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The Wellcome Trust Lecture: Inflammatory responses to filarial connective tissue parasites

Published online by Cambridge University Press:  23 August 2011

F. Von Lichtenberg
F. Von Lichtenberg
Affiliation:
Harvard Medical School and Brigham and Women's Hospital, 75 Francis Street, Boston, MA 02115, USA
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Summary

The inflammatory responses to lymphatic filariae and to Onchocerca volvulus are reviewed with particular attention to (1) evolutionary biology; (2) inflammatory host spectrum; (3) non-specific components; (4) immunoregulation; (5) immune evasion versus immunomodulation; (6) chronic tissue damage and scarring and (7) disease models. Basic principles of pathogenesis are emphasized, comparisons drawn with schistosome infection, and critical items of missing information are highlighted.

Type
Research Article
Information
Parasitology , Volume 94 , supplement S1: Symposia of the British Society for Parasitology Volume 24 Pathophysiological responses to parasites , January 1987 , pp. S101 - S122
Copyright
Copyright © Cambridge University Press 1987

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References

REFERENCES

Ah, H. S., McCall, J. W. & Thompson, P. E. (1974). Vaccination against experimental Brugia pahangi infection in dogs. Proceedings of the 3rd International Congress of Parasitology 3, 1236–7.Google Scholar
Albertine, K. H., Vickery, A. C. & Nayar, J. K. (1985). Lymphatic histopathology of immunologically reconstituted nude mice chronically parasitized by Brugia malayi. 34th Annual Meeting of the American Society of Tropical Medicine and Hygiene, Miami, Florida, November 7, 1985.Google Scholar
Anderson, J. & Font, R. (1976). Ocular onchocerciasis. In Pathology of Tropical and Extraordinary Diseases (ed. Binford, C. H. and Connor, D. H.), pp. 373–81. Washington D.C.: Armed Forces Institute of Pathology.Google Scholar
Bartlett, A., Turk, J., Ngu, J. L., Mackenzie, C. D., Fuglsang, H. & Anderson, J. (1978). Variation in delayed hypersensitivity in onchocerciasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 72, 372–7.CrossRefGoogle ScholarPubMed
Büttner, D. W., Laer, G., Mannweiler, E. & Büttner, M. (1982). Clinical, parasitological and serological studies on onchocerciasis in the Yemen Arab Republic. Tropenmedizin und Parasitologie 33, 201–12.Google ScholarPubMed
Cahill, K. M. & Kaiser, R. L. (1964). Lymphangiography in bancroftian filariasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 58, 356–62.CrossRefGoogle ScholarPubMed
Canlas, M. M. & Piessens, W. F. (1984). Stage-specific and common antigens of Brugia malayi identified with monoclonal antibodies. Journal of Immunology 132, 3138–41.CrossRefGoogle ScholarPubMed
Casley-Smith, J. R. & Gaffney, R. M. (1981). Excess plasma protein as a cause of chronic inflammation and lymphoedema. I. Quantitative electron microscopy. Journal of Pathology 133, 243–72.CrossRefGoogle ScholarPubMed
Cohen, L. B., Nelson, G., Wood, A. M., Manson-Bahr, P. E. C. & Bowen, R. (1961). Lymphangiography in filarial lymphoedema and elephantiasis. American Journal of Tropical Medicine and Hygiene 10, 843–8.CrossRefGoogle ScholarPubMed
Colley, D. G., Garcia, A. A., Lambertucci, J. R., Parra, J. C., Katz, N., Rocha, R. S. & Gazzinelli, G. (1986). Immune responses during human schistosomiasis. XII. Differential responsiveness in patients with hepatosplenic disease. American Journal of Tropical Medicine and Hygiene 35, 793–802.CrossRefGoogle ScholarPubMed
