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Bulletin of the World Health Organization logoLink to Bulletin of the World Health Organization
. 1974;51(6):553–595.

Immunology of schistosomiasis*

PMCID: PMC2366272  PMID: 4219757

Abstract

This Memorandum, after summarizing the life cycle of the different species of human schistosome, reviews the present knowledge of the immunology of schistosomiasis. Each stage of the parasite contains antigen that may stimulate an immune response. However, at the moment there are no accepted serological in vitro tests that correlate with protection; this develops only after the host has experienced a living infection, which suggests that the stimulation of immunity is due to some metabolic process involving the release of protective antigen. The adult worm, however, seems to be able to escape the immune mechanism of the host. Specific antigens are also released by the eggs, and the immune response against these antigens seems to cause granuloma formation around the egg itself. The granuloma is the main lesion found in schistosomiasis. Evidence for protective immunity in experimental animals and man is reviewed, together with the possible mechanism by which the adult worm escapes the immune response of the host. A review of methods used for the diagnosis of schistosomiasis and a list of recommendations for further research are also included.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. ANDRADE Z. A. WARREN KS: MILD PROLONGED SCHISTOSOMIASIS IN MICE: ALTERATIONS IN HOST RESPONSE WITH TIME AND THE DEVELOPMENT OF PORTAL FIBROSIS. Trans R Soc Trop Med Hyg. 1964 Jan;58:53–57. doi: 10.1016/0035-9203(64)90068-9. [DOI] [PubMed] [Google Scholar]
  2. Allen A. V., Ridley D. S. Further observations on the formol-ether concentration technique for faecal parasites. J Clin Pathol. 1970 Sep;23(6):545–546. doi: 10.1136/jcp.23.6.545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Amin M. A., Nelson G. S., Soud M. F. Studies on heterologous immunity in schistosomiasis. 2. Heterologous schistosome immunity in rhesus monkeys. Bull World Health Organ. 1968;38(1):19–27. [PMC free article] [PubMed] [Google Scholar]
  4. Andrade Z. A., Abreu W. N. Follicular lymphoma of the spleen in patients with hepatosplenic Schistosomiasis mansoni. Am J Trop Med Hyg. 1971 Mar;20(2):237–243. doi: 10.4269/ajtmh.1971.20.237. [DOI] [PubMed] [Google Scholar]
  5. Andrade Z. A., Andrade S. G., Sadigursky M. Renal changes in patients with hepatosplenic schistosomiasis. Am J Trop Med Hyg. 1971 Jan;20(1):77–83. doi: 10.4269/ajtmh.1971.20.77. [DOI] [PubMed] [Google Scholar]
  6. BELL D. R. A NEW METHOD FOR COUNTING SCHISTOSOMA MANSONI EGGS IN FAECES: WITH SPECIAL REFERENCE TO THERAPEUTIC TRIALS. Bull World Health Organ. 1963;29:525–530. [PMC free article] [PubMed] [Google Scholar]
  7. BLAGG W., SCHLOEGEL E. L., MANSOUR N. S., KHALAF G. I. A new concentration technic for the demonstration of protozoa and helminth eggs in feces. Am J Trop Med Hyg. 1955 Jan;4(1):23–28. doi: 10.4269/ajtmh.1955.4.23. [DOI] [PubMed] [Google Scholar]
  8. Bawden M. P., Weller T. H. Schistosoma mansoni circulating antigen: detection by complement fixation in sera from infected hamsters and mice. Am J Trop Med Hyg. 1974 Nov;23(6):1077–1084. doi: 10.4269/ajtmh.1974.23.1077. [DOI] [PubMed] [Google Scholar]
  9. Beer R. J. A rapid technique for the concentration and collection of helminth eggs from large quantities of faeces. Parasitology. 1972 Oct;65(2):343–350. doi: 10.1017/s0031182000045121. [DOI] [PubMed] [Google Scholar]
