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The Immune Regulation of Intestinal Helminthiases

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Enteric Infections and Immunity

Part of the book series: Infectious Agents and Pathogenesis ((IAPA))

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Abstract

Intestinal helminthiases represent collectively the most prevalent parasitic infection of humankind. In developing countries, where nearly 75% of the global population lives, between one-third and one-half of the residents carry one or more intestinal parasitic worms; children born in endemic areas are likely to acquire these infections early and remain infected for the rest of their lives. The impact of these parasites on the health of their hosts covers the entire spectrum from negligible to catastrophic; therefore, there is a dearth of reliable information on the actual medical and financial burden caused by these infections. There is, however, little doubt that the combined morbidity resulting from intestinal worms represents a major obstacle to the full social and economic development of many tropical nations, and that the elimination of intestinal parasitoses would be a desirable goal.

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References

  1. Noble, E. R., Noble, G. A., Schad, G. A., and MacGuiness, A.J., 1989, Parasitology: The Biology of Animal Parasites, Lea & Febiger, Philadelphia.

    Google Scholar 

  2. Genta, R. M., 1992, The dysregulation of strongyloidiasis: A new hypothesis, Clin. Microbiol. Rev. 5:345–355.

    PubMed  CAS  Google Scholar 

  3. Warren, K. S. (ed.), 1993, Immunobiology and Molecular Biology of Parasitic Infections, 3rd ed., Blackwell, Oxford.

    Google Scholar 

  4. Gleich, G. J., Ottesen, E. A., Leiferman, K. M., and Ackerman, S. J., 1989, Eosinophils and human disease, Int. Arch. Allergy Appl. Immunol. 88:59–62.

    Article  PubMed  CAS  Google Scholar 

  5. Jarrett, E. E. E., and Miller, H. R. P., 1982, Production and activities of IgE in helminthic infections, Prog. Allergy 31:178–233.

    PubMed  CAS  Google Scholar 

  6. Lynch, N. R., Isturiz, G., Sanchez, Y., Perez, M., Martinez, A., and Castes, M., 1992, Bronchial challenge of tropical asthmatics with Ascaris lumbricoides, J. Invest. Allergol. Clin. Immunol. 2: 97–105.

    CAS  Google Scholar 

  7. Maizels, R. M., Bundy, D. A. P., Selkirk, M. E., Smith, D. F., and Anderson, R. M., 1993, Immunological modulation and evasion by helminth parasites in human populations, Nature 365:797–805.

    Article  PubMed  CAS  Google Scholar 

  8. Romagnani, S., 1992, Human Thl and Th2 subsets: Regulation of differentiation and role in protection and immunopathology, Int. Arch. Allergy Appl. Immunol. 98:279–284.

    Article  CAS  Google Scholar 

  9. Hermanek, J., Goyal, P. K., and Wakelin, D., 1994, Lymphocyte, antibody and cytokine responses during concurrent infections between helminths that selectively promote T-helper-1 or T-helper-2 activity, Parasite Immunol. 16:111–117.

    Article  PubMed  CAS  Google Scholar 

  10. Turner, K., Fedde, A. L., and Quinn, E. H., 1979, Non-specific potentiation of IgE by parasite infections in man, Int. Arch. Allergy Appl. Immunol. 58:232–238.

    Article  PubMed  CAS  Google Scholar 

  11. Fraser, E. M., Christie, J. F., and Kennedy, M. W., 1993, Heterogeneity amongst infected children in IgE antibody repertoire to the antigens of the parasitic nematode Ascaris, Int. Arch. Allergy Immunol 100:283–286.

    Article  PubMed  CAS  Google Scholar 

  12. Egwang, T. G., Nguiri, C., Kombila, M., Duong, T. H., and Richard-Lenoble, D., 1993, Elevated antifilarial IgG4 antibody levels in microfilaremic and micronlarermic Gabonese adults and children, Am. J. Trop. Med. Hyg. 49:135–142.

    PubMed  CAS  Google Scholar 

  13. Kurniawan, A., Yazdanbakhsh, M., van Ree, R., Aalberse, R., Selkirk, M. E., Partono, F., and Maizels, R. M., 1993, Differential expression of IgE and IgG4 specific antibody responses in asymptomatic and chronic human filariasis, J. Immunol. 150:3941–3950.

    PubMed  CAS  Google Scholar 

  14. Urban, J. F., Jr., Madden, K. B., Svetic, A., Cheever, A., Trotta, P. P., Gause, W. C., Katona, I. M., and Finkelman, F. D., 1992, The importance of Th2 cytokines in protective immunity to nematodes, Immunol. Rev. 127:205–220.

