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Studies on the sex ratio of worms in schistosome infections

Published online by Cambridge University Press:  06 April 2009

G. F. Mitchell
Affiliation:
The Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria 3050, Australia
E. G. Garcia
Affiliation:
Department of Parasitology, College of Public Health, University of the Philippines Manila, Manila 1000, Philippines
S. M. Wood
Affiliation:
The Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria 3050, Australia
R. Diasanta
Affiliation:
Department of Parasitology, College of Public Health, University of the Philippines Manila, Manila 1000, Philippines
R. Almonte
Affiliation:
Department of Parasitology, College of Public Health, University of the Philippines Manila, Manila 1000, Philippines
E. Calica
Affiliation:
Department of Parasitology, College of Public Health, University of the Philippines Manila, Manila 1000, Philippines
K. M. Davern
Affiliation:
The Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria 3050, Australia
W. U. Tiu
Affiliation:
Department of Parasitology, College of Public Health, University of the Philippines Manila, Manila 1000, Philippines

Summary

Sex ratios of adult schistosomes in mice are almost invariably different from 1·0 and are biased towards males. The bias applies to wild rats infected with Schistosoma japonicum and trapped in an endemic area of the Philippines (male: female ratio = 1·7). It also applies to cercariae of snails collected in such areas and assessed by infection of laboratory mice using cercariae from individual snails (male: female ratio may approach 6·0). Experiments were designed to determine if duration of infection in the mammalian host was a factor that influenced the sex ratio of miracidia used for infecting snails and subsequently mice. BALB/c and C57BL/6 mice were infected with 100 cercariae of S. mansoni, and liver eggs harvested at early and late time points for infection of snails and production of cercariae. Two phenomena were demonstrated: firstly, a more pronounced male bias when eggs were harvested late compared with early in infection; secondly, a reduced apparent hatchability of eggs in BALB/c compared with C57BL/6 livers. The possibility is raised by the data that female miracidia within eggs of chronically infected individuals may be more prone to immune damage than male miracidia with important epidemiological consequences.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1990

