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Human malaria infectiousness measured by age-specific sporozoite rates in Anopheles gambiae in Tanzania

Published online by Cambridge University Press:  06 April 2009

J. D. Lines ,
T. J. Wilkes  and
E. O. Lyimo
J. D. Lines
Affiliation:
Amani Research Centre, N.I.M.R., P.O. Box 4, Amani, Tanzania and London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, UK
T. J. Wilkes
Affiliation:
Amani Research Centre, N.I.M.R., P.O. Box 4, Amani, Tanzania and London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, UK
E. O. Lyimo
Affiliation:
Amani Research Centre, N.I.M.R., P.O. Box 4, Amani, Tanzania and London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, UK
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Summary

In an area of holoendemic malaria in Northern Tanzania, Anopheles gambiae s.l. females were age-graded by Polovodova's method and dissected for sporozoites. Age-specific sporozoite rates implied that mosquitoes acquired new infections at all ages. The extrinsic period lasted just over 3 gonotrophic cycles (9–11 days). Very high sporozoite rates in the oldest females implied the absence or rarity of genetic refractoriness to infection. A method is described for estimating the proportion of bloodmeals which result in mosquito infection. This method makes relatively few assumptions about mosquito behaviour, and could be useful for evaluating transmission-blocking interventions. Overall, it is estimated that about 21% of meals are infectious. This is much higher than previous estimates derived either from experimental mosquito feeding studies or from similar age-grading data collected from the same area in 1962. Various alternative explanations are considered, and it is concluded that there has been a 2.5-fold increase in human infectiousness in the last 25 years. This is partly attributable to suppression of human infectiousness by widespread chloroquine usage during the 1960s, followed by removal of this effect by drug resistance. It is argued that chloroquine would be expected to select for increased infectivity in the parasite, and this may also have contributed to the observed increase.

Keywords

malariasporozoitesgametocytesAnopheles gambiaeage-gradingchloroquine
Type
Research Article
Information
Parasitology , Volume 102 , Issue 2 , April 1991 , pp. 167 - 177
Copyright
Copyright © Cambridge University Press 1991

