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Brugia malayi microfilaraemia in mice: a model for the study of the host response to microfilariae

Published online by Cambridge University Press:  06 April 2009

D. I. Grove ,
R. S. Davis  and
K. S. Warren
D. I. Grove
Affiliation:
Division of Geographic Medicine, Department of Medicine, Case Western Reserve University and University Hospitals, Cleveland, Ohio 44106
R. S. Davis
Affiliation:
Division of Geographic Medicine, Department of Medicine, Case Western Reserve University and University Hospitals, Cleveland, Ohio 44106
K. S. Warren
Affiliation:
Division of Geographic Medicine, Department of Medicine, Case Western Reserve University and University Hospitals, Cleveland, Ohio 44106
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Summary

Microfilariae of Brugia malayi were obtained from the peritoneal cavities of infected gerbils and were then injected intravenously into mice. A sub-periodic, nocturnal microfilaraemia was produced. The level of microfilaraemia was proportional to the number of parasites injected, with approximately 1–3% of microfilariae being found in the peripheral circulation. The duration of microfilaraemia was proportional to the number of parasites injected; it subsided by 30 days after injection of 104 microfilariae but was still present at a low level 120 days after injection of 2 × 105 microfilariae. A transient splenomegaly developed after injection of microfilariae. Histopathological examination revealed large numbers of microfilariae free in the lumens of pulmonary small blood vessels and without any accompanying inflammatory reaction. Lesser numbers of microfilariae were seen in the cardiac blood and hepatic and renal blood vessels for the first few days after injection. There was cellular proliferation in the splenic white pulp and vascular congestion of the red pulp. Microfilariae labelled with 51Cr were injected intravenously; 57% of radioactivity was found in the lungs, 8·5% in the liver and 2·9% in the spleen. Mice developed immediate hypersensitivity reactions to B. malayi antigen by 4 weeks after injection, but Arthus and delayed hypersensitivity reactions were not seen at any time. When mice which had been injected 5 months previously were challenged with a 2nd injection of microfilariae, there was an accelerated clearance of parasites over 2 weeks and a marked peripheral blood eosinophilia developed. In contrast with natural infections, in which the continuous production of microfilariae complicates assessment, this model provides a system in which factors controlling the circulation of microfilariae in the bloodstream can be studied independently.

Type
Research Article
Information
Parasitology , Volume 79 , Issue 3 , December 1979 , pp. 303 - 316
Copyright
Copyright © Cambridge University Press 1979

