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Immunity in human schistosomiasis mansoni: prevention by blocking antibodies of the expression of immunity in young children

Published online by Cambridge University Press:  06 April 2009

A. E. Butterworth*
Affiliation:
Department of Pathology, Tennis Court Road, Cambridge CB2 1QP, UK
R. Bensted-Smith
Affiliation:
Department of Pure and Applied Biology, Imperial College of Science and Technology, Prince Consort Road, London, UK
A. Capron
Affiliation:
Centre d'Immunologie et de Biologie Parasitaire, Institut Pasteur, Lille, FR
M. Capron
Affiliation:
Centre d'Immunologie et de Biologie Parasitaire, Institut Pasteur, Lille, FR
P. R. Dalton
Affiliation:
Division of Vector-Borne Diseases, Ministry of Health, Nairobi, KE
D. W. Dunne
Affiliation:
Department of Pathology, Tennis Court Road, Cambridge CB2 1QP, UK
J. M. Grzych
Affiliation:
Centre d'Immunologie et de Biologie Parasitaire, Institut Pasteur, Lille, FR
H. C. Kariuki
Affiliation:
Division of Vector-Borne Diseases, Ministry of Health, Nairobi, KE
J. Khalife
Affiliation:
Centre d'Immunologie et de Biologie Parasitaire, Institut Pasteur, Lille, FR
D. Koech
Affiliation:
Kenya Medical Research Institute, Nairobi, KE
M. Mugambi
Affiliation:
Kenya Medical Research Institute, Nairobi, KE
J. H. Ouma
Affiliation:
Division of Vector-Borne Diseases, Ministry of Health, Nairobi, KE
T. K. Arap Siongok
Affiliation:
Division of Disease Control and Research, Ministry of Health, Nairobi, KE
R. F. Sturrock
Affiliation:
London School of Hygiene and Tropical Medicine, Keppel Street, London, UK
*
*Reprint requests: Dr A. E. Butterworth, Department of Pathology, Tennis Court Road, Cambridge CB2 IQP, UK.

Summary

A total of 129 children were treated for Schistosoma mansoni infections, and followed for intensity of reinfection at 3-monthly intervals over a 21-month period. Blood samples were taken before treatment and at 5 weeks and 6, 12 and 18 months after treatment. This paper presents a statistical analysis of the relationship between various immune responses and subsequent reinfection. Responses analysed were: blood eosinophil levels; IgE antibodies against schistosomulum antigens; IgG antibodies mediating eosinophil-dependent killing of schistosomula; antibodies inhibiting the binding to schistosomulum antigens of two rat monoclonal antibodies that also recognize egg antigens; the levels of anti-adult worm and of anti-egg (total, IgM and IgG) antibodies; and IgM anti-schistosomulum antibodies. Results for each assay were well correlated for each of the five separate blood samples. None of the assays were predictive of resistance to reinfection, but susceptibility to reinfection was strongly correlated with results in the preceding blood samples for total anti-egg antibodies and the inhibition of binding of one of the two monoclonal antibodies. Further analysis also revealed a correlation between reinfection intensities and both IgM anti-schistosomulum antibodies and IgM and IgG anti-egg antibodies. These results are consistent with the hypothesis that early infections elicit the development, in response to egg antigens, of antibodies that block immune mechanisms directed against schistosomula. Blocking antibodies may be IgM, but might also be of an ineffective IgG isotype. The existence of such antibodies in young children would explain the slow development of immunity in the face of a range of detectable, potentially protective immune responses.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1987