    Article  PubMed  CAS  Google Scholar 

  15. Capron, A., Dessaint, J. P., and Capron, M., 1992, Allergy and immune defense: Common IgE mechanisms or divergent pathways, in: Allergy and Immunity to Helminths: Common Mechanisms or Divergent Pathways? (R. Moqbel, ed.), Taylor & Francis, London, pp. 1–16.

    Google Scholar 

  16. Pritchard, D. I., 1992, Parasites and allergic diseases: A review of the field and experimental evidence for a cause-and-effect relationship, in: Allergy and Immunity to Helminths: Common Mechanisms or Divergent Pathways? (R. Moqbel, ed.), Taylor & Francis, London, pp. 38–50.

    Google Scholar 

  17. Wehner, J. H., Kirsch, C. M., Kagawa, F. T., Jensen, W. A., Campagna, A. C., and Wilson, M., 1994, The prevalence and response to therapy of Strongyloides stercoralis in patients with asthma from endemic areas, Chest 106:762–766.

    Article  PubMed  CAS  Google Scholar 

  18. Genta, R. M., Ottesen, E. A., Poindexter, R., Gam, A. A., Neva, F. A., Tanowitz, H. B., and Wittner, M., 1983, Specific allergic sensitization to Strongyloides antigens in human strongy-loidiasis, Lab. Invest. 48:633–638.

    PubMed  CAS  Google Scholar 

  19. McRury, J., de Messias, I. T., Walzer, P. D., Huitger, T., and Genta, R. M., 1986, Specific IgE responses in human strongyloidiasis, Clin. Exp. Immunol. 65:631–638.

    PubMed  CAS  Google Scholar 

  20. Hussain, R., Poindexter, R. W., and Ottesen, E. A., 1992, Control of allergic reactivity in human filariasis. Predominant localization of blocking antibody to the IgG4 subclass, J. Immunol. 148:2731–2737.

    PubMed  CAS  Google Scholar 

  21. Genta, R. M., and Lillibridge, J. P., 1989, Prominence of IgG4 antibodies in the human responses to Strongyloides stercoralis infection, J. Infect. Dis. 160:692–699.

    Article  PubMed  CAS  Google Scholar 

  22. Genta, R. M., 1988, Predictive value of an enzyme-linked immunosorbent assay (ELISA) for the serodiagnosis of strongyloidiasis, Am. J. Clin. Pathol. 89:391–394.

    PubMed  CAS  Google Scholar 

  23. Conway, D. J., Lindo, J. F., Robinson, R. D., Bundy, D. A., and Bianco, A. E., 1994, Strongyloides stercoralis: Characterization of immunodiagnostic larval antigens, Exp. Parasitol. 79:99–105.

    Article  PubMed  CAS  Google Scholar 

  24. Genta, R. M., and Weil, G. J., 1982, Antibodies to Strongyloides stercoralis larval surface antigens in chronic strongyloidiasis, Lab. Invest. 47:87–90.

    PubMed  CAS  Google Scholar 

  25. Genta, R. M., Frei, D. F., and Linke, M. J., 1987, Demonstration and partial characterization of parasite-specific immunoglobulin A responses in human strongyloidiasis, J. Clin. Micro-biol. 25:1505–1510.

    CAS  Google Scholar 

  26. Badarò, R., Carvalho, E. M., Santos, R. B., Gam, A. A., and Genta, R. M., 1987, Parasite-specific humoral responses in different clinical forms of strongyloidiasis, Trans. R. Soc. Trop. Med. Hyg. 81:149–150.

    Article  PubMed  Google Scholar 

  27. Genta, R. M., Gatti, S., Linke, M. J., Cevini, C., and Scaglia, M., 1988, Endemic strongyloidiasis in northern Italy: Clinical and immunological aspects, Q. J. Med. 68:679–690.

    PubMed  CAS  Google Scholar 

  28. Mansfield, L. S., and Schad, G. A., 1992, Strongyloides stercoralis infection in IgA-deficient dogs, Am. J. Trop. Med. Hyg. 47:830–836.

    PubMed  CAS  Google Scholar 

  29. Needham, C. S., Lillywhite, J. E., Didier, J. M., Bianco, A. E., and Bundy, D. A., 1994, Temporal changes in Trichuris trichiura infection intensity and serum isotype responses in children, Parasitology 109:197–200.

