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Concomitant malaria (Plasmodium gallinaceum) and filaria (Brugia pahangi) infections in Aedes aegypti: effect on parasite development

Published online by Cambridge University Press:  06 April 2009

C. M. R. Albuquerque
Affiliation:
Centre for Applied Entomology and Parasitology, Department of Biological Sciences, Keele University, Keele, Staffs ST5 5BG
P. J. Ham
Affiliation:
Centre for Applied Entomology and Parasitology, Department of Biological Sciences, Keele University, Keele, Staffs ST5 5BG

Extract

Mixed infections with malarial (Plasmodium gallinaceum) and filarial (Brugia pahangi) parasites were carried out in 8 trials with filaria susceptible (REFM) and filaria refractory (REP-RR) Aedes aegypti strains. A secondary infection with B. pahangi microfilariae (mff) by intrathoracic inoculation, reduced the development rate of a pre-existing P. gallinaceum infection. The level of reduction ranged from 9·5 to 49% in REFM and from 50 to 90% in REP-RR. An immune response against oocysts was seen as melanization in mosquitoes with a double infection in the strain refractory to B. pahangi (REP-RR) and a reduction in oocyst size in both mosquito strains. Melanization was not observed in mosquitoes infected only with P. gallinaceum. This may indicate that activation of the prophenoloxidase (PPO) cascade in response to mff in the haemolymph can also be addressed against oocysts in the midgut. No significant difference in the number of filarial parasites recovered was observed when comparing groups with a single or double infection. Retardation in development of filaria larvae was observed in mosquitoes with double infection (REFM strain), together with melanization and a higher rate of abnormal development. Nutritional deficiency caused by superinfection might also be responsible for the delay in filarial development and reduced oocyst size.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1995

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References

REFERENCES

Bartlett, C. M. (1984). Development of Dirofilaria scapiceps (Leidy, 1886) (Nematoda: Filarioidea) in Aedes spp. and Mansonia perturbans (Walker) and responses of mosquitoes to infection. Canadian Journal of Zoology 62, 112–29.CrossRefGoogle Scholar
Burkot, T. R., Molineaux, L., Graves, P. M., Paru, R., Battistutta, D., Dagoro, H., Barnes, A., Wirtz, R. A. & Garner, P. (1990). The prevalence of naturally acquired multiple infections of Wuchereria bancrofti and human malarias in anophelines. Parasitology 100, 369–75.CrossRefGoogle ScholarPubMed
Coleman, R. E., Edman, J. D. & Semprevivo, L. H. (1988). Interactions between malaria (Plasmodium yoelli) and leishmaniasis (Leishmania mexicana amazonensis): Effect of concomitant infection on host activity, host body temperature and vector engorgement success. Journal of Medical Entomology 25, 467–71.CrossRefGoogle ScholarPubMed
Collins, F. H., Vernick, K. D., Paskewitz, S., Seiley, 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.CrossRefGoogle ScholarPubMed
Ham, P. J. & Gale, C. L. (1984). Blood meal enhanced Onchocerca development and its correlation with fecundity in laboratory reared Blackflies (Diptera, Simuliidae). Tropenmedizin und Parasitologie 35, 212–16.Google Scholar
McCall, J. W., Malone, J. B., Ah, H. S. & Thompson, P. E. (1973). Mongolian jirds (Meriones unguiculatus) infected with Brugia pahangi by intraperitoneal route: a rich source of developing larvae, adult filariae and microfilariae. Journal of Parasitology 59, 436.Google Scholar
MacDonald, W. W. (1962). The genetic basis of susceptibility to infection with semi-periodic Brugia malayi in Aedes aegypti. Annals of Tropical Medicine and Parasitology 56, 373–82.CrossRefGoogle Scholar
MacDonald, W. W. & Ramachandran, C. P. (1965). The influence of the gene fm (filarial susceptibility, Brugia malayi) on the susceptibility of Aedes aegypti to seven strains of Brugia, Wuchereria and Dirofilaria. Annals of Tropical Medicine and Parasitology 59, 6473.CrossRefGoogle ScholarPubMed
Matthews, H. A. (1987). An analysis of gene linkage, interaction and expression in relation to susceptibility of Aedes aegypti, to infection with Dirofilaria immitis, D. repens and Brugia pahangi. Ph.D. thesis, University of Liverpool.Google Scholar
Medley, G. F., Sinden, R. E., Fleck, S., Billingsley, P. F., Tirawanchai, N. & Rodrigues, M. H. (1993). Heterogeneity in patterns of malarial oocyst infections in the mosquito vector. Parasitology 106, 441–9.CrossRefGoogle ScholarPubMed
Nayar, J. K. & Knight, J. W. (1991). Nutritional factors and antimicrobials on development of infective larvae of subperiodic Brugia malayi (Nematoda: Filarioidea)in Anopheles quadrimaculatus and Aedes aegypti (Diptera: Culicidae). Journal of Medical Entomology 28, 275–9.CrossRefGoogle ScholarPubMed
Nayar, J. K., Knight, J. W. & Vickery, A. C. (1989). Intracellular melanization in the mosquito Anopheles quadrimaculatus (Diptera: Culicidae) against the filarial nematodes, Brugia spp. (Nematoda: Filarioidea). Journal of Medical Entomology 26, 159–66.CrossRefGoogle ScholarPubMed
Pumpuni, C. B., Beier, M. S., Natori, J. P., Guers, L. D. & Davis, J. R. (1993). Plasmodium falciparum: Inhibition of sporogonic development in Anopheles stephensi by gram-negative bacteria. Experimental Parasitology 77, 195–9.CrossRefGoogle ScholarPubMed
Roseboom, L. E., Behin, R. & Kassira, E. N. (1966). Dual infections of Aedes aegypti L. with Plasmodium gallinaceum Brumpt and West Nile Virus. Journal of Parasitology 52, 579–82.CrossRefGoogle Scholar
Schmidt, L. H. & Essinger, J. H. (1981). Courses of infection with Plasmodium falciparum in owl monkeys displaying a microfilaremia. American Journal of Tropical Medicine and Hygiene 30, 511.CrossRefGoogle ScholarPubMed
Travi, B. L. & Orihel, T. C. (1987). Development of Brugia malayi and Dirofilaria immitis in Aedes aegypti: Effect of the host's nutrition. Tropical Medicine and Parasitology 38, 1922.Google Scholar
Turell, M. J., Rossignol, P. A., Spielman, A., Rossi, C. A. & Bailey, C. L. (1984). Enhanced arboviral transmission by mosquitoes that concurrently ingested-microfilariae. Science 225, 1039–41.CrossRefGoogle ScholarPubMed