Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Immunological modulation and evasion by helminth parasites in human populations

Abstract

Helminth parasites are highly prevalent in human communities in developing countries. In an endemic area an infected individual may harbour parasitic worms for most of his or her life, and the ability of these infections to survive immunological attack has long been a puzzle. But new techniques are starting to expose the diverse mechanisms by which these agents modulate or evade their hosts' defences, creating a dynamic interaction between the human immune system and the parasite population.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

References

  1. Warren, K. S. & Mahmoud, A. A. F. Tropical and Geographic Medicine (McGraw-Hill, New York, 1984).

    Google Scholar 

  2. Anderson, R. M. & May, R. M. Nature 280, 361–367 (1979).

    ADS  CAS  PubMed  Google Scholar 

  3. Anderson, R. M. & May, R. M. Adv. Parasit 24, 1–101 (1985).

    CAS  Google Scholar 

  4. Butterworth, A. E. Fulford, A. J. C., Dunne, D. W., Ouma, J. H. & Sturrock, R. F. Phil. Trans. R. Soc. B 321, 495–511 (1988).

    CAS  Google Scholar 

  5. Maizels, R. M. & Selkirk, M. E. in The Biology of Parasitism (eds Englund, P. T. & Sher, A.) 285–308 (Liss, New York, 1988).

    Google Scholar 

  6. Anderson, R. M. Trans. R. Soc. Trop. Med. Hyg. 80, 686–696 (1986).

    CAS  PubMed  Google Scholar 

  7. Schad, G. A. & Anderson, R. M. Science 228, 1537–1540 (1985).

    ADS  CAS  PubMed  Google Scholar 

  8. Keymer, A. & Pagel, M. in Hookworm Disease: Current Status and New Directions (eds Schad, G. A. & Warren, K. S.) 177–209 (Taylor and Francis, London, 1990).

    Google Scholar 

  9. Warren, K. S. in Bailliere's Clinical Tropical Medicine and Communicable Diseases (ed. Mahmoud, A. A. F.) 301–313 (Balliere, London, 1987).

    Google Scholar 

  10. Nokes, C., Grantham-McGregor, S. M., Sawyer, A. W., Cooper, E. S. & Bundy, D. A. P. Proc. R. Soc. B 247, 77–81 (1992).

    ADS  CAS  Google Scholar 

  11. Ottesen, E. A. Rev. Infect. Dis. 7, 796–801 (1985).

    CAS  PubMed  Google Scholar 

  12. Nadler, S. A. Parasit. Today 3, 154–155 (1987).

    CAS  Google Scholar 

  13. Anderson, R. M. & May, R. M. Infectious Diseases of Humans. Dynamics and Control 1–757 (Oxford Univ. Press, Oxford, 1991).

    Google Scholar 

  14. Anderson, R. M. & Medley, G. F. Parasitology 90, 629–660 (1985).

    PubMed  Google Scholar 

  15. Anderson, R. M. & May, R. M. Nature 297, 557–563 (1982).

    ADS  CAS  PubMed  Google Scholar 

  16. Guyatt, H. L., Bundy, D. A. P., Medley, G. F. & Grenfell, B. T. Parasitology 101, 139–143 (1990).

    PubMed  Google Scholar 

  17. Butterworth, A. E. et al. Trans. R. Soc. Trop. Med. Hyg. 79, 393–408 (1985).

    CAS  PubMed  Google Scholar 

  18. Bundy, D. A. P., Grenfell, B. T. & Rajagopalan, P. K. in Immunoparasit. Today (eds Ash, C. & Gallagher, R. B.) A71–A75 (Elsevier, Cambridge, 1991).

    Google Scholar 

  19. Wilkins, H. A., Blumenthal, U. J., Hagan, P., Hayes, R. J. & Tulloch, S. Trans. R. Soc. Trop. Med. Hyg. 81, 29–35 (1987).

