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Acquired resistance to Onchocerca lienalis infections in Simulium ornatum Meigen and Simulium lineatum Meigen following passive transfer of haemolymph from previously infected simuliids (Diptera, Simuliidae)

Published online by Cambridge University Press:  06 April 2009

P. J. Ham
Affiliation:
Department of Medical Helminthology, Winches Farm Field Station, London School of Hygiene and Tropical Medicine, 395 Hatfield Road, St Albans, Hertfordshire AL4 OXQ

Summary

This study describes experiments which demonstrate the presence of a parasite-induced or derived factor in the haemocoel of Onchocerca lienalis-infected simuliids. Haemolymph, when transferred from previously infected donor flies to previously untreated recipient flies, using fine glass needles, confers protection against a subsequent challenge to the recipients. In three trials using Simulium ornatum sl. or S. linealum, significant levels of protection in ‘immunized’ compared to ‘challenge control’ groups were achieved (84% and 81% with S. ornatum sl. and 85% with S. lineaturm). This is despite the fact that the worm burdens of the infected donor groups in the three trials were very different (means of 33·1 and 3·4 larvae/fly with S. ornatum sl. and 1·6 larvae/fly with S. linealum). The use of sham-operated and bentonite-inoculated control groups demonstrate that this effect is not merely a non-specific reaction to trauma, but is probably parasitic in its derivation. The use of double infections separated by 4 days shows that the donor flies have themselves probably acquired resistance to O. lienalis. Frequency distributions of O. lienalis burdens in individual flies show that there is a shift froni a normal to a skew distribution when comparing ‘challenge control’ flies with ‘immunized’. This possible acquired resistance could have important implications in the transmission of forest and savanna human onchocerciasis by the Simulium damnosum complex.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1986