    Article  PubMed  Google Scholar 

  30. Needham, C. S., Bundy, D. A., Lillywhite, J. E., Didier, J. M., Simmons, I., and Bianco, A. E., 1992, The relationship between Trichuris trichiura transmission intensity and the age-profiles of parasite-specific antibody isotopes in two endemic communities, Parasitology 105:273–283.

    Article  PubMed  Google Scholar 

  31. Haswell-Elkins, M. R., Leonard, H., Kennedy, M. W., Alkenes, D. B., and Maizels, R. M., 1992, Immunoepidemiology of Ascaris lumbricoides: Relationships between antibody specificities, exposure and infection in a human community, Parasitology 104:153–159.

    Article  PubMed  Google Scholar 

  32. Haswell-Elkins, M. R., Kennedy, M. W., Maizels, R. M., Elkins, D. B., and Anderson, R. M., 1989, The antibody recognition profiles of humans naturally infected with Ascaris lumbricoides, Parasite Immunol. 11:615–627.

    Article  PubMed  CAS  Google Scholar 

  33. Pritchard, D. L., Walsh, E. A., Quinell, R. J., Raiko, A., Edmonds, P., and Keymer, A. E., 1992, Isotypic variation in antibody responses in a community in Papua New Guinea to larval and adult antigens during infection, and following reinfection, with the hookworm Necator americanus, Parasite Immunol. 14:617–631.

    Article  PubMed  CAS  Google Scholar 

  34. Capron, M., 1992, Dual function of eosinophils in pathogenesis and protective immunity against parasites, Mem. Inst. Oswaldo Cruz 87(Suppl 5):83:-89.

    Google Scholar 

  35. Cromwell, O., Wardlaw, A. J., Champion, A., Moqbel, R., Osei, D., and Kay, A. B., 1990, IgG-dependent generation of platelet-activating factor by normal and low-density human eosinophils, J.Immunol 145:3862–3868.

    PubMed  CAS  Google Scholar 

  36. Butterworth, A. E., 1984, Cell-mediated damage to helminths, Adv. Parasitol. 23:143–235.

    Article  PubMed  CAS  Google Scholar 

  37. Miller, H. R. P., 1992, Mast cells: Their function and heterogeneity, in: Allergy and Immunity to Helminths: Common Mechanisms or Divergent Pathways? (R. Moqbel, ed.), Taylor & Francis, London, pp. 228–248.

    Google Scholar 

  38. Madden, K. B., Urban, J. F., Jr., Ziltener, H.J., Schrader, J. W., Finkelman, F. D., and Katona, I. M., 1991, Antibodies to IL-3 and IL-4 suppress helminth-induced intestinal mastocytosis, J. Immunol. 15:1387–1391.

    Google Scholar 

  39. Marsh, M. N. (ed.), 1987, Immunopathology of the Small Intestine, Wiley, New York.

    Google Scholar 

  40. Moqbel, R., and MacDonald, A., 1990, Immunological and inflammatory responses in the small intestine associated with helminthic infections, in: Parasites: Immunity and Pathology (J. M. Behnke, ed.), Taylor & Francis, London, pp. 249–282.

    Google Scholar 

  41. Brandtzaeg, O., Vaines, K., Scott, H., Rognum, T. O., Bjerke, K., and Baklien, K., 1985, The human gastrointestinal secretory immune system in health and disease, Scand. J. Gastroente-rol. 20(Suppl. 114):17–38.

    Article  Google Scholar 

  42. Castro, G. A., 1990, Intestinal pathology, in: Parasites: Immunity and Pathology (J. M. Behnke, ed.), Taylor & Francis, London, pp. 282–310.

    Google Scholar 

  43. Abe, T., and Nawa, Y, 1988, Worm expulsion and mucosa mast cells response induced by repetitive IL-3 administration in Strongyloides ratti-infected nude mice, Immunology 63:181–185.

    PubMed  CAS  Google Scholar 

  44. Kassai, T., Redl, P., Jecsai, G., Balla, E., and Harangozo, E., 1989, Studies on the involvement of prostaglandins and their precursors in the rejection of Nippostrongylus brasiliensis from the rat, Int. J. Parasitol. 10:115–120.

    Article  Google Scholar 

  45. Gilman, R. H., Chong, Y. H., Davis, C., Greenberg, B., Virik, H. K., and Dixon, H. B., 1983, The adverse consequences of heavy Trichuris infection, Trans. R. Soc. Trop. Med. Hyg. 77: 432–438.