Conley, J. W. C. & Mendis, A. H. W. (1986). Advances in the biochemistry of filariae. Parasitology Today 2, 34–7.CrossRefGoogle Scholar
Connor, D. H., Gibson, D. W., Neafie, R. C., Merighi, B. & Buck, A. A. (1983). Sowdaonchocerciasis in North Yemen: Clinicopathologic study of 18 patients. American Journal of Tropical Medicine and Hygiene 32, 123–37.CrossRefGoogle ScholarPubMed
Connor, D. H., Morrison, N. E., Kerdel-Vegas, F., Berkoff, H. A., Johnson, F., Tunnicliffe, R., Failing, F. C.Hale, L. N., Lindquist, K., Thornbloom, W., Mccormick, J. & Anderson, S. L. (1970). Onchocerciasis, onchocercal dermatitis, lymphadenitis and elephantiasis in the Ubangi Territory. Human Pathology 1, 553–79.CrossRefGoogle ScholarPubMed
Connor, D. H., Palmieri, J. R. & Gibson, D. W. (1986). Pathogenesis of lymphatic filariasis in man. Zeitschrift für Parasitenkunde 72, 13–28.CrossRefGoogle ScholarPubMed
Coolidge, C, Weller, P. F., Ramsey, P. G., Ottesen, E. A., Beaver, P. C. & Von Lichtenberg, F. C. (1979). Zoonotic Brugia filariasis in New England. Annals of Internal Medicine 90, 341–3.CrossRefGoogle ScholarPubMed
Damian, R. T. (1984). Immunity in schistosomiasis: A holistic view. In Contemporary Topics in Immunology, vol. 12, (ed. Marchalonis, J. J.), pp. 359–20. Antwerp: Plenum Publishing Company.Google Scholar
Dean, S. D., Playfair, J. H. L., Denham, D. A. & Noscoe, N. (1983). Effect of immunosuppressive or inflammatory agents on lymphatic dilatation in cats infected with Brugia pahangi. Parasite Immunology 5, 113–22.CrossRefGoogle ScholarPubMed
Dessaint, J. P., Camus, D., Fischer, E. & Capron, A. (1977). Inhibition of lymphocyte proliferation by factor(s) produced by Schistosoma mansoni. European Journal of Immunology 7, 624–9.CrossRefGoogle ScholarPubMed
Doenhoff, M. J., Peason, S., Dunne, D. W., Bickle, Q., Lucas, S., Bain, J. & Hassounah, O. (1981). Immunological control of hepatotoxicity and parasite egg excretion in Schistosoma mansoni infections: Stage-specificity of the reactivity of immune serum in T-cell deprived mice. Transactions of the Royal Society of Tropical Medicine and Hygiene 75, 41–53.CrossRefGoogle ScholarPubMed
Domingo, E. O. & Warren, K. S. (1968). Endogenous desensitization: Changing host granulomatous response to schistosome eggs at different stages of infection with Schistosoma mansoni. American Journal of Pathology 52, 369–79.Google Scholar
Doughty, B. L. & Phillips, S. M. (1982). Delayed hypersensitivity granuloma formation and modulation around Schistosoma mansoni eggs in vitro. Journal of Immunology 128, 37–41.CrossRefGoogle ScholarPubMed
Ellner, J. J., Olds, G. R., Sabry, G., El Kholy, A. & Mahmoud, A. A. F. (1981). Dichotomies in the reactivity to worm antigen in human schistosomiasis mansoni. Journal of Immunology 126, 309–12.CrossRefGoogle ScholarPubMed
Ewert, A., Reitmeyer, J. C. & Folse, D. (1980). Chronic infection of cats with Brugia pahangi and Streptococcus. South East Asian Journal of Tropical Medicine and Public Health 11, 32–9.Google Scholar
Furman, A. & Ash, L. R. (1983). Analysis of Brugia pahangi microfilariae surface carbohydrates: Comparison of the binding of a panel of fluoresceinated lectins to mature in vivo derived and immature in utero derived microfilariae. Acta Tropica 40, 45–51.Google ScholarPubMed