  10. Berggren W. L., Weller T. H. Immunoelectrophoretic demonstration of specific circulating antigen in animals infected with Schistosoma mansoni. Am J Trop Med Hyg. 1967 Sep;16(5):606–612. doi: 10.4269/ajtmh.1967.16.606. [DOI] [PubMed] [Google Scholar]
  11. Boros D. L., Pelley R. P., Warren K. S. Spontaneous modulation of granulomatous hypersensitivity in schistosomiasis mansoni. J Immunol. 1975 May;114(5):1437–1441. [PubMed] [Google Scholar]
  12. Boros D. L., Warren K. S. Delayed hypersensitivity-type granuloma formation and dermal reaction induced and elicited by a soluble factor isolated from Schistosoma mansoni eggs. J Exp Med. 1970 Sep 1;132(3):488–507. doi: 10.1084/jem.132.3.488. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Boros D. L., Warren K. S. Specific granulomatous hypersensitivity elicited by bentonite particles coated with soluble antigens from schistosome eggs and turcle bacilli. Nature. 1971 Jan 15;229(5281):200–201. doi: 10.1038/229200a0. [DOI] [PubMed] [Google Scholar]
  14. Bradley D. J., McCullough F. S. Egg output stability and the epidemiology of Schistosoma haematobium. II. An analysis of the epidemiology of endemic S. haematobium. Trans R Soc Trop Med Hyg. 1973;67(4):491–500. doi: 10.1016/0035-9203(73)90080-1. [DOI] [PubMed] [Google Scholar]
  15. Bradley D. J. The measurement of bilharziasis prevalence and schistosomal egg output. Aims and techniques, with an account of a field method. Bull World Health Organ. 1965;33(4):503–508. [PMC free article] [PubMed] [Google Scholar]
  16. Buchanan R. D., Fine D. P., Colley D. G. Schistosoma mansoni infection in mice depleted of thymus-dependent lymphocytes. II. Pathology and altered pathogenesis. Am J Pathol. 1973 May;71(2):207–218. [PMC free article] [PubMed] [Google Scholar]
  17. Buck A. A., Anderson R. I. Validation of the complement fixation and slide flocculation tests for schistosomiasis. Geographic variations of test capacities. Am J Epidemiol. 1972 Sep;96(3):205–214. doi: 10.1093/oxfordjournals.aje.a121449. [DOI] [PubMed] [Google Scholar]
  18. Butterworth A. E., Sturrock R. F., Houba V., Rees P. H. Antibody-dependent cell-mediated damage to schistosomula in vitro. Nature. 1974 Dec 6;252(5483):503–505. doi: 10.1038/252503a0. [DOI] [PubMed] [Google Scholar]
  19. Capron A., Biguet J., Rose F., Vernes A. Les antigènes de Schistosoma mansoni. II. Etude immunoélectrophorétique comparée de divers stades larvaires et des adults des deux sexes. Aspects immunologiques des relations hote-parasite de la cervaire et de l'adulte de S. mansoni. Ann Inst Pasteur (Paris) 1965 Nov;109(5):798–810. [PubMed] [Google Scholar]
  20. Capron A., Biguet J., Tran Van Ky P., Moschetto Y. Immunological studies in various types of schistosomiasis. Ann N Y Acad Sci. 1969 Oct 6;160(2):863–879. doi: 10.1111/j.1749-6632.1969.tb15906.x. [DOI] [PubMed] [Google Scholar]
  21. Capron A., Biguet J., Vernes A., Afchain D. Structure antigénique des helminthes. Aspects immunologiques des relations hote-parasite. Pathol Biol. 1968 Feb;16(3):121–138. [PubMed] [Google Scholar]
  22. Capron A., Capron M., Dupas H., Bout D., Petitprez A. Etude in vitro des phénomènes immunologiques dans la schistosomiase humaine et expérimentale. I. Etude comparative in vitro de l'activité léthale d'immunsérums sur les formes immatures et sur les adultes de Schistosoma mansoni. Int J Parasitol. 1974 Dec;4(6):613–623. doi: 10.1016/0020-7519(74)90026-5. [DOI] [PubMed] [Google Scholar]
  23. Capron A., Dessaint J. P., Capron M., Bazin H. Specific IgE antibodies in immune adherence of normal macrophages to Schistosoma mansoni schistosomules. Nature. 1975 Feb 6;253(5491):474–475. doi: 10.1038/253474a0. [DOI] [PubMed] [Google Scholar]