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References

REFERENCES

Bickle, Q., Bain, J., Mcgregory, A. & Doenhoff, M. (1979). Factors affecting the acquisition of resistance against Schistosoma mansoni in the mouse. III. The failure of primary infection with cercariae of one sex to induce resistance to reinfection. Transactions of the Royal Society of Tropical Medicine and Hygiene 73, 3741.CrossRefGoogle ScholarPubMed
Blagg, E., Schlagel, E. L., Mansour, N. S. & Khalag, G. I. (1955). A new concentration technic for the demonstration of protozoan and helminth eggs in the feces. American Journal of Tropical Medicine 4, 23–8.Google Scholar
Blas, B. L. (1970). Studies on egg-quantitation in the stools. I. Evaluation of the merthiolate-iodine-formalin concentration technique. Journal of the Philippine Medical Association 48, 59.Google Scholar
Butterworth, A. E., Bensted-smith, R., Capron, A., Capron, M., Dalton, P. R., Dunne, D. W., Grzych, J. M., Kariuki, H. C., Khalife, J., Koech, D., Mugabi, M., Ouma, J. H., Arap-Siongkok, T. K. & Sturrock, R. F. (1987). Immunity in human schistosomiasis mansoni: prevention by blocking antibodies of the expression of immunity in young children. Parasitology 94, 281300.CrossRefGoogle ScholarPubMed
Cheever, A. W., Duvall, R. H., Hallack, T. A. Jr, Minker, R. G., Malley, J. D. & Malley, K. G. (1987). Variation of hepatic fibrosis and granuloma size among mouse strains infected with Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 37, 8597.CrossRefGoogle ScholarPubMed
Colley, D. G. & Freeman, G. L. Jr (1981). Differences in adult Schistosoma mansoni worm burden requirements for the establishment of resistance to reinfection in inbred mice. I. CBA/J and C57BL/6 mice. American Journal of Tropical Medicine and Hygiene 29, 1279–85.CrossRefGoogle Scholar
Dean, D. A., Minard, P., Stirewalt, M. A., Vannier, W. E. & Murrell, K. D. (1978). Resistance of mice to secondary infection with Schistosoma mansoni. I. Comparison of bisexual and unisexual initial infections. American Journal of Tropical Medicine and Hygiene 27, 951–6.CrossRefGoogle ScholarPubMed
Evans, A. s. & Stirewalt, M. A. (1951). Variations in infectivity of cercariae of Schistosoma mansoni. Experimental Parasitology 1, 1933.CrossRefGoogle Scholar
Garcia, E. G., Cabrera, B. D., Cristi, Z. A. & Silan, R. B. (1968). Evaluation of some laboratory procedures for the diagnosis of schistosomiasis japonica. Acta Medica Philippina 4, 130–6.Google Scholar
Garcia, E. G. & Mitchell, G. F. (1982). Vaccination against severe hepato-splenic disease in schistosomiasis japonica: an hypothesis. Acta Medica Philippina 18, 107–12.Google Scholar
Garcia, E. G., Mitchell, G. F., Espinas, F. J. M., Tapales, F. P., Quicho, L. P. & Tiu, W. U. (1984). Further studies on resistance to reinfection with Schistosoma japonicum in mice. Asian Pacific Journal of Allergy and Immunology 2, 2731.Google ScholarPubMed
Garcia, E. G., Mitchell, G. F., Rivera, P. T., Evardome, R. R., Almonte, R. E. & Tiu, W. U. (1987). Evidence of anti-embryonation immunity and egg destruction in mice sensitized with immature eggs of Schistosoma japonicum. Asian Pacific Journal of Allergy and Immunology 5, 137–41.Google ScholarPubMed
Garcia, E. G. & Mitchell, G. F. (1987). Immunology of resistance to infection and disease in schistosomiasis japonica. In Immunology, Immunopathology and Immunoprophylaxis of Parasitic Infections, Vol. II (ed. Soulsby, E. J. L.), pp. 3548. Boca Raton, Florida: CRC Press.Google Scholar
Garcia, E. G., Tapales, F. P., Valdez, C. A., Mitchell, G. F. & Tiu, W. U. (1981). Attempts to standardize the circumoval precipitin test (COPT) for schistosomiasis japonica. Southeast Asian Journal of Tropical Medicine and Public Health 12, 384–94.Google ScholarPubMed
Grossman, A. I., Short, R. B. & Cain, G. D. (1981). Karyotype evolution and sex chromosome differentiation in schistosomes (Trematoda, Schistosomatidae). Chromosana 84, 413–30.CrossRefGoogle ScholarPubMed
Jueco, N. L. (1970). Evaluation of the direct fecal smear, Kato thick smear technique as diagnostic tools for common parasitic infection. Acta Medica Philippina 12, 62–6.Google Scholar
Liberatos, J. D. (1987). Schistosoma mansoni: male-biased sex ratios in snails and mice. Experimental Parasitology 64, 165–77.CrossRefGoogle ScholarPubMed
Menzel, M. Y. & Short, R. B. (1960). Pachytene chromosomes in three species of schistosomes: sex and autosomal bivalents in males and females. Journal of Heredity 51, 212.CrossRefGoogle Scholar