Galindo, L., Von Lichtenberg, F. & Baldizon, C. (1962). Bancroftian filariasis in Puerto Rico: Infection pattern and tissue lesions. American Journal of Tropical Medicine and Hygiene 11, 739–48.CrossRefGoogle ScholarPubMed
Gazzinelli, G., Lambertucci, J. R., Katz, N., Rocha, R. S., Lima, M. S. & Colley, D. G. (1985). Immune responses during human schistosomiasis mansoni. XI. Immunologic status of patients with acute infection and after treatment. Journal of Immunology 135, 2121–7.CrossRefGoogle ScholarPubMed
George, G. H., Palmieri, J. R. & Connor, D. H. (1985). The onchocercal nodule: Interrelationship of adult worms and blood vessels. American Journal of Tropical Medicine and Hygiene 34, 1144–8.CrossRefGoogle ScholarPubMed
Georgi, J. R. (1982). Schistosoma mansoni: temporal distribution of radioselenium-labelled schistosomula in the lungs of mice during the first two weeks of infection. Parasitology 84, 263–81.CrossRefGoogle Scholar
Gibson, D. W., Connor, D. H., Brown, H. L., Fuglsang, H., Anderson, J., Duke, B. O. L. & Buck, A. A. (1976). Onchocercal dermatitis: Ultrastructural studies of microfilariae and host tissues before and after treatment with diethylcarbamazine (Hetrazan). American Journal of Tropical Medicine and Hygiene 25, 259–65.CrossRefGoogle ScholarPubMed
Hartz, P. H. & Van Der Saar, A. (1948). Tropical eosinophilia in filariasis – occurrence of radiating processes about microfilariae. American Journal of Clinical Pathology 18, 637–44.CrossRefGoogle ScholarPubMed
Henson, P. M., Mackenzie, C. D. & Spector, D. W. (1981). Inflammatory reactions in onchocerciasis. A report on current knowledge and recommendations for further study. Geneva: World Health Organization, Internal Document, 24 pp.Google Scholar
Hussain, R. & Ottesen, E. A. (1985). Immunoglobulin E responses in human filariasis. III. Specificities of IgE and IgG antibodies compared by immunoblot analysis. Journal of Immunology 135, 1415–20.CrossRefGoogle ScholarPubMed
Jachowski, L. A. Jr, Gonzalez-Flores, B. & Von Lichtenberg, F. (1962). Filarial etiology of tropical hydrocele in Puerto Rico. American Journal of Tropical Medicine and Hygiene 11, 220–33.CrossRefGoogle ScholarPubMed
Kaushal, N. A., Hussein, R. & Ottesen, E. A. (1984). Excretory-secretory and somatic antigens in the diagnosis of human filariasis. Clinical and Experimental Immunology 56, 567–76.Google ScholarPubMed
Kephart, G. M., Gleich, G. J., Connor, D. H., Gibson, D. W. & Ackerman, S. J. (1984). Deposition of eosinophil granule major basic protein onto microfilariae of Onchocerca volvulus in the skin of patients treated with diethylcarbamazine. Laboratory Investigation 50, 51–61.Google ScholarPubMed
Klei, T. R., Enright, F. M., Blanchard, D. P. & Uhl, S. A. (1981). Specific hyporesponsive granulomatous tissue reactions in Brugia pahangi infected jirds. Acta Tropica 38, 267–76.Google ScholarPubMed
Lammie, P. J. & Katz, S. P. (1983). Immunoregulation in experimental filariasis. II. Responses to parasite and non-parasite antigens in jirds with Brugia pahangi. Journal of Immunology 130, 1386–9.CrossRefGoogle Scholar
Lichtenberg, F. (1957). The early phase of endemic Bancroftian filariasis in the male. Pathological study. Journal of the Mount Sinai Hospital 24, 983–1000.Google ScholarPubMed
VoN, Lichtenberg F. (1984). Infectious diseases. In Pathologic Basis of Disease, 3rd Edn (ed. Robbins, S. L., Cotran, R. S. and Kumar, V.), p. 277. Philadelphia: W. B. Saunders.Google Scholar