  24. Cavallo T., Galvanek E. G., Ward P. A., von Lichtenberg F. The nephropathy of experimental hepatosplenic schistosomiasis. Am J Pathol. 1974 Sep;76(3):433–450. [PMC free article] [PubMed] [Google Scholar]
  25. Clegg J. A., Smithers S. R., Terry R. J. "Host" antigens associated with schistosomes: observations on their attachment and their nature. Parasitology. 1970 Aug;61(1):87–94. doi: 10.1017/s0031182000040889. [DOI] [PubMed] [Google Scholar]
  26. Clegg J. A., Smithers S. R., Terry R. J. Acquisition of human antigens by Schistosoma mansoni during cultivation in vitro. Nature. 1971 Aug 27;232(5313):653–654. doi: 10.1038/232653a0. [DOI] [PubMed] [Google Scholar]
  27. Clegg J. A., Smithers S. R., Terry R. J. Concomitant immunity and host antigens associated with schistosomiasis. Int J Parasitol. 1971 May;1(1):43–49. doi: 10.1016/0020-7519(71)90045-2. [DOI] [PubMed] [Google Scholar]
  28. Clegg J. A., Smithers S. R. The effects of immune rhesus monkey serum on schistosomula of Schistosoma mansoni during cultivation in vitro. Int J Parasitol. 1972 Mar;2(1):79–98. doi: 10.1016/0020-7519(72)90036-7. [DOI] [PubMed] [Google Scholar]
  29. Colley D. G. Eosinophils and immune mechanisms. Eosinophil stimulation promoter (ESP): a lymphokine induced by specific antigen or phytohemagglutinin. J Immunol. 1973 May;110(5):1419–1423. [PubMed] [Google Scholar]
  30. Colley D. G. Schistosoma mansoni: eosinophilia and the development of lymphocyte blastogenesis in response to soluble egg antigen in inbred mice. Exp Parasitol. 1972 Dec;32(3):520–526. doi: 10.1016/0014-4894(72)90070-7. [DOI] [PubMed] [Google Scholar]
  31. Damian R. T., Greene N. D., Fitzgerald K. Schistosomiasis mansoni in baboons. The effect of surgical transfer of adult Schistosoma mansoni upon subsequent challenge infection. Am J Trop Med Hyg. 1972 Nov;21(6):951–958. [PubMed] [Google Scholar]
  32. Damian R. T., Greene N. D., Hubbard W. J. Occurrence of mouse 2 -macroglobulin antigenic determinants on Schistosoma mansoni adults, with evidence on their nature. J Parasitol. 1973 Feb;59(1):64–73. [PubMed] [Google Scholar]
  33. Davis A. Comparative trials of antimonial drugs in urinary schistosomiasis. Bull World Health Organ. 1968;38(2):197–227. [PMC free article] [PubMed] [Google Scholar]
  34. Dean D. A., Wistar R., Murrell K. D. Combined in vitro effects of rat antibody and neutrophilic leukocytes on schistosomula of Schistosoma mansoni. Am J Trop Med Hyg. 1974 May;23(3):420–428. doi: 10.4269/ajtmh.1974.23.420. [DOI] [PubMed] [Google Scholar]
  35. Deelder A. M., Ploem J. S. An immunofluorescence reaction for Schistosoma manosoni using the defined antigen substrate spheres (DASS) system. J Immunol Methods. 1974 Mar;4(2):239–251. doi: 10.1016/0022-1759(74)90067-2. [DOI] [PubMed] [Google Scholar]
  36. Domingo E. O., Warren K. S. Endogenous desensitization: changing host granulomatou response to schistosome eggs at different stages of infection with schistosoma mansoni. Am J Pathol. 1968 Feb;52(2):369–379. [PMC free article] [PubMed] [Google Scholar]
  37. Engvall E., Perlmann P. Enzyme-linked immunosorbent assay, Elisa. 3. Quantitation of specific antibodies by enzyme-labeled anti-immunoglobulin in antigen-coated tubes. J Immunol. 1972 Jul;109(1):129–135. [PubMed] [Google Scholar]
  38. Erasmus D. A. A comparative study of the reproductive system of mature, immature and "unisexual" female Schistosoma mansoni. Parasitology. 1973 Oct;67(2):165–183. doi: 10.1017/s0031182000046394. [DOI] [PubMed] [Google Scholar]