    Article  PubMed  CAS  Google Scholar 

  46. Bundy, D. A. P., 1986, Epidemiological aspects of Trichuris and trichuriasis in Caribbean communities, Trans. R. Soc. Trop. Med. Hyg. 80:706–718.

    Article  PubMed  CAS  Google Scholar 

  47. Cooper, E. S., and Bundy, D. A. P., 1987, Trichuriasis, in: Bailliere’s Clinical Tropical Medicine and Communicable Diseases, Intestinal Helminthic Infections (Z. S. Pawlowski, ed.), Bailliere Tindall, London, pp. 629–643.

    Google Scholar 

  48. Cooper, E. S., Spencer, J., Whyte-Alleng, C. A. M., Cromwell, O., Whitney, P., Venugopal, S., Bundy, D. A., Haynes, B., and MacDonald, T. T., 1992, Immediate hypersensitivity in colon of children with chronic Trichuris trichiura dysentery, Lancet 338:1104–1107.

    Article  Google Scholar 

  49. Pawlowski, Z. B., 1982, Ascariasis: Host-pathogen biology, Rev. Inf. Dis. 4:806–814.

    Article  CAS  Google Scholar 

  50. Schulz, M. G., 1982, Ascariasis: Nutritional implications, Rev. Inf. Dis. 4:815–819.

    Article  Google Scholar 

  51. Gilles, H. M., 1990, Naturally acquired infections: What’s needed? in: Hookworm Disease, Current Status and New Directions (G. A. Schad and K. S. Warren, eds.), Taylor & Francis, London, pp. 221–230.

    Google Scholar 

  52. Schad, G. A., 1991, The parasite, in: Hookworm Infections (H. M. Gilles and P. A. J. Ball, eds.), Elsevier, Amsterdam, pp. 15–50.

    Google Scholar 

  53. Miller, T. A., 1979, Hookworm infection in man, Adv. Parasitol. 17:315–384.

    Article  PubMed  CAS  Google Scholar 

  54. Behnke, J. M., 1991, Pathology, in: Hookworm Infections (H. M. Gilles and P. A. J. Ball, eds.), Elsevier, Amsterdam, pp. 51–92.

    Google Scholar 

  55. Genta, R. M., and Caymmi-Gomes, M., 1989, Pathology, in: Strongyloidiasis, a Major Round-worm Infection of Man (D. A. Grove, ed.), Taylor & Francis, London, pp. 105–132.

    Google Scholar 

  56. Harper, J. S., Genta, R. M., Gam, A. A., London, W. J., and Neva, F. A., 1984, Experimental disseminated strongyloidiasis in Erythrocebus patas. Part I. Pathology, Am. J. Trop. Med. Hyg. 33:431–443.

    PubMed  Google Scholar 

  57. Longworth, D. L., and Weller, P. F., 1986, Hyperinfection syndrome with strongyloidiasis, in: Current Clinical Topics in Infectious Diseases (J. S. Remington and M. N. Swartz, eds.) McGraw-Hill, New York, pp. 1–26.

    Google Scholar 

  58. MacDonald, T. T., 1992, Epithelial proliferation in response to gastrointestinal inflammation, Ann. N.Y. Acad. Sci. 664:202–209.

    Article  PubMed  CAS  Google Scholar 

  59. MacDonald, T. T., Choy, M. Y., Spencer, J., Richman, P. I., Diss, T., Hanchard, B., Venugopal, S., Bundy, D. A., and Cooper, E. S., 1991, Histopathology and immunohistochemistry of the caecum in children with the Trichuris dysentery syndrome, J. Clin. Pathol. 44:194–199.

    Article  PubMed  CAS  Google Scholar 

  60. Butterworth, A. E., Sturrock, R. F., and Ouma, J. H., 1992, On the use of age-intensity data to detect immunity to parasitic infections, with special reference to Schistosoma mansoni in Kenya, Parasitology 105(Pt. 2):219–227.

    Article  PubMed  Google Scholar 

  61. Day, K. P., Gregory, W. E., and Maizels, R. M., 1991, Age-specific acquisition of immunity to infective larvae in a bancroftian filariasis endemic area of Papua New Guinea, Parasite Immunol. 13:277–290.

    Article  PubMed  CAS  Google Scholar 

  62. Capron, A., and Dessaint, J. P., 1992, Immunologic aspects of schistosomiasis, Annu. Rev. Med. 43:209–218.

    Article  PubMed  CAS  Google Scholar 

  63. Bundy, D. A., Lillywhite, J. E., Didier, J. M., Simmons, I., and Bianco, A. E., 1991, Age-dependency of infection status and serum antibody levels in human whipworm (Trichuris trichiura) infection, Parasite Immunol 13:629–638.

