of parasite numbers with host populations with special emphasis on parasite-induced host mortalities. Parasitology 85, 373–98.
Barr, P. J., Green, K. M., Gibson, H. L., Bathurst, I. C., Quakyi, I. A. & Kaslow, D. c. (1991). Recombinant Pfs25 protein of Plasmodium falciparum elicits malaria transmission-blocking immunity in experimental animals. Journal of Experimental Medicine 174, 1203–8.
Billingsley, P. F. & Rudin, W. (1992). The role of the mosquito peritrophic membrane in bloodmeal digestion and infectivity of Plasmodium species. Journal of Parasitology 78, 430–40.
Cantrell, W. & Jordan, H. B. (1946). Changes in the infectiousness of gametocytes during the course of Plasmodium gallinaceum infections. Journal of Infectious Diseases 78, 153–9.
Collins, F. H., Sakai, R. K., Vernick, K. D., Paskewitz, S., Seeley, D. C., Miller, L. H., Collins, W. E., Campbell, C. C. & Gwadz, R.W. (1986). Genetic selection of a Plasmodium refractory strain of the malaria vector Anopheles gambiae. Science 234, 607–10.
Dearsly, A. L., Sinden, R. E. & Self, I. A. (1990). Sexual development in malarial parasites – gametocyte production, fertility and infectivity to the mosquito vector. Parasitology 100, 359–68.
Elliot, J. M. (1977). Statistical Analysis of Samples of Benthic Invertebrates. 2nd Edn.Freshwater Biological Association, Scientific Publication.
Eyles, D. E. (1951). Studies on Plasmodium gallinaceum I. Characteristics of the infection in the mosquito, Aedes aegypti. American Journal of Hygiene 54, 101–12.
Eyles, D. E. (1952 a). Studies on Plasmodium gallinaceum II. Factors in the blood of the vertebrate host influencing mosquito infection. American Journal of Hygiene 55, 276–90.
Eyles, D. E. (1952 b). Studies on Plasmodium gallinaceum IV. A comparison of the susceptibility of Aedes aegypti, Anopheles quadrimaculatus and Anopheles freeborni. American Journal of Hygiene 56, 71–7.
Eyles, D. E. (1952 c). Studies on Plasmodium gallinaceum. III Factors associated with the malaria infection in the vertebrate host which influence the degree of infection in the mosquito. American Journal of Tropical Medicine and Hygiene 55, 386–91.
Feldmann, A. M. & Ponnudurai, T. (1989). Selection of Anopheles stephensi for refractoriness and susceptibility to Plasmodium falciparum. Medical and Veterinary Entomology 3, 4152.
Gamagemendis, A. C., Rajakaruna, J., Carter, R. & Mendis, K. N. (1991). Infectious reservoir of Plasmodium vivax and Plasmodium falciparum malaria in an endemic region of Sri Lanka. American Journal of Tropical Medicine and Hygiene 45, 479–87.
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.
Huff, C. G. (1927). Studies on the infectivity of Plasmodia of birds for mosquitoes, with special reference to the problem of immunity in the mosquito. American Journal of Hygiene 7, 706–34.
Ichimori, K., Curtis, C. F. & Targett, G. A. T. (1990). The effects of chloroquine on the infectivity of chloroquine-sensitive and -resistant populations of Plasmodium yoelii nigeriensis to mosquitoes. Parasitology 100, 377–81.
Maier, w. (1987). Pathology of malaria infected mosquitoes. Parasitology Today 3, 216–18.
Muirhead-Thomson, R. C. (1954). Factors determining the true reservoir of infection of Plasmodium falciparum and Wuchereria bancrofti in a West African village. Transactions of the Royal Society of Tropical Medicine and Hygiene 48, 208–25.
Nelder, J. A. & Mead, R. (1965). A Simplex method of function minimisation. Computer Journal 7, 308–13.
Pacala, S. & Dobson, A. P. (1988). The relation between the number of parasites/host and host age: population dynamic causes and maximum likelihood estimation. Parasitology 96, 197210.
Ponnudurai, T., Lensen, A. H. W., Vangemert, G. J. A., Bolmer, M. G. & Meuwissen, J. H. E. T. (1991). Feeding behaviour and sporozoite ejection by infected Anopheles stephensi. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 175–80.
Robert, V., Verhave, J. P. & Carnevale, P. (1990). Plasmodium falciparum infection does not increase the precocious mortality rate of Anopheles gambiae. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 346–7.
Rosenberg, R., Koontz, L. C. & Carter, R. (1982). Infection of Aedes aegypti with zygotes of Plasmodium gallinaceum fertilized in vitro. Journal of Parasitology 68, 653–6.
Rosenberg, R. & Rungsiwongse, J. (1991). The number of sporozoites produced by individual malaria oocysts. American Journal of Tropical Medicine and Hygiene 45, 574–7.
Sieber, K-P., Huber, M., Kaslow, D., Banks, S. M., Toril, M., Aikawa, M. & Miller, L. H. (1991). The peritrophic membrane as a barrier: its penetration by Plasmodium gallinaceum and the effect of a monoclonal antibody to ookinetes. Experimental Parasitology 72, 145–56.
Tirawanchai, N., Winger, L. A., Nicholas, J. & Sinden, R. E. (1991). Analysis of immunity induced by the affinity-purified 21-kilodalton zygote-ookinete surface antigen of Plasmodium berghei. Infection and Immunity 59, 3644.
Vaughan, J. A., Narum, D. & Azad, A. F. (1991). Plasmodium berghei ookinete densities in 3 anopheline species. Journal of Parasitology 77, 758–61.
Vaughan, J. A., Noden, B. H. & Beier, J. C. (1992). Population dynamics of Plasmodium falciparum sporogony in laboratory-infected Anopheles gambiae. Journal of Parasitology 78, 716–24.


Heterogeneity in patterns of malarial oocyst infections in the mosquito vector

  • G. F. Medley (a1), R. E. Sinden (a1), S. Fleck (a1), P. F. Billingsley (a1), N. Tirawanchap (a1) and M. H. Rodriguez (a2)...


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