  39. Eveland L. K., Hsü S. Y., Hsü H. F. Cross-immunity of Schistosoma japonicum, S. mansoni, and S. bovis in rhesus monkeys. J Parasitol. 1969 Apr;55(2):279–288. [PubMed] [Google Scholar]
  40. Fife E. H., Jr Advances in methodology for immunodiagnosis of parasitic diseases. Exp Parasitol. 1971 Aug;30(1):132–163. doi: 10.1016/0014-4894(71)90079-8. [DOI] [PubMed] [Google Scholar]
  41. Fine D. P., Buchanan R. D., Colley D. G. Schistosoma mansoni infection in mice depleted of thymus-dependent lymphocytes. I. Eosinophilia and immunologic responses to a schistosomal egg preparation. Am J Pathol. 1973 May;71(2):193–206. [PMC free article] [PubMed] [Google Scholar]
  42. GOTHE K. M. BEOBACHTUNGEN UEBER DIE IMMUNITAET BEI SCHISTOSOMA HAEMATOBIUM-INFEKTIONEN. Z Tropenmed Parasitol. 1963 Dec;14:512–518. [PubMed] [Google Scholar]
  43. GOTHE K. M. BEOBACHTUNGEN UEBER DIE IMMUNITAET BEI SCHISTOSOMA HAEMATOBIUM-INFEKTIONEN. Z Tropenmed Parasitol. 1963 Dec;14:512–518. [PubMed] [Google Scholar]
  44. Gold R., Rosen F. S., Weller T. H. A specific circulating antigen in hamsters infected with Schistosoma mansoni. Detection of antigen in serum and urine, and correlation between antigenic concentration and worm burden. Am J Trop Med Hyg. 1969 Jul;18(4):545–552. doi: 10.4269/ajtmh.1969.18.545. [DOI] [PubMed] [Google Scholar]
  45. Hang L. M., Boros D. L., Warren K. S. Induction of immunological hyporesponsiveness to granulomatous hypersensitivity in Schistosoma mansoni infection. J Infect Dis. 1974 Nov;130(5):515–522. doi: 10.1093/infdis/130.5.515. [DOI] [PubMed] [Google Scholar]
  46. Hillyer G. V. Deoxyribonucleic acid (DNA) and antibodies to DNA in the serum of hamsters and man infected with schistosomes. Proc Soc Exp Biol Med. 1971 Mar;136(3):880–883. doi: 10.3181/00379727-136-35386. [DOI] [PubMed] [Google Scholar]
  47. Hillyer G. V., Lewert R. M. Studies on renal pathology in hamsters infected with Schistosoma mansoni and S. japonicum. Am J Trop Med Hyg. 1974 May;23(3):404–411. doi: 10.4269/ajtmh.1974.23.404. [DOI] [PubMed] [Google Scholar]
  48. Hockley D. J., McLaren D. J. Schistosoma mansoni: changes in the outer membrane of the tegument during development from cercaria to adult worm. Int J Parasitol. 1973 Jan;3(1):13–25. doi: 10.1016/0020-7519(73)90004-0. [DOI] [PubMed] [Google Scholar]
  49. Jordan P., Cook J. A., Davis A. Letter: Schistosoma haematobium infection: immunity or concomitant immunity? Trans R Soc Trop Med Hyg. 1974;68(4):340–341. doi: 10.1016/0035-9203(74)90048-0. [DOI] [PubMed] [Google Scholar]
  50. Jordan P. Epidemiology and control of schistosomiasis. Br Med Bull. 1972 Jan;28(1):55–59. doi: 10.1093/oxfordjournals.bmb.a070894. [DOI] [PubMed] [Google Scholar]
  51. Jordan P., Von Lichtenberg F., Goatly K. D. Experimental schistosomiasis in primates in Tanzania. Preliminary observations on the susceptibility of the baboon Papio anubis to Schistosoma haematobium and Schistosoma mansoni. Bull World Health Organ. 1967;37(3):393–403. [PMC free article] [PubMed] [Google Scholar]
  52. KAGAN I. G., PELLEGRINO J. A critical review of immunological methods for the diagnosis of bilharziasis. Bull World Health Organ. 1961;25:611–674. [PMC free article] [PubMed] [Google Scholar]
  53. Kloetzel K., da Silva J. R. Schistosomiasis mansoni acquired in adulthood: behavior of egg counts and the intradermal test. Am J Trop Med Hyg. 1967 Mar;16(2):167–169. doi: 10.4269/ajtmh.1967.16.167. [DOI] [PubMed] [Google Scholar]
  54. Kusel J. R. Protein composition and protein synthesis in the surface membranes of Schistosoma mansoni. Parasitology. 1972 Aug;65(1):55–69. doi: 10.1017/s0031182000044231. [DOI] [PubMed] [Google Scholar]
