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Vector survival and parasite infection: the effect of Wuchereria bancrofti on its vector Culex quinquefasciatus

Published online by Cambridge University Press:  10 June 2004

K. KRISHNAMOORTHY ,
S. SUBRAMANIAN ,
G. J. VAN OORTMARSSEN ,
J. D. F. HABBEMA  and
P. K. DAS
K. KRISHNAMOORTHY
Affiliation:
Vector Control Research Centre (Indian Council of Medical Research), Indira Nagar, Medical Complex, Pondicherry-605 006, India
S. SUBRAMANIAN
Affiliation:
Vector Control Research Centre (Indian Council of Medical Research), Indira Nagar, Medical Complex, Pondicherry-605 006, India
G. J. VAN OORTMARSSEN
Affiliation:
Department of Public Health, Erasmus MC, University Medical Center Rotterdam, P.O. Box 1738, 3000 DR Rotterdam, The Netherlands
J. D. F. HABBEMA
Affiliation:
Department of Public Health, Erasmus MC, University Medical Center Rotterdam, P.O. Box 1738, 3000 DR Rotterdam, The Netherlands
P. K. DAS
Affiliation:
Vector Control Research Centre (Indian Council of Medical Research), Indira Nagar, Medical Complex, Pondicherry-605 006, India
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Abstract

This paper investigates a cohort of 2187 laboratory reared Culex quinquefasciatus fed on 69 human volunteers, including 59 persons with different levels of Wuchereria bancrofti microfilariae and 10 without microfilaria. Mosquitoes were followed until death. Mosquito survival was analysed in relation to the level of microfilaria in the human and larval count in the dead mosquito. Vector mortality during the extrinsic incubation period (12 days post-engorgement) was significantly higher in mosquitoes fed on microfilaraemic volunteers (50%) than in those fed on amicrofilaraemics (29%). Both the percentage infected and the geometric mean parasite density was significantly higher among mosquitoes which died before 13 days (45% infected and 10 larvae per infected mosquito) than those surviving beyond 13 days (39% and 2·2), suggesting a parasite loss of more than 80% during the extrinsic incubation period. A large proportion (62%) of the mosquitoes that died during the early of phase of parasite development were infected (36% in low, 26% in medium and 90% in high human Mf-density). Survival analysis showed that the parasite load in mosquitoes and the human Mf-density for a given parasite load are independent risk factors of vector survival. Overall, the hazard of dying was found to be 11–15 times higher among mosquitoes fed on microfilaraemic volunteers than those fed on amicrofilaraemics. The hazard doubles for every increase of about 60–70 parasites in the vector. As a consequence of the parasite-induced reduction in vector survival, the transmission success of the parasite is reduced. The implication of the results on control/elimination of lymphatic filariasis using mass-drug administration is discussed.

Keywords

lymphatic filariasisWuchereria bancroftiCulex quinquefasciatusparasite-induced vector mortalityWeibull model
Type
Research Article
Information
Parasitology , Volume 129 , Issue 1 , July 2004 , pp. 43 - 50
Copyright
© 2004 Cambridge University Press