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References

Auriault, C., Damonneville, M., Verwabrde, C., Pierce, R., Joseph, M., Capron, M. & Capron, A. (1984). Rat IgE directed against schistosomula-released products is cytotoxic for Schistosoma mansoni schistosomula in vitro. European Journal of Immunology 14, 132–8.CrossRefGoogle ScholarPubMed
Bensted-Smith, R., Anderson, R. M., Butterworth, A. E., Dalton, P. R., Kariuki, H. C., Koech, D., Mugambi, M., Ouma, J. H., Arap Siongok, T. K. & Sturrock, R. F. (1986). Evidence for predisposition of individual patients to reinfection with Schistosoma mansoni after treatment. Transactions of the Royal Society of Tropical Medicine and Hygiene (in the Press).Google Scholar
Bickle, Q. D., Taylor, M. G., Doenhoff, M. J. & Nelson, G. S. (1979). Immunization of mice with gamma-irradiated intramuscularly injected schistosomula of Schistosoma mansoni. Parasitology 79, 209–22.CrossRefGoogle ScholarPubMed
Butterworth, A. E., Capron, M., Cordingley, J. S., Dalton, P. R., Dunne, D. W., Kariuki, H. C., Koech, D., Mugambi, M., Ouma, J. H., Prentice, M. A., Richardson, B. A., Arap Siongok, T. K., Sturrock, R. F. & Taylor, D. W. (1985). Immunity after treatment of human schistosomiasis mansoni. II. Identification of resistant individuals, and analysis of their immune responses. Transactions of the Royal Society of Tropical Medicine and Hygiene 79, 393408.CrossRefGoogle ScholarPubMed
Butterworth, A. E., Dalton, P. R., Dunne, D. W., Mugambi, M., Ouma, J. H., Richardson, B. A., Arap Siongok, T. K. & Sturrock, R. F. (1984). Immunity after treatment of human schistosomiasis mansoni. I. Study design, pretreatment observations and the results of treatment. Transactions of the Royal Society of Tropical Medicine and Hygiene 78, 108–23.CrossRefGoogle ScholarPubMed
Capron, A., Capron, M. & Dessaint, J.-P. (1980). ADCC as primary mechanisms of defence against metazoan parasites. In Immunology 80: Progress in Immunology IV (ed. Fougereau, M. and Dausset, J.), pp. 782–93. New York: Academic Press.Google Scholar
Dalton, P. R. & Pole, D. (1978). Water contact patterns in relation to Schistosoma haematobium infection. Bulletin of the World Health Organization 56, 417–26.Google ScholarPubMed
Dunne, D. W., Bickle, Q. D., Butterworth, A. E. & Richardson, B. A. (1987). The blocking of human antibody-dependent, eosinophil-mediated killing of Schistosoma mansoni schistosomula by monoclonal antibodies which cross react with a polysaccharide-containing egg antigen. Parasitology 94,Google ScholarPubMed
Grzych, J. M., Capron, M., Bazin, H. & Capron, A. (1982). In vitro and in vivo effector function of rat IgG2a monoclonal anti-Schistosoma mansoni antibodies. Journal of Immunology 129, 2739–43.CrossRefGoogle Scholar
Grzych, J. M., Capron, M., Dissous, C. & Capron, A. (1984). Blocking activity of rat monoclonal antibodies in experimental schistosomiasis. Journal of Immunology 133, 9981004.CrossRefGoogle ScholarPubMed
Grzych, J. M., Capron, M., Lambert, P. H., Dissous, C, Torres, S. & Capron, A. (1985). An anti-idiotype vaccine against experimental schistosomiasis. Nature, London 316, 74–6.Google ScholarPubMed
Hagan, P., Wilkins, H. A., Blumenthal, U. J., Hayes, R. J. & Greenwood, B. M. (1985). Eosinophilia and resistance to Schistosoma haematobium in man. Parasite Immunology 7, 625–32.CrossRefGoogle ScholarPubMed
Hsü, S. Y. L., Hsü, H. F. & Osborne, J. W. (1969). Immunization of rhesus monkeys against schistosome infection by cercariae exposed to high doses of X-irradiation. Proceedings of the Society for Experimental Biology and Medicine 131, 1146–9.CrossRefGoogle Scholar