  55. Kusel J. R. Studies on the surfaces of cercariae and schistosomula of Schistosoma mansoni. Parasitology. 1970 Aug;61(1):127–134. doi: 10.1017/s0031182000040920. [DOI] [PubMed] [Google Scholar]
  56. Maddison S. E., Geiger S. J., Botero B., Kagan I. G. Schistosoma mansoni infection in the rat. II. Effects of immunosuppression and serum and cell transfer on innate and acquired immunity. J Parasitol. 1970 Dec;56(6):1066–1073. [PubMed] [Google Scholar]
  57. Mahmoud A. A., Warren K. S., Boros D. I. Production of a rabbit antimouse eosinophil serum with no cross-reactivity to neutrophils. J Exp Med. 1973 Jun 1;137(6):1526–1531. doi: 10.1084/jem.137.6.1526. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Martin L. K., Beaver P. C. Evaluation of Kato thick-smear technique for quantitative diagnosis of helminth infections. Am J Trop Med Hyg. 1968 May;17(3):382–391. doi: 10.4269/ajtmh.1968.17.382. [DOI] [PubMed] [Google Scholar]
  59. Massound J., Nelson G. S. Studies on heterologous immunity in schistosomiasis. 6. Observations on cross-immunity to Ornithobilharzia turkestanicum, Schistosoma bovis, S. mansoni, and S. haematobium in mice, sheep, and cattle in Iran. Bull World Health Organ. 1972;47(5):591–600. [PMC free article] [PubMed] [Google Scholar]
  60. McLaren D. J., Clegg J. A., Smithers S. R. Acquisition of host antigens by young Schistosoma mansoni in mice: correlation with failure to bind antibody in vitro. Parasitology. 1975 Feb;70(1):67–75. doi: 10.1017/s0031182000048873. [DOI] [PubMed] [Google Scholar]
  61. Moriearty P. L., Lewert R. M. Delayed hypersensitivity in Ugandan schistosomiasis. I. Sensitivity, specificity, and immunological features of intradermal responses. Am J Trop Med Hyg. 1974 Mar;23(2):169–178. [PubMed] [Google Scholar]
  62. Murrell K. D., Vannier W. E., Ahmed A. Schistosoma mansoni: antigenic heterogeneity of excretions and secretions. Exp Parasitol. 1974 Oct;36(2):316–330. doi: 10.1016/0014-4894(74)90071-x. [DOI] [PubMed] [Google Scholar]
  63. NEWSOME J. Problems of fluke immunity: with special reference to schistosomiasis. Trans R Soc Trop Med Hyg. 1956 May;50(3):258–274. doi: 10.1016/0035-9203(56)90033-5. [DOI] [PubMed] [Google Scholar]
  64. Nash T. E. Localization of the circulating antigen within the gut of Schistosoma mansoni. Am J Trop Med Hyg. 1974 Nov;23(6):1085–1087. doi: 10.4269/ajtmh.1974.23.1085. [DOI] [PubMed] [Google Scholar]
  65. Nash T. E., Prescott B., Neva F. A. The characteristics of a circulating antigen in schistosomiasis. J Immunol. 1974 Apr;112(4):1500–1507. [PubMed] [Google Scholar]
  66. Nelson G. S., Amin M. A., Saoud M. F., Teesdale C. Studies on heterologous immunity in schistosomiasis. I. Heterologous schistosome immunity in mice. Bull World Health Organ. 1968;38(1):9–17. [PMC free article] [PubMed] [Google Scholar]
  67. Ogilvie B. M., Smithers S. R., Terry R. J. Reagin-like antibodies in experimental infections of Schistosoma mansoni and the passive transfer of resistance. Nature. 1966 Mar 19;209(5029):1221–1223. doi: 10.1038/2091221a0. [DOI] [PubMed] [Google Scholar]
  68. Ongom V. L., Bradley D. J. The epidemiology and consequences of Schistosoma mansoni infection in West Nile, Uganda. I. Field studies of a community at Panyagoro. Trans R Soc Trop Med Hyg. 1972;66(6):835–851. doi: 10.1016/0035-9203(72)90118-6. [DOI] [PubMed] [Google Scholar]
  69. Perez H., Clegg J. A., Smithers S. R. Acquired immunity to Schistosoma mansoni in the rat: measurement of immunity by the lung recovery technique. Parasitology. 1974 Dec;69(3):349–359. doi: 10.1017/s0031182000063046. [DOI] [PubMed] [Google Scholar]