Lichtenberg, F. & Medina, R. (1957). Bancroftian filariasis in the etiology of funiculoepididymitis. periorchitis and hydrocele in Puerto Rico. (Statistical study of surgical and autopsy material over a 13 year period.) American Journal of Tropical Medicine and Hygiene 6. 739–50.CrossRefGoogle Scholar
Lie, K. J. (1962). Occult filariasis: Its relationship with tropical eosinophilia. American Journal of Tropical Medicine and Hygiene 11, 646–63.Google Scholar
Longworth, D. L., Foster, D. W, Dvorak, A. M. & Weller, P. F. (1986). Incorporation of arachidonic acid by microfilariae of Brugia malayi. Journal of Infectious Diseases 152. 1317–23.CrossRefGoogle Scholar
Mackenzie, CD. (1984). Sequestration – beneficial to both host and parasite. Parasitology 88, 593–5.CrossRefGoogle ScholarPubMed
Mak, J. W., Lim, P. K. C, Sim, B. K. L. & Liew, L. M. (1983). Brujia malayi and Brugia pahangi: Cultivation in vitro of infective larvae to the fourth and fifth stages. Experimental Parasitology 55, 243–8.CrossRefGoogle Scholar
Neva, F. A. & Ottesen, E. A. (1978). Tropical (filarial) eosinophilia. New England Journal of Medicine 298. 1129–31.CrossRefGoogle ScholarPubMed
O'connor, F. W. & Hulse, C. R. (1935). Studies in filariasis. I. In Puerto Rico. Puerto Rico Journal of Public Health and Tropical Medicine 11, 167–272.Google Scholar
Ogilvie, B. M. & Wilson, R. J. M. (1976). Evasion of the immune response by parasites. British Medical Bulletin 32, 177–81.CrossRefGoogle ScholarPubMed
Olds, G. R. & Kresina, T. F. (1985). Network interactions in Schistosoma japonicum infections. Identification and characterization of a serologically distinct immunoregulatory auto-antiidiotypic antibody population. Journal of Clinical Investigation 76, 2338–47.CrossRefGoogle ScholarPubMed
Ottesen, E. A. (1984). Immunological aspects of lymphatic filariasis and onchocerciasis in man. Transactions of the Royal Society of Tropical Medicine and Hygiene 78 Suppl., 9–17.CrossRefGoogle ScholarPubMed
Ottesen, E. A., Kumaraswami, V., Paranjape, R., Poindexter, R. W. & Tripathy, S. P. (1981). Naturally occurring blocking antibodies modulate immediate hypersensitivity responses in human filariasis. Journal of Immunology 127, 2014–20.CrossRefGoogle ScholarPubMed
Ottesen, E. A., Neva, F. A., Paranjape, R. S., Tripathy, S. P., Thiruvengadam, K. V. & Beaven, M. A. (1979). Specific allergic sensitization to filarial antigens in tropical eosinophilia syndrome. Lancet i, 1158–60.CrossRefGoogle Scholar
Ottesen, E. A., Weller, P. F. & Heck, L. (1977). Specific cellular immune unresponsiveness in human filariasis. Immunology 33, 413–21.Google ScholarPubMed
Ouaissi, M. A., Dessaint, J. P., Cornette, J., Desmoutis, I. & Capron, A. (1983). Induction of non-specific human suppressor cells in vitro by defined Onchocerca volvulus antigens. Clinical and Experimental Immunology 53, 634–44.Google ScholarPubMed
Partono, F. (1986). Diagnosis and treatment of lymphatic filariasis. Parasitology Today 1, 52–7.CrossRefGoogle Scholar
Phillip, M., Gomez-Priego, A., Parkhouse, R. M. E., Davies, M. W., Clarke, N. W. T., Ogilvie, B. M. & Beltran-Hernandez, P. (1984a). Identification of an antigen of Onchocerca volvulus of possible diagnostic significance. Parasitology 89, 295–309.CrossRefGoogle Scholar
Phillip, M., Worms, M. J., Maizels, R. M. & Ogilvie, B. M. (1984b). Rodent models of filariasis. Contemporary Topics of Immunobiology 12, 276–321.Google Scholar
Piessens, W. F. & Da Silva, W. D. (1982). Complement-mediated adherence of cells to microfilariae of Brugia pahangi. American Journal of Tropical Medicine and Hygiene 31, 297–301.CrossRefGoogle Scholar