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References

REFERENCES

Boreham, P. F. L., Chandler, J. A. & Jolly, J. (1978). The incidence of mosquitoes feeding on mothers and babies at Kisumu, Kenya. Journal of Tropical Medicine and Hygiene 81, 63–7.Google ScholarPubMed
Burkot, T. R., Narara, A., Paru, R., Graves, P. M. & Garner, P. (1989). Human host selection by anophelines: no evidence for preferential selection of malaria or microfilariae-infected individuals in a hyperendemic area. Parasitology 98, 337–42.Google Scholar
Carnevale, P., FrÉzil, J. L., Bosseno, M. F., Le Pont, F. & Lancien, J. (1978). Étude de l'agressivité d'Anopheles gambiae A en fonction de l'âge et du sexe des sujets humains. Bulletin of the World Health Organization 56, 147–54.Google Scholar
Carnevale, P. & Le Pont, F. (1973). Épidémiologie du paludisme humain en République populaire du Congo. II. Utilisation des pièges lumineux ‘CDC’ comme moyen d'échantillonage des populations anophéliennes. Cahiers de l'ORSTOM, Série Entomologie Médicale et Parasitologie 11, 263–70.Google Scholar
Carter, R. & Graves, P. M. (1988). Gametocytes. In Malaria–Principles and Practice of Malariology (ed. Wernsdorfer, W. H. & McGregor, I.), pp. 253–305. Edinburgh: Churchill Livingstone.Google Scholar
Carter, R. & Gwadz, R. W. (1980). Infectiousness and gamete immunisation in malaria. In Malaria, vol. 3, Immunology and Immunisation (ed. Kreier, J. P.), pp. 263–98. New York: Academic Press.Google Scholar
Charlwood, J. D., Birley, M. H., Dagoro, H., Paru, R. & Holmes, P. R. (1985). Assessing survival rates of Anopheles farauti (Diptera: Culicidae) from Papua New Guinea. Journal of Animal Ecology 54, 1003–16.CrossRefGoogle Scholar
Clements, A. N. & Paterson, G. D. (1981). The analysis of mortality and survival rates in wild populations of mosquitoes. Journal of Applied Ecology 18, 373–99.CrossRefGoogle Scholar
Clyde, D. F. (1967). Malaria in Tanzania. London: Oxford University Press.Google Scholar
Clyde, D. F. & Shute, G. T. (1958). Selective feeding habits of anophelines amongst Africans of different ages. American Journal of Tropical Medicine and Hygiene 7, 543–5.CrossRefGoogle ScholarPubMed
Davidson, G. & Draper, C. C. (1953). Field studies of the basic factors in the transmission of malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene 47, 522–35.CrossRefGoogle ScholarPubMed
Day, J. F. & Edman, J. D. (1983). Malaria renders mice susceptible to mosquito feeding when gametocytes are most infective. Journal of Parasitology 69, 163–70.CrossRefGoogle ScholarPubMed
Draper, C. C. (1953). Observations on the infectiousness of gametocytes in hyperendemic malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene 47, 160–5.CrossRefGoogle ScholarPubMed
Garnham, P. C. C. (1957). Microsporidia in laboratory colonies of Anopheles. Bulletin of the World Health Organization 15, 845–7.Google Scholar
Garrett-JONES, C. & Magayuka, S. A. (1975). Studies on the natural incidence of Plasmodium and Wuchereria infections in Anopheles in rural East Africa. I. Assessment of densities by trapping hungry female Anopheles gambiae Giles Species A. Mimeographed document WHO/MAL/75.851, WHO/VBC/75.541. Geneva: World Health Organization.Google Scholar
Gillies, M. T. (1954 a). Studies in house-leaving and outside resting of Anopheles gambiae and Anopheles funestus in East Africa. I. The outdoor-resting population. Bulletin of Entomological Research 45, 361–73.Google Scholar
Gillies, M. T. (1954 b). Studies in house-leaving and outside resting of Anopheles gambiae and Anopheles funestus in East Africa. II. The exodus from houses and the house-resting population. Bulletin of Entomological Research 45, 375–87.CrossRefGoogle Scholar
Gillies, M. T. (1988). Anopheline mosquitoes: vector behaviour and bionomics. In Malaria: Principles and Practice of Malariology, vol. 2 (ed. Wernsdorfer, W. H. & McGregor, I.), pp. 453–86. Edinburgh: Churchill Livingstone.Google Scholar
Gillies, M. T. & De Meillon, B. (1968). The Anophelinae of Africa South of the Sahara, 2nd edn. Publication No. 54. Johannesburg: South African Institute for Medical Research.Google Scholar
Gillies, M. T. & Wilkes, T. J. (1965). A study of the age-composition of populations of A. gambiae Giles and A. funestus Giles in North-Eastern Tanzania. Bulletin of Entomological Research 56, 237–62.CrossRefGoogle Scholar
Graves, P. M., Burkot, T. R., Carter, R., Cattani, J. A., Lagog, M., Parker, J., Brabin, B. J., Gibson, F. D., Bradley, D. J. & Alpers, M. (1988). Measurement of malarial infectivity of human populations to mosquitoes in the Madang area, Papua New Guinea. Parasitology 96, 251–63.CrossRefGoogle ScholarPubMed
Graves, P. M., Burkot, T. R., Saul, A. J., Hayes, R. J. & Carter, R. (1990). Estimation of anopheline survival rate, vectorial capacity, and mosquito infection probability from malaria vector infection rates in villages near Madang, Papua New Guinea. Journal of Applied Ecology 27, 134–7.CrossRefGoogle Scholar
Graves, P. M., Carter, R. & McNeill, K. M. (1984). Gametocyte production in cloned lines of Plasmodium falciparum. American Journal of Tropical Medicine and Hygiene 33, 1045–50.CrossRefGoogle ScholarPubMed
Ichimori, K. (1987). Studies on transmission of chloroquine resistant and sensitive populations of Plasmodium yoelli nigeriensis by Anopheles stephensi. Ph.D. thesis, University of London.Google Scholar
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 yoelli nigeriensis to mosquitoes. Parasitology 100, 377–81.CrossRefGoogle ScholarPubMed