    CAS  PubMed  Google Scholar 

  20. Chandiwana, K. K., Woolhouse, M. E. J. & Bradley, M. Parasitology 102, 73–83 (1991).

    PubMed  Google Scholar 

  21. Wong, M. S. Trans. R. Soc. Trop. Med. Hyg. 85, 89–91 (1990).

    ADS  Google Scholar 

  22. Anderson, R. M. & May, R. M. Nature 315, 493–496 (1985).

    ADS  CAS  PubMed  Google Scholar 

  23. Woolhouse, M. E. J., Taylor, P., Matanhire, D. & Chandiwana, S. K. Nature 351, 757–759 (1991).

    ADS  CAS  PubMed  Google Scholar 

  24. Day, K. P., Gregory, W. F. & Maizels, R. M. Parasite Immun. 13, 277–290 (1991).

    CAS  Google Scholar 

  25. Day, K. P., Grenfell, B., Spark, R., Kazura, J. W. & Alpers, M. P. Am. J. Trop. Med,. Hyg. 44, 518–527 (1991).

    CAS  Google Scholar 

  26. Hagan, P., Blumenthal, U. J., Dunn, D., Simpson, A. J. G. & Wilkins, H. A. Nature 349, 243–245 (1991).

    ADS  CAS  PubMed  Google Scholar 

  27. Bundy, D. A. P., Lillywhite, J. E., Didier, J. M., Simmons, I. & Bianco, A. E. Parasite Immun. 13, 629–638 (1991).

    CAS  Google Scholar 

  28. Dunne, D. W. et al. Eur. J. Immun. 22, 1483–1494 (1992).

    CAS  Google Scholar 

  29. Smithers, S. R. & Terry, R. J. Ann. N.Y. Acad. Sci. 160, 826 (1969).

    ADS  CAS  PubMed  Google Scholar 

  30. Mitchell, G. F. Immunology 38, 209–223 (1979).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Miller, H. R. P. Vet. Immun. Immunopath. 6, 167–259 (1984).

    CAS  Google Scholar 

  32. Wilson, R. A. Parasit. Today 6, 354–358 (1990).

    CAS  Google Scholar 

  33. Haswell-Elkins, M. R., Elkins, D. B. & Anderson, R. M. Parasitology 95, 323–328 (1987).

    PubMed  Google Scholar 

  34. Tingley, G. A. et al. Trans. R. Soc. Trop. Med. Hyg. 82, 448–452 (1988).

    CAS  PubMed  Google Scholar 

  35. Lammie, P. J., Hitch, W. L., Walker Allen, E. M., Hightower, W. & Eberhard, M. L. Lancet 337, 1005–1006 (1991).

    CAS  PubMed  Google Scholar 

  36. Schweitzer, N. & Anderson, R. Proc. R. Soc. B 247, 107–112 (1992).

    ADS  CAS  Google Scholar 

  37. Wakelin, D., in Genetics of Resistance to Bacterial and Parasitic Infection (eds Wakelin, D. M. & Blackwell, J. M.) 153–232 (Taylor and Francis, London, 1988).

    Google Scholar 

  38. Bundy, D. A. P. Parasitology 95, 623–635 (1987).

    PubMed  Google Scholar 

  39. Bundy, D. A. P. & Medley, G. F. Parasitology 104, 105–119 (1992).

    Google Scholar 

  40. Kennedy, M. W. Parasit. Today 5, 316–324 (1989).

    CAS  Google Scholar 

  41. Hirayama, K. et al. Nature 327, 426–430 (1987).

    ADS  CAS  PubMed  Google Scholar 

  42. Wassom, D. L., Wakelin, D., Brooks, B. O., Krco, C. J. & David, C. S. Immunology 51, 625–631 (1984).

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Needham, C. S. et al. Parasitology 105, 275–283 (1992).

    Google Scholar 

  44. Needham, C. S. & Lillywhite, J. E. Trans. R. Soc. Trop. Med. Hyg. (in the press).

  45. Capron, A. & Dessaint, J. P. A. Rev. Immun. 3, 455–476 (1985).

    CAS  Google Scholar 

  46. Ogilvie, B. M., Smithers, S. R. & Terry, R. J. Nature 209, 1221–1223 (1966).

    ADS  CAS  PubMed  Google Scholar 

  47. Jarrett, E. E. E. & Miller, H. R. P. Prog. Allerg. 31, 178–233 (1982).

    CAS  Google Scholar 

  48. Finkelman, F. D. et al. A. Rev. Immun. 8, 303–333 (1990).

    CAS  Google Scholar 

  49. Lundgren, M. et al. Eur. J. Immun. 19, 1311–1315 (1989).

    CAS  Google Scholar 

  50. Brown, T. R. J. exp. Med. 3, 315–347 (1898).

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Grove, D. I., Mahmoud, A. A. F. & Warren, K. S. J. exp. Med. 145, 755–759 (1977).

    CAS  PubMed  Google Scholar 

  52. Coffman, R. L., Seymour, B. W. P., Hudak, S., Jackson, J. & Rennick, D. Science 245, 308–310 (1989).

    ADS  CAS  Google Scholar 

  53. Madden, K. B. et al. J. Immun. 147, 1387–1391 (1991).

    CAS  PubMed  Google