Mitchell, G. F. (1989). Portal system peculiarities may contribute to resistance in 129/J mice against schistosomiasis. Parasite Immunology 11, 713–17.CrossRefGoogle Scholar
Mitchell, G. F., Wright, M. D., Wood, S. M. & Tiu, W. U. (1990). Further studies on variable resistance of 129/J and C57BL/6 mice to infection with Schistosoma japonicum and Schistosoma mansoni. Parasite Immunology (in the Press).CrossRefGoogle ScholarPubMed
Mitchell, G. F. (1990). Immunopathology of schistosomiasis. In Reviews in Medical Microbiology (ed. Williams, R. J.). London: Churchill Livingstone (in the Press).Google Scholar
Mitchell, G. F., Garcia, E. G., Anders, R. F., Valdez, C. A., Tapales, F. P. & Cruise, K. M. (1981). Schistosoma japonicum: infection characteristics in mice of various strains and a difference in the response to eggs. International Journal for Parasitology 11, 267–76.CrossRefGoogle Scholar
Mitchell, G. F., Garcia, E. G., Cruise, K. M., Tiu, W. U. & Hocking, R. E. (1982). Lung granulomatous hypersensitivity to eggs of Schistosoma japonicum in mice analysed by a radioisotopic assay and effects of hybridoma (idiotype) sensitization. Australian Journal of Experimental Biology and Medical Science 60, 401–16.CrossRefGoogle ScholarPubMed
Moloney, N. A., Webbe, G. & Luty, A. J. (1984). Factors affecting the acquisition of resistance to Schistosoma japonicum in the mouse. I. The correlation between egg deposition and worm elimination. Parasitology 89, 345–60.CrossRefGoogle ScholarPubMed
Mott, K. E., Dixon, H., Carter, C. E., Garcia, E., Ishii, A., Matsuda, G., Mitchell, G., Owashi, M., Tanaka, H. & Tsang, V. C. (1986). Collaborative study on antigens for immunodiagnosis of Schistosoma japonicum infection. Bulletin of the World Health Organization 65, 233–44.Google Scholar
Olveda, R. M. & Domingo, E. O. (1987). Schistosomiasis japonica. Baillière's Clinics in Tropical Medicine and Communicable Diseases 2, 387417.Google Scholar
Pesigan, T. P., Farooq, M., Hairston, N. G., Jauregui, J. J., Garcia, E. G., Santos, A. T., Santos, B. C. & Besa, A. A. (1958). Studies on Schistosoma japonicum in the Philippines. I. General consideration and epidemiology. Bulletin of the World Health Organization 18, 345455.Google ScholarPubMed
Sadun, E. H. (1963). Immunization in schistosomiasis by previous exposure to homologous and heterologous cercariae by inoculation of preparations from schistosomes and by exposure to irradiated cercariae. Annals of the New York Academy of Sciences 113, 418–39.CrossRefGoogle ScholarPubMed
Spotila, L. D., Rekosh, D. M., Boucher, J. M. & Loverde, P. T. (1987). A cloned DNA probe identifies the sex of Schistosoma mansoni cercariae. Molecular and Biochemical Parasitology 26, 1720.CrossRefGoogle ScholarPubMed
Stavitsky, A. B. (1987). Immune regulation of schistosomiasis japonica. Immunology Today 8, 228–33.CrossRefGoogle ScholarPubMed
Vogel, H. & Minning, W. (1953). The acquired resistance of Macacus rhesus to Schistosoma japonicum. Zeitschrift für Tropenmedizin und Parasitologie 4, 418505.Google ScholarPubMed
Walker, T. K., Rollinson, D. & Simpson, A. J. G. (1989). A DNA probe from Schistosoma mansoni allows rapid determination of the sex of larval parasites. Molecular and Biochemical Parasitology 33, 93100.CrossRefGoogle ScholarPubMed
Warren, K. S. (1982). The secret of immunopathogenesis of schistosomiasis: in vivo models. Immunological Reviews 61, 189213.CrossRefGoogle ScholarPubMed
Webster, P., Mansour, T. E. & Breber, D. (1989). Isolation of a female-specific, highly repetitive Schistosoma mansoni DNA probe and its use in an assay of cercarial sex. Molecular and Biochemical Parasitology 36, 217–22.CrossRefGoogle Scholar
Wright, M. D., Tiu, W. U., Wood, S. M., Walker, J. C., Garcia, E. G. & Mitchell, G. F. (1988). Schistosoma mansoni and S. japonicum worm numbers in 129/J mice of two types and dominance of susceptibility in F1 hybrids. Journal of Parasitology 74, 618–22.CrossRefGoogle ScholarPubMed
Yi, X., Omer-ali, P., Kelly, C, Simpson, A. J. G. & Smithers, S. R. (1986). IgM antibodies recognizing carbohydrate epitopes shared between schistosomula and miracidia of Schistosoma mansoni which block in vitro killing. Journal of Immunology 137, 3946–54.CrossRefGoogle ScholarPubMed
Yogore, M. G. Jr., Lewert, R. M. & Blas, B. L. (1983). Seroepidemiology of schistosomiasis japonica in the Philippines. I. Underestimation by stool examination of the prevalence in school children. American Journal of Tropical Medicine and Hygiene 23, 1322–5.CrossRefGoogle Scholar