    Article  PubMed  CAS  Google Scholar 

  64. Smithers, S. R., and Terry, R. J., 1969, Immunity in schistosomiasis, Ann. N.Y. Acad. Sci. 160(2):826–840.

    Article  PubMed  CAS  Google Scholar 

  65. Mitchell, G. F., 1990, A note on concomitant immunity in host-parasite relationships: A successfully transplanted concept from tumor immunology, Adv. Cancer Res. 54: 319–332.

    Article  PubMed  CAS  Google Scholar 

  66. Schad, G. A., and Anderson, R. M., 1985, Predisposition to hookworm infection in humans, Science 228:1537–1541.

    Article  PubMed  CAS  Google Scholar 

  67. Chan, L., Bundy, D. A., and Kan, S. P., 1994, Aggregation and predisposition to Ascaris lumbricoides and Trichuris trichiura at the familial level, Trans. R. Soc. Trop. Med. Hyg. 88: 46–48.

    Article  PubMed  CAS  Google Scholar 

  68. Bennett, K., Levine, T., Ellis, J. S., Peanasky, R. J., Samloff, I. M., Kay, J., and Chain, B. M., 1992, Antigen processing for presentation by class II major histocompatibility complex requires cleavage by cathepsin E, Eur. J. Immunol. 22:1519–1524.

    Article  PubMed  CAS  Google Scholar 

  69. Leid, R. W., Suquet, C. M., and Tanigoshi, L., 1987, Parasite defense mechanisms for evasion of host attack; a review, Vet. Parasitol. 25:147–162.

    Article  PubMed  CAS  Google Scholar 

  70. Else, K.J., Finkelman, F. D., Maliszewski, C. R., and Grencis, R. K., 1994, Cytokine-mediated regulation of chronic intestinal helminth infection, J. Exp. Med. 179:347–351.

    Article  PubMed  CAS  Google Scholar 

  71. Leid, R. W., Suquet, C. M., Bouwer, H. G., and Hinrichs, D. J., 1986, Interleukin inhibition by a parasite proteinase inhibitor, taeniaestatin, J. Immunol. 137:2700–2702.

    PubMed  CAS  Google Scholar 

  72. Fowlkes, B. J., and Ramsdell, F., 1993, T-cell tolerance, Curr. Opin. Immunol. 5:873–879.

    Article  PubMed  CAS  Google Scholar 

  73. Fishelson, Z., 1991, Complement evasion by parasites: Search for “Achilles’ heel,” Clin. Exp. Immunol. 86(Suppl. 1):47–52.

    PubMed  CAS  Google Scholar 

  74. De Messias, I. J. T., Genta, R. M., and Mohren, W. D., 1994, Adherence of monocytes and polymorphonuclear cells to infective larvae of Strongyloides stercoralis after complement activation, J. Parasitol. 80:267–274.

    Article  PubMed  Google Scholar 

  75. Liu, L. X., Serhan, C. N., and Weiler, P. F., 1990, Intravascular filarial parasites elaborate cyclooxygenase-derived eicosanoids, J. Exp. Med. 172:993–996.

    Article  PubMed  CAS  Google Scholar 

  76. Maizels, R. M., Blaxter, M. L., and Selkirk, M. E., 1993, Forms and functions of nematode surfaces, Exp. Parasitol. 77:380–384.

    Article  PubMed  CAS  Google Scholar 

  77. Page, A. P., Rudin, W., Fluri, E., Blaxter, M. L., and Maizels, R. M., 1992, Toxocara canis: A labile antigenic surface coat overlying the infective larvae, Exp. Parasitol. 75:72–86.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Departments of Pathology, Medicine, and Microbiology and Immunology, Baylor College of Medicine, and Center for Infectious Diseases, University of Texas School of Public Health, Houston, Texas, 77030, USA

    Robert M. Genta

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  1. University of South Florida College of Medicine, Tampa, Florida, USA

    Lois J. Paradise  & Herman Friedman  & 

  2. University of Pisa, Pisa, Italy

    Mauro Bendinelli

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Genta, R.M. (1996). The Immune Regulation of Intestinal Helminthiases. In: Paradise, L.J., Bendinelli, M., Friedman, H. (eds) Enteric Infections and Immunity. Infectious Agents and Pathogenesis. Springer, Boston, MA. https://doi.org/10.1007/978-1-4899-0313-6_13

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  • DOI: https://doi.org/10.1007/978-1-4899-0313-6_13

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