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References

REFERENCES

BASANEZ, 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: relation between microfilarial intake and mortality in the simuliid vector. Parasitology 113, 331–355.CrossRefGoogle Scholar
BASU, B. C. & RAO, S. S. ( 1939). Studies on filariasis transmission. Indian Journal of Medical Research 27, 233–249.Google Scholar
BRENGUES, J. & BAIN, O. ( 1972). Passage of microfilariae from the stomach to the haemocoel of the vector, in the case of Wuchereria bancrofti in Anopheles gambiae A and Aedes aegypti and Setaria labiatopapillosa in Aedes aegypti. Cahhiers ORSTOM, Serie Entomologie medicale et Parasitologie 10, 235–249.Google Scholar
BRYAN, J. H. & SOUTHGATE, B. A. ( 1988). Factors affecting transmission of Wuchereria bancrofti by anopheline mosquitoes. 2. Damage to ingested microfilarie by mosquito foregut armatures and development of filarial larvae in mosquitoes. Transactions of the Royal Society of Tropical Medicine and Hygiene 82, 138–145.Google Scholar
COLLETT, D. ( 1994). Modelling Survival Data in Medical Research. Chapman and Hall, Madras.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, 189–193.CrossRefGoogle Scholar
CRAWLEY, M. J. ( 1993). Methods in Ecology. Blackwell Scientific Publications Ltd, Oxford.
DAS, M. ( 1976). Vectors of filaria with special reference to India. Journal of Communicable Diseases 8, 101–109.Google Scholar
DAS, P. K., MANOHARAN, A., SRIVIDYA, A., GRENFELL, B. T., BUNDY, D. A. & VANAMAIL, P. ( 1990). Frequency distribution of Wuchereria bancrofti microfilariae in human populations and its relationships with age and sex. Parasitology 3, 429–434.CrossRefGoogle Scholar
DAS, P. K., SUBRAMANIAN, S., MANOHARAN, A., RAMAIAH, K. D., VANAMAIL, P., GRENFELL, B. T., BUNDY, D. A. P. & MICHAEL, E. ( 1995). Frequency distribution of Wuchereria bancrofti infection in the vector host in relation to human host: evidence for density dependence. Acta Tropica 60, 159–165.CrossRefGoogle Scholar
DYE, C. & WILLIAMS, B. G. ( 1995). Non-linearities in the dynamics of indirectly-transmitted infections (or, does having a vector make a difference?). In Ecology of Infectious Diseases in Natural Populations ( ed. Grenfell, B. T. & Dobson, A. P.), pp. 260–279. Cambridge University Press, Publications of the Newton Institute, Cambridge.
FAILLOUX, A. B., RAYMOND, M., UNG, A., GLAZIOU, P., MARTIN, P. M. V. & PASTEUR, A. ( 1995). Variation in the vector competence of Aedes polynesiensis for Wuchereria bancrofti. Parasitology 111, 19–29.CrossRefGoogle Scholar
JAYASEKERA, N., KALPAGE, K. S. & DE SILVA, C. S. ( 1991). The significance of low density microfilaraemia in the transmission of Wuchereria bancrofti by Culex (Culex) quinquefasciatus Say in Sri Lanka. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 250–254.CrossRefGoogle Scholar
JORDAN, P. & GOATLY, K. D. ( 1962). Bancroftian filariasis in Tanganyika: a quantitative study of the uptake, fate and development of microfilariae of Wuchereria bancrofti in Culex fatigans. Annals of Tropical Medicine Parasitology 56, 173–187.CrossRefGoogle Scholar
KRISHNASWAMI, A. K., PATTANAYAK, S. & RAGHAVAN, N. G. S. ( 1959). The susceptibility of Culex fatigans to different densities of microfilariae bancrofti. Indian Journal of Malariology 13, 153–157.Google Scholar
MAEDA, R. & KURIHARA, T. ( 1980). The effect of age of Aedes togoi on the transmission of Brugia malayi in the laboratory. Japanese Journal of Sanitary Zoology 31, 277–281.CrossRefGoogle Scholar
McGREEVY, P. B., BRYAN, J. H., OOTHUMAN, P. & KOLSTRUP, N. ( 1978). The lethal effects of the cibarial and pharyngeal armatures of mosquitoes on microfilariae. Transactions of the Royal Society of Tropical Medicine and Hygiene 72, 361–368.CrossRefGoogle Scholar
NATHAN, M. B. ( 1981). Bancroftian filariasis in coastal North Trinidad, West Indies: intensity of transmission by Culex quinquefasciatus. Transactions of the Royal Society of Tropical Medicine and Hygiene 75, 721–730.CrossRefGoogle Scholar
OTTESEN, E. A. & RAMACHANDRAN, C. P. ( 1995). Lymphatic filariasis infection and disease: control strategies. Parasitology Today 11, 129–131.CrossRefGoogle Scholar
PICHON, G. ( 1974). Relations mathematiques entre le nombre des microfilaires ingereese et le nombre des parasites chez differents vecteurs naturels ou experimentaux de filarioses. Cahiers ORSTOM serie Entomologie medicale et Parasitologie 12, 199–216.Google Scholar
PICHON, G., PRODHON, J. & RIVIERE, F. ( 1980 a). Filariasis: excessive dispersal of parasites and excessive infection of the invertebrate host. Entomologie Medicale et Parasitologie 18, 27–47.Google Scholar
PICHON, G., PRODHON, J. & RIVIERE, F. ( 1980 b). Heterogeneous nature of the ingestion of blood-inhabiting parasites by their vectors: quantitative description and interpretation. Comptes Rendus Hebdomadaires des Seances de l'Academie des Sciences, D 290, 1011–1013.Google Scholar
RAJAGOPALAN, P. K., KAZMI, S. J. & MANI, T. R. ( 1977). Some aspects of transmission of Wuchereria bancrofti and ecology of the vector Culex pipiens fatigans in Pondicherry. Indian Journal of Medical Research 66, 200–215.Google Scholar
SAMARAWICKREMA, W. A. ( 1967). A study of the age composition of natural populations of Culex pipiens fatigans Widemann in relation to the transmission of filariasis due to Wuchereria bancrofti (Cobbold) in Ceylon. Bulletin of World Health Organisation 37, 117–137.Google Scholar
SAMARAWICKREMA, W. A. & LAURENCE, B. R. ( 1978). Loss of filarial larvae in a natural mosquito population. Annals of Tropical Medicine and Parasitology 72, 561–565.CrossRefGoogle Scholar
SAPORU, F. W. ( 1993). Analysis of survival data for Simulium damnosum using the regression method. Annals of Tropical Medicine and Parasitology 87, 563–569.CrossRefGoogle Scholar
SUBRAMANIAN, S., MANOHARAN, A., RAMAIAH, K. D. & DAS, P. K. ( 1994). Rates of acquisition and loss of Wuchereria bancrofti infection in Culex quinquefasciatus. American Journal of Tropical Medicine and Hygiene 51, 244–249.CrossRefGoogle Scholar
SUBRAMANIAN, S., KRISHNAMOORTHY, K., RAMAIAH, K. D., HABBEMA, J. D. F., DAS, P. K. & PLAISIER, A. P. ( 1998). The relationship between microfilarial load in the human host and uptake and development of Wuchereria bancrofti microfilariae by Culex quinquefasciatus: a study under natural conditions. Parasitology 116, 243–255.CrossRefGoogle Scholar