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References

REFERENCES

Ahmed, S. S. (1967). Studies on the laboratory transmission of subperiodic Brugia malayi and Brugia pahangi I. The resistance of guinea-pigs, rabbits and white mice to infection. Annals of Tropical Medicine and Parasitology 61, 93–100.CrossRefGoogle ScholarPubMed
Ash, L. R. & Schacher, J. F. (1971). Early life cycle and larval morphogenesis of Wuchereria bancrofti in the jird, Meriones unguiculatus. Journal of Parasitology 57, 1043–51.Google Scholar
Augustine, D. L. & Drinker, C. K. (1935). The migration of microfilariae (Dirofilaria immitis) from the blood vessels to the lymphatics. Transactions of the Royal Society of Tropical Medicine and Hygiene 29, 303–6.Google Scholar
Fulleborn, F. (1912). Beiträge zur Biologie der Filarien. Zentralblatt für Bakteriologie, Parasitenkunde und Infektionskrankheiten 66, 255–67.Google Scholar
Gonnert, R. (1942). Zur Lebensdauer menschlicher Microfilarien. Zentralblatt für Bakteriologie, Parasitenkunde und Infektionskrankheiten 149, 75–81.Google Scholar
Grove, D. I., Cabrera, B. D., Valeza, F. S., Guinto, R. S., Ash, L. R. & Warren, K. S. (1977). Sensitivity and specificity of skin reactivity to Brugia malayi and Dirofilaria immitis antigens in bancroftian and malayan filariasis in the Philippines. American Journal of Tropical Medicine and Hygiene 26, 220–9.CrossRefGoogle ScholarPubMed
Grove, D. I. & Davis, R. S. (1978). Serological diagnosis of bancroftian and malayan filariasis. American Journal of Tropical Medicine and Hygiene 27, 508–13.Google Scholar
Grove, D. I., Mahmoud, A. A. F. & warren, K. S. (1977). Eosinophils and resistance to Trichinella spiralis. Journal of Experimental Medicine 145, 755–9.CrossRefGoogle ScholarPubMed
Gruby, D. & Delafond, H. (1852). Troisième memoire sur le ver filaire que vit dans le sang du chien domestique. Compte Rendu de l'Académie de Science 34, 9–14.Google Scholar
Hawking, F. (1940). The transference of Microfilaria bancrofti into natural and unnatural hosts. Annals of Tropical Medicine and Parasitology 34, 121–9.CrossRefGoogle Scholar
Hawking, F. (1953). The periodicity of microfilariae: III. Transfusion of microfilariae in a clean host. Transactions of the Royal Society of Tropical Medicine and Hygiene 47, 82–3.Google Scholar
Hawking, F. (1975). Circadian and other rhythms of parasites. In Advances in Parasitology, vo1. 13 (ed. Dawes, B.), pp. 123–82. London: Academic Press.Google Scholar
Hawking, F. & Thurston, J. D. (1951). The periodicity of microfilariae. I. The distribution of microfilariae in the body. Transactions of the Royal Society of Tropical Medicine and Hygiene 45, 307–28.Google Scholar
Hawking, F., Worms, M. J. & Walker, P. (1965). The periodicity of microfilariae. IX. Transfusion of microfilariae (Edesonfilaria) into monkeys at a different phase of the circadian rhythm. Transactions of the Royal Society of Tropical Medicine and Hygiene 59, 26–41.CrossRefGoogle Scholar
Hinman, E. H., Faust, E. C. & De Bakey, M. E. (1934). Filiarial periodicity in the dog heartworm Dirofilaria immitis after blood transfusion. Proceedings of the Society for Experimental Biology and Medicine 31, 1043–6.Google Scholar
Kazura, J. W. & Grove, D. I. (1978). Stage-specific antibody-dependent eosinophilmediated destruction of Trichinella spiralis. Nature, London 274, 588–9.CrossRefGoogle ScholarPubMed
Kershaw, W. E. (1949). Observations on Litomosoides carinii (Travassos, 1919) Chandler, 1931. II. The migration of the first-stage larva. Annals of Tropical Medicine and Parasitology 43, 96–115.CrossRefGoogle Scholar
Knott, J. (1935). The periodicity of the microfilaria of Wuchereria bancrofti. Preliminary report of some injection experiments. Transactions of the Royal Society of Tropical Medicine and Hygiene 29, 59–64.CrossRefGoogle Scholar
Mahmoud, A. A. F., Warren, K. S. & Peters, P. A. (1975). A role for the eosinophil in acquired resistance to Schistosoma mansoni infection as determined by anti-eosinophil serum. Journal of Experimental Medicine 142, 805–13.Google Scholar
Mazzotti, L. & Palomo, E. (1957). A note on the survival of the microfilariae of Mansonella ozzardi. Bulletin of the World Health Organization 16, 696–9.Google Scholar
Nelson, G. S. (1962). Observations on the development of Setaria labiatopapillosa using new techniques for infecting Aedes aegypti with this nematode. Journal of Helminthology 36, 281–96.CrossRefGoogle ScholarPubMed
Pachecho, G. (1974). Relationship between the number of circulating microfilariae and the total population of microfilariae in a host. Journal of Parasitology 60, 814–8.CrossRefGoogle Scholar
Pachecho, G. & Orihel, T. C. (1968). Relationship between detectable microfilaremia and total population of microfilariae in monkeys infected with Dirofilaria corynodes. Journal of Parasitology 54, 1234–5.CrossRefGoogle Scholar
Ponnudurai, T., Denham, D. A., Nelson, G. S. & Rogers, R. (1974). Studies with Brugia pahangi 4. Antibodies against adult and microfilarial stages. Journal of Helminthology 48, 107–11.Google Scholar
Ponnudurai, T., Denham, D. A. & Rogers, R. (1975). Studies on Brugia pahangi 9. The longevity of microfilariae transfused from cat to cat. Journal of Helminthology 49, 25–30.Google Scholar
Underwood, P. C. & Harwood, P. D. (1939). Survival and location of the microfilaria of Dirofilaria immitis of dog. Journal of Parasitology 25, 23–33.CrossRefGoogle Scholar
Vincent, A. L. & Ash, L. R. (1978). Splenomegaly in jirds (Meriones unguiculatus) infected with Brugia malayi (Nematoda: Filarioidea) and related species. American Journal of Tropical Medicine and Hygiene 27, 514–20.CrossRefGoogle Scholar
Weiss, N. (1970). Parasitologische und immunobiologische Untersuchungen über die durch Dipetalonema viteae erzeugte Nagetierfilariose. Acta Tropica 27, 219–59.Google Scholar
Wong, M. M. (1964 a). Studies on microfilaremia in dogs I. A search for the mechanisms that stabilise the level of microfilaremia. American Journal of Tropical Medicine and Hygiene 13, 57–65.CrossRefGoogle Scholar
Wong, M. M. (1964 b). Studies on microfilaremia in dogs. II. Levels of microfilaremia in relation to immunologic response of the host. American Journal of Tropical Medicine and Hygiene 13, 66–77.CrossRefGoogle ScholarPubMed
Wong, M. M. & Guest, M. F. (1969). Filarial antibodies and eosinophilia in human subjects in an endemic area. Transactions of the Royal Society of Tropical Medicine and Hygiene 63, 796–800.Google Scholar