Iskander, R., Das, P. K. & Aalbeerse, R. C. (1981). IgG4 antibodies in Egyptian patients with schistosomiasis. International Archives of Allergy and Applied Immunology 66, 200–7.CrossRefGoogle ScholarPubMed
Khalife, J., Capron, M., Capron, A., Grzych, J. M., Butterworth, A. E., Dunne, D. W. & Ouma, J. H. (1986). Immunity in human schistosomiasis mansoni. Regulation of protective immune mechanisms by IgM blocking antibodies. Journal of Experimental Medicine, (in the Press).CrossRefGoogle ScholarPubMed
McLaren, M. L., Draper, C. C., Roberts, R. M., Minter-Goedbloed, E., Lighthart, G. S., Teesdale, C. H., Amin, M. A., Omer, A. H. S., Bartlett, A. & Voller, A. (1978). Studies on the enzyme-linked immunosorbent assay (ELISA) test for Schistosoma mansoni infection. Annals of Tropical Medicine and Parasitology 72, 243–53.CrossRefGoogle Scholar
McLaren, M. L., Lillywhite, J. E., Dunne, D. W. & Doenhoff, M. J. (1981). Serodiagnosis of human Schistosoma mansoni infections: enhanced sensitivity and specificity in ELISA using a fraction containing S. mansoni egg antigens ω1 and α1. Transactions of the Royal Society of Tropical Medicine and Hygiene 75, 72–9.CrossRefGoogle Scholar
Minard, P., Dean, D. A., Jacobson, R. H., Vannier, W. E. & Murrell, K. D. (1978). Immunization of mice with Cobalt-60 irradiated Schistosoma mansoni cercariae. American Journal of Tropical Medicine and Hygiene 27, 7693.Google ScholarPubMed
Pierce, R. J., Verwaerde, C., Damonneville, M., Lepresle, T. & Capron, A. (1983). Allergens of Schistosoma mansoni. I. Comparison of the IgE response in human and experimental infections towards characterized allergens from adult worm products. International Archives of Allergy and Applied Immunology 72, 219–26.CrossRefGoogle ScholarPubMed
Siegel, S. (1956). Non-parametric Statistics. New York: McGraw-Hill.Google Scholar
Smithers, S. R. & Terry, R. J. (1965). Naturally-acquired resistance to experimental infections of Schistosoma mansoni in the rhesus monkey (Macaca mulatta). Parasitology 55, 701–10.CrossRefGoogle ScholarPubMed
Sturrock, R. F., Bensted-Smith, R., Butterworth, A. E., Dalton, P. R., Kariuki, H. C., Koech, D., Mugambi, M., Ouma, J. H. & Arap Siongok, T. K. (1986). Immunity after treatment of human schistosomiasis mansoni. III. Long-term effects of treatment and retreatment. Transactions of the Royal Society of Tropical Medicine and Hygiene (in the Press).Google Scholar
Sturrock, R. F., Kimani, R., Cottrell, B. J., Butterworth, A. E., Seitz, H. M., Siongok, T. K. & Houba, V. (1983). Observations on possible immunity to reinfection among Kenyan schoolchildren after treatment for Schistosoma mansoni. Transactions of the Royal Society of Tropical Medicine and Hygiene 77, 363–71.CrossRefGoogle ScholarPubMed
Taylor, M. G., Nelson, G. S., Smith, M. & Andrews, B. J. (1973). Studies on heterologous immunity in schistosomiasis. 7. Observations on the development of acquired homologous and heterologous immunity to Schistosoma mansoni infections in baboons. Bulletin of the World Health Organization 49, 5766.Google ScholarPubMed
Vadas, M. A., David, J. R., Butterworth, A. E., Pisani, N. & Siongok, T. A. (1979). A new method for the purification of human eosinophils and neutrophils, and a comparison of the ability of these cells to damage schistosumula of Schistosoma mansoni. Journal of Immunology 122, 1228–36.CrossRefGoogle Scholar
Warren, K. S. (1973). Regulation of the prevalence and intensity of schistosomiasis in man. Immunology or ecology? Journal of Infectious Diseases 127, 595609.CrossRefGoogle ScholarPubMed