Piessens, W. F., Fuhrman, J. A. & Vickery, A. C. (1987). Immunobiology of lymphatic filariasis. In Biology of Parasitic Infections, (ed. Wyler, D.Pereira, M. and Wirth, D. F.). New York: Scientific American Publishing Company (in the Press.)Google Scholar
Piessens, W. F., McGreevy, P. B.. Ratiwayanto, S., Mcgreevy, M.. Piessens, P. W.. Koiman, I., Saroso, J. S. & Dennis, D. T. (1980). Immune responses in human infections with Brugia malayi: Correlation of cellular and humoral reactions to microfilarial antigens with clinical status. American Journal of Tropical Medicine and Hygiene 29, 563–70.CrossRefGoogle ScholarPubMed
Piessens, W. F., Ratiwayanto, S., Piessens, P. W., Tuti, S., McGreevy, P. B., Darwis, F., Palmieri, J. R.. Koiman, I. & Dennis, D. T. (1981). Effect of treatment with diethylcarbamazine on immune responses to filarial antigens in patients infected with Brugia malayi. Acta Tropica 38. 227–34.Google ScholarPubMed
Prost, A., Nebout, M. & Rougement, A. (1979). Lepromatous leprosy and onchocerciasis. British Medical Journal i, 589–90.CrossRefGoogle Scholar
Rogers, R., Denham, D. A., Nelson, G. S., Guy, F. & Ponnudurai, T. (1975). Studies with Brugia pahangi. III. Histological changes in the affected lymph nodes in infected cats. Annals of Tropical Medicine and Parasitology 69, 77–84.CrossRefGoogle ScholarPubMed
Schacher, J. F. & Sayhoun, P. F. (1967). A chronological study of the histopathology of filarial disease in cats and dogs, caused by Brugia pahangi. Transactions of the Royal Society of Tropical Medicine and Hygiene 61, 234–43.CrossRefGoogle ScholarPubMed
Schiller, E. L., Turner, V. M., Marroquin, H. F. & D'antonio, R. (1979). The cryopreservation and in vitro cultivation of larval Onchocerca volvulus. American Journal of Tropical Medicine and Hygiene 28, 997–1009.CrossRefGoogle ScholarPubMed
Snowden, K., Hammerberg, B. & Smallwood, J. E. (1986). Clinical and xeroradiographic lymphangiography studies of acute and chronic Brugia pahangi infection in dogs. Annals of Tropical Medicine and Parasitology 80, 197–210.CrossRefGoogle ScholarPubMed
Sternon, J., Parmentieri, R. & Kenis, J. (1962). Filariose et endocardite fibroplastique. Annales de la Société Belge de Medicine Tropicale 3, 351–66.Google Scholar
Thompson, J. P., Bentley, A. G., Crandall, R. B. & Crandall, C. A. (1984). The histology and ultrastructure of the Meyers-Kouvenaar body in ferrets infected with Brugia malayi. American Journal of Tropical Medicine and Hygiene 33, 1141–6.CrossRefGoogle ScholarPubMed
Vickery, A. C. & Vincent, A. C. (1984). Immunity to Brugia pahangi in athymic nude and normal mice: Eosinophilia, antibody and hypersensitivity responses. Parasite Immunology 6, 545–59.CrossRefGoogle ScholarPubMed
Wartman, W. B. (1947). Filariasis in American armed forces in World War II. Medicine 26, 333–94.CrossRefGoogle ScholarPubMed
Weinstein, P. (1986). Filariasis: Problems and challenges. American Journal of Tropical Medicine and Hygiene 35, 221–33.CrossRefGoogle Scholar
Weiss, N. & Tanner, M. (1979). Studies on Dipetalonema viteae (Filaroidea). Antibody-dependent, cell-mediated destruction of microfilariae in vivo. Tropenmedizin und Parasitologie 30, 73–80.Google Scholar
Yates, J. A. & Higashi, G. I. (1985). Brugia malayi: Vaccination of jirds with 60 Cobalt-attenuated infective stage larvae protects against homologous challenge. American Journal of Tropical Medicine and Hygiene 34, 1132–7.CrossRefGoogle Scholar