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References

REFERENCES

Beckett, E. B. (1971). Histological changes in mosquito flight muscle fibres associated with parasitization by filarial larvae. Parasitology 63, 365–72.CrossRefGoogle ScholarPubMed
Bianco, A. E., Ham, P., El Sinnary, K. & Nelson, G. S. (1980). Large scale recovery of Onchocerca microfilariae from naturally infected cattle and horses. Transactions of the Royal Society of Tropical Medicine and Hygiene 74, 109.Google Scholar
Bianco, A. E. & El Sinnary, K. (1980). Infection of Aedes aegypti with Onchocerca gutturosa. Journal of Helminthology 54, 105–7.CrossRefGoogle ScholarPubMed
Bianco, A. E., Townson, S., El Sinnary, K. & Nelson, G. S. (1979). Successful development of Onchocerca from cattle in Aedes, Anopheles, Culex and Culicoides sp. Parasitology 79, 35.Google Scholar
Boman, H. G., Boman, A. & Pigon, A. (1981). Immune and injury responses in Cecropia pupae – RNA isolation and comparison of protein synthesis in vivo and in vitro. Insect Biochemistry 11, 3342.CrossRefGoogle Scholar
Chadwick, J. S. (1970). Relation of lysozyme concentration to acquired immunity against Pseudomonas aeruginosa in Galleria mellonella. Journal of Invertebrate Pathology 15, 455–6.CrossRefGoogle Scholar
Collins, R. C. & Jones, R. H. (1978). Laboratory transmission of Onchocerca cervicalis with Culicoides variipennis. American Journal of Tropical Medicine and Hygiene 27, 4650.CrossRefGoogle ScholarPubMed
Duke, B. O. L. & Lewis, D. J. (1964). Studies on factors influencing the transmission of onchocerciasis. III. Observations on the effect of the peritrophic membrane in limiting the development of Onchocercavolvulus microfil ariae in Simuliumdamnosum. Annals of Tropical Medicine and Parasitology 58, 83–8.CrossRefGoogle Scholar
Eichler, D. A. (1973). Studies on Onchocerca gutturosa (Neumann, 1910) and its development in Simulium ornatum (Meigen, 1818). 3. Factors affecting the development in its vector. Journal of Helminthology 47, 7388.CrossRefGoogle ScholarPubMed
Hall, D. W. (1983). Mosquito hemocytes: A review. Developmental and Comparative Immunology 7, 112.CrossRefGoogle ScholarPubMed
Ham, P. J. & Banya, A. J. (1984). The effect of experimental Onchocerca infections on the fecundity and oviposition of laboratory reared Simulium sp. (Diptera, Simuliidae). Tropenmedizin und Parasitologie 35, 61–6.Google ScholarPubMed
Ham, P. J. & Bianco, A. E. (1983). Screening of some British simuliids for susceptibility to experimental Onchocerca lienalis infection. Zeitschrift für Parasitenkunde 69, 765–72.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). Tropenmedizinund Parasitologie 35, 212–16.Google ScholarPubMed
Ham, P. J., Townson, S., James, E. R. & Bianco, A. E. (1981). An improved technique for the cryopreservation of Onchocerca microfilariae. Parasitology 83, 139–46.CrossRefGoogle ScholarPubMed
Ho, B.-C., Yap, E.-H. & Singh, M. (1982). Melanization and encapsulation in Aedes aegypti and Aedes togoi in response to parasitization by a filarioid nematode (Breinlia booliati). Parasitology 85, 567–75.CrossRefGoogle ScholarPubMed
Hultmark, D., Steiner, H., Rasnuson, T. & Boman, H. G. (1980). Insect immunity. Purification and properties of three inducible bacterial proteins from hemolymph of immunized pupae of Hyalophora cecropia. European Journal of Biochemistry 106, 716.CrossRefGoogle Scholar
Kartman, L. (1953). Factors influencing infection of the mosquito with Dirofilaria immitis (Leidy, 1856). Experimental Parasitology 2, 2778.CrossRefGoogle Scholar
Lackie, A. M. (1981). Immune recognition in insects. Developmental and Comparative Immunology 5, 191204.CrossRefGoogle ScholarPubMed
Lebied, B. (1950). Une nouvelle théorie endémiologique sur 1e rôle de lafonction du parasitisme: Mécanisme du vol du vecteur comme fact eur décisif de l'établissement du foyer de l'endémicité de l'onchocercose et defilarioses en général. Dijon: Imprimerie Darantière.Google Scholar
Lox, J. B., Cupp, E. W., Bernardo, M. J. & Pollacx, R. J. (1983). Further studies on the development of Onchocerca spp. (Nematoda:Filarioidea) in Nearctic black flies (Diptera:Simuliidae). American Journal of Tropical Medicine and Hygiene 32, 1298–305.Google Scholar
Lou, J. B., Cupp, E. W., Braide, E. I. & Bernardo, M. J. (1980). Aedes aegypti as a surrogate host for Onchocerca spp. American Journal of Tropical Medicine and Hygiene 29, 382–8.Google Scholar
Mellor, P. S. (1971). Studies on Onchocerca cervicalis (Railliet and Henry, 1910) and its development in Culicoides, Latrielle. Ph.D. thesis, University of London.Google Scholar
Omar, M. S. & Garms, R. (1975). The fate and migration of a Guatemalan strain of Onchocerca volvulus in Simulium ochraceum and S. metallicum and the role of the buccopharyngeal armature in the destruction of microfilariae. Tropenmedizin und Parasitologie 26, 183–90.Google ScholarPubMed
Oothuman, P., Simpson, M. S. & Laurence, B. R. (1974). Abnormal development of a filarial worm, Brugia patei (Buckley, Nelson and I-Ieisch), in a mosquito host, Anopheles labranchiae atroparvus van Thiel. Journal of Helminthology 48, 161–5.CrossRefGoogle Scholar
Owen, R. R. (1979). Non-development of Brugia pahangi in a refractory mosquito, Aedes malayensis. Annals of Tropical Medicine and Parasitology 73, 193–5.CrossRefGoogle Scholar
Reid, G. D. F. (1978). Cibarial armature of Simulium vectors of onchocerciasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 72, 438.Google Scholar
Reid, G. D. F. (1979). The development of Onchocerca volvulus in two temperate blackfly species, Simulium ornatum Meigen and Simulium lineatum Meigen. Annals of Tropical Medicine and Parasitology 73, 577–81.CrossRefGoogle ScholarPubMed
Steward, J. S. (1937). The occurrence of Onchocerca gutturosa Neumann in cattle in England with an account of its life-history and development in Simulium ornatum (Meigen, 1818). Parasitology 29, 212–19.CrossRefGoogle Scholar
Sutherland, D. R., Christensen, I. M. & Forton, K. F. (1984). Defense reactions of mosquitoes to filarial worms: role of the microfilarial sheath in the response of mosquitoes to inoculated Brugia pahangi microfilariae. Journal of Invertebrate Pathology 44, 275–81.CrossRefGoogle ScholarPubMed
Weathersby, A. B. (1960). Further studies on exogenous development of malaria in the haemocoels of mosquitoes. Experimental Parasitology 10, 211–13.CrossRefGoogle ScholarPubMed
Yoeli, M. (1973). Plasmodium berghei: mechanisms and sites of resistance to sporogonic development in different mosquitoes. Experimental Parasitology 34, 448–58.CrossRefGoogle ScholarPubMed
Zielke, E. (1977). Further studies on the development of Onchocerca volvulus in mosquitoes. Transactions of the Royal Society of Tropical Medicine and Hygiene 71, 546–7.CrossRefGoogle ScholarPubMed
Zielke, E., Schulz-Key, H. & Albiez, E. J. (1977). On the development of Onchocerca volvulus in mosquitoes. Tropenmedizin und Parasitologie 28, 254–7.Google ScholarPubMed