  70. SADUN E. H., ANDERSON R. I., SCHOENBECHLER M. J. A plasma card test for rapid serodiagnosis of schistosomiasis (SPC). Proc Soc Exp Biol Med. 1963 Feb;112:280–283. doi: 10.3181/00379727-112-28016. [DOI] [PubMed] [Google Scholar]
  71. SAPERO J. J., LAWLESS D. K. The MIF stain-preservation technic for the identification of intestinal protozoa. Am J Trop Med Hyg. 1953 Jul;2(4):613–619. doi: 10.4269/ajtmh.1953.2.613. [DOI] [PubMed] [Google Scholar]
  72. Sadun E. H., Von Lichtenberg F., Bruce J. I. Susceptibility and comparative pathology of ten species of primates exposed to infection with Schistosoma mansoni. Am J Trop Med Hyg. 1966 Sep;15(5):705–718. doi: 10.4269/ajtmh.1966.15.705. [DOI] [PubMed] [Google Scholar]
  73. Sadun E. H., Von Lichtenberg F., Cheever A. W., Erickson D. G., Hickman R. L. Experimental infection with Schistosoma haematobium in chimpanzees. Am J Trop Med Hyg. 1970 May;19(3):427–458. doi: 10.4269/ajtmh.1970.19.427. [DOI] [PubMed] [Google Scholar]
  74. Sher A., Kusel J. R., Perez H., Clegg J. A. Partial isolation of a membrane antigen which induces the formation of antibodies lethal to schistosomes cultured in vitro. Clin Exp Immunol. 1974 Nov;18(3):357–369. [PMC free article] [PubMed] [Google Scholar]
  75. Sher A., Mackenzie P., Smithers S. R. Decreased recovery of invading parasites from the lungs as a parameter of acquired immunity to schistosomiasis in the mouse. J Infect Dis. 1974 Dec;130(6):626–633. doi: 10.1093/infdis/130.6.626. [DOI] [PubMed] [Google Scholar]
  76. Smithers S. R., Terry R. J. Immunity in schistosomiasis. Ann N Y Acad Sci. 1969 Oct 6;160(2):826–840. doi: 10.1111/j.1749-6632.1969.tb15904.x. [DOI] [PubMed] [Google Scholar]
  77. Smithers S. R., Terry R. J. Resistance to experimental infection with Schistosoma mansoni in rhesus monkeys induced by the transfer of adult worms. Trans R Soc Trop Med Hyg. 1967;61(4):517–533. doi: 10.1016/0035-9203(67)90102-2. [DOI] [PubMed] [Google Scholar]
  78. Smithers S. R., Terry R. J. The immunology of schistosomiasis. Adv Parasitol. 1969;7:41–93. doi: 10.1016/s0065-308x(08)60434-0. [DOI] [PubMed] [Google Scholar]
  79. Taylor M. G., Nelson G. S., Smith M., Andrews B. J. Studies on heterologous immunity in schistosomiasis. 7. Observations on the development of acquired homologous and heterologous immunity to Schistosoma mansoni in baboons. Bull World Health Organ. 1973;49(1):57–65. [PMC free article] [PubMed] [Google Scholar]
  80. Vernes A., Camus D., Capron A., Capron M., Gentilini M. Les phénomènes d'hypersensibilité au cours des schistosomiases humaines a "Schistosoma mansoni" et "Schistosoma haematobium". I. Etude de l'hypersensibilité retardée in vivo par intradermo-réaction et in vitro par le test de migration leucocytaire et un test mixte dérivé du test d'inhibition de l'étalement des macrophages. Pathol Biol (Paris) 1973 Dec;21(10):1073–1078. [PubMed] [Google Scholar]
  81. Visser P. S., Pitchford R. J. A simple apparatus for rapid recovery of helminth eggs from excreta with special reference to Schistosoma mansoni. S Afr Med J. 1972 Sep 16;46(37):1344–1346. [PubMed] [Google Scholar]
  82. Von Lichtenberg F., Sadun E. H., Cheever A. W., Erickson D. G., Johnson A. J., Boyce H. W. Experimental infection with Schistosoma japonicum in chimpanzees. Am J Trop Med Hyg. 1971 Nov;20(6):850–893. doi: 10.4269/ajtmh.1971.20.850. [DOI] [PubMed] [Google Scholar]