Klein, T. A., Harrison, B. A., Grove, J. S., Dixon, S. V. & AndrÉ, R. G. (1986). Correlation of survival rates of Anopheles dirus A (Diptera: Culicidae) with different infection densities of Plasmodium cynomolgi. Bulletin of the World Health Organization 64, 901–7.Google ScholarPubMed
Koella, J. C., Mshinda, H., Teuscher, T., Sublet, A., Betschart, B. & Tanner, M. (1990). Patterns of chloroquine usage. Abstracts of the VIIth International Congress of Parasitology, in Bulletin de la Société Française de la Parasitologie 8 (supplément no. 1), 460.Google Scholar
Lyimo, E. O., Nicholson, E., Lines, J. & Msuya, A. (1988). Measuring the effect of community-wide use of permethrin treated bednets on malaria in Tanzania. Abstracts of the XIIth International Congress for Tropical Medicine and Malaria, 18–23 Sept. 1988, Amsterdam (ed. Kager, P. A. & Polderman, A. M.). Amsterdam: Excerpta Medica.Google Scholar
Macdonald, G. (1952). The analysis of the sporozoite rate. Tropical Disease Bulletin 49, 569–85.Google Scholar
Mnzava, A. E. P. & Kilama, W. L. (1986). Observations on the distribution of the Anopheles gambiae complex in Tanzania. Acta Tropica 43, 277–82.Google ScholarPubMed
Muench, H. (1959). Catalytic Models in Epidemiology. Cambridge, Ma: Harvard University Press.Google Scholar
Muirhead-THOMSON, R. C. (1951). The distribution of anopheline mosquito bites among different age groups, a new factor in malaria epidemiology. British Medical Journal 1, 1114–17.Google Scholar
Muirhead-THOMSON, R. C. (1957). The malarial infectivity of an African village population to mosquitoes (Anopheles gambiae): a random xenodiagnostic survey. American Journal of Tropical Medicine and Hygiene 6, 971–9.Google Scholar
Nasci, R. S. (1986). The size of emerging and host-seeking Aedes aegypti and the relation of size to blood-feeding success in the field. Journal of the American Mosquito Control Association 2, 61–2.Google Scholar
Nasci, R. S. (1987). Adult body size and parity in field populations of the mosquitoes Anopheles crucians, Aedes taeniorhynchus, and Aedes sollicitans. Journal of the American Mosquito Control Association 3, 636–7.Google ScholarPubMed
Otieno, L. H., Lelijveld, J., Meuwissen, J. H. E. TH., Verbeek, A. M. J. A. & Doesburg, W. H. (1971). Serological studies of malaria in East Africa. I. Sero-epidemiological survey in a highly endemic malarious area. Tropical and Geographical Medicine 23, 369–75.Google Scholar
Packer, M. J. & Corbet, P. S. (1989). Size variation and reproductive success of female Aedes punctor (Diptera: Culicidae). Ecological Entomology 14, 297–309.CrossRefGoogle Scholar
Polovodova, V. P. (1949). The determination of the physiological age of female Anopheles, by the number of gonotrophic cycles completed [In Russian]. Meditsinskaya Parazitologiya i Parazitarnye Bolezni (Moscow) 18, 352–5.Google Scholar
Port, G. R., Boreham, P. F. L. & Bryan, J. H. (1980). The relationship of host size to feeding by mosquitoes of the Anopheles gambiae Giles complex (Diptera: Culicidae). Bulletin of Entomological Research 70, 133–44.Google Scholar
Pringle, G. (1964). Some factors affecting the detection of residual transmission in malaria eradication schemes in Africa. Bulletin of the World Health Organization 30, 858–62.Google ScholarPubMed
Pringle, G. (1965). Report of the Malaria Co-ordinating Committee. Annual Report of the East African Institute of Malaria and Vector-borne Diseases, 1965. Dar-es-Salaam: Government Printer.Google Scholar
Pringle, G. (1966). The effect of social factors in reducing the intensity of malaria transmission in coastal East Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene 60, 549–53.CrossRefGoogle ScholarPubMed
Ramkaran, A. E. & Peters, W. (1969). Infectivity of chloroquine-resistant Plasmodium berghei to Anopheles stephensi enhanced by chloroquine. Nature, London 223, 635–6.CrossRefGoogle ScholarPubMed
Saul, A. J., Graves, P. M. & Kay, B. H. (1990). A cyclical feeding model for pathogen transmission and its application to determine vectorial capacity from vector infection rates. Journal of Applied Ecology 27, 123–33.Google Scholar
Sucharit, S., Surathin, K., Turnrasvin, W. & Sucharit, P. (1977). Chloroquine-resistant Plasmodium falciparum in Thailand and susceptibility of Anopheles. Journal of the Medical Association of Thailand 60, 648–54.Google Scholar
Tarimo, S. A., Snow, F. W., Butler, L. & Dransfield, R. (1985). The probability of tsetse acquiring trypanosome infection from single blood-meal in different localities in Kenya. Acta Tropica 42, 199–207.Google ScholarPubMed
Ward, R. A. & Savage, K. E. (1972). Effects of microsporidian parasites upon anopheline mosquitoes and malarial infection. Proceedings of the Helminthological Society of Washington (Special Issue) 39, 434–8.Google Scholar
White, G. B., Magayuka, S. A. & Boreham, P. F. L. (1972). Comparative studies on sibling species of the Anopheles gambiae Giles complex (Dipt.: Culicidae): bionomics and vectorial activity of species A and species B at Segera, Tanzania. Bulletin of Entomological Research 62, 295–317.CrossRefGoogle Scholar
Wilkinson, R. N., Noeypatimanondh, S. & Gould, D. J. (1976). Infectivity of P. falciparum malaria patients for anopheline mosquitoes before and after chloroquine treatment. Transactions of the Royal Society of Tropical Medicine and Hygiene 70, 306–7.Google Scholar
Wilson, D. B. (1960). Report on the Pare-Taveta Malaria Scheme. Dar es Salaam: Government Printer.Google Scholar
Wilson, D. B. & Wilson, M. E. (1962). Rural hyperendemic malaria in Tanganyika territory. Part II. Transactions of the Royal Society of Tropical Medicine Hygiene 56, 287–93.Google Scholar