  83. Warren K. S., Domingo E. O., Cowan R. B. Granuloma formation around schistosome eggs as a manifestation of delayed hypersensitivity. Am J Pathol. 1967 Nov;51(5):735–756. [PMC free article] [PubMed] [Google Scholar]
  84. Warren K. S., Kellermeyer R. W., Jordan P., Littell A. S., Cook J. A., Kagan I. G. Immunologic diagnosis of schistosomiasis. I. A controlled study of intradermal (immediate and delayed) and serologic tests in St. Lucians infected with Schistosoma mansoni and in uninfected St. Vincentians. Am J Trop Med Hyg. 1973 Mar;22(2):189–198. doi: 10.4269/ajtmh.1973.22.189. [DOI] [PubMed] [Google Scholar]
  85. Warren K. S. Regulation of the prevalence and intensity of schistosomiasis in man: immunology or ecology? J Infect Dis. 1973 May;127(5):595–609. doi: 10.1093/infdis/127.5.595. [DOI] [PubMed] [Google Scholar]
  86. Warren K. S. The immunopathogenesis of schistosomiasis: a multidisciplinary approach. Trans R Soc Trop Med Hyg. 1972;66(3):417–434. doi: 10.1016/0035-9203(72)90273-8. [DOI] [PubMed] [Google Scholar]
  87. Watten K. S., Peters P. A. Comparison of penetration and maturation of Schistosoma mansoni in the hamster, mouse, guinea pig, rabbit, and rat. Am J Trop Med Hyg. 1967 Nov;16(6):718–722. [PubMed] [Google Scholar]
  88. Webbe G., James C. Infra-specific variations of Schistosoma haematobium. J Helminthol. 1971;45(4):403–413. doi: 10.1017/s0022149x00000651. [DOI] [PubMed] [Google Scholar]
  89. Webbe G., James C. Letter: Acquired resistance to Schistosoma haematobium in the baboon (Papio anubis). Trans R Soc Trop Med Hyg. 1973;67(1):151–152. doi: 10.1016/0035-9203(73)90343-x. [DOI] [PubMed] [Google Scholar]
  90. Webbe G., James C., Nelson G. S. Schistosoma haematobium in the baboon (Papio anubis). Ann Trop Med Parasitol. 1974 Jun;68(2):187–203. doi: 10.1080/00034983.1974.11686937. [DOI] [PubMed] [Google Scholar]
  91. Webbe G., James C., Nelson G. S. Schistosoma haematobium in the baboon (Papio anubis). Ann Trop Med Parasitol. 1974 Jun;68(2):187–203. doi: 10.1080/00034983.1974.11686937. [DOI] [PubMed] [Google Scholar]
  92. Wilson R. A., Barnes P. E. An in vitro investigation of dynamic processes occurring in the schistosome tegument, using compounds known to disrupt secretory processes. Parasitology. 1974 Apr;68(2):259–270. doi: 10.1017/s0031182000045777. [DOI] [PubMed] [Google Scholar]
  93. Wilson R. A., Barnes P. E. The tegument of Schistosoma mansoni: observations on the formation, structure and composition of cytoplasmic inclusions in relation to tegument function. Parasitology. 1974 Apr;68(2):239–258. [PubMed] [Google Scholar]
  94. Yogore M. G., Jr, Lewert R. M. Schistosomiasis japonica in the Philippines: results of standardized immediate intradermal (ID) tests. Am J Trop Med Hyg. 1974 May;23(3):393–399. doi: 10.4269/ajtmh.1974.23.393. [DOI] [PubMed] [Google Scholar]
  95. da Silva L. C., de Brito T., Camargo M. E., de Boni D. R., Lopes J. D., Gunji J. Kidney biopsy in the hepatosplenic form of infection with Schistosoma mansoni in man. Bull World Health Organ. 1970;42(6):907–910. [PMC free article] [PubMed] [Google Scholar]
  96. von LICHTENBERG, RITCHIE L. S. Cellular resistance against schistosomula of Schistosoma mansoni in Macaca mulatta monkeys following prolonged infections. Am J Trop Med Hyg. 1961 Nov;10:859–869. doi: 10.4269/ajtmh.1961.10.859. [DOI] [PubMed] [Google Scholar]
  97. von Lichtenberg F., Bawden M. P., Shealey S. H. Origin of circulating antigen from the schistosome gut. An immunofluorescent study. Am J Trop Med Hyg. 1974 Nov;23(6):1088–1091. doi: 10.4269/ajtmh.1974.23.1088. [DOI] [PubMed] [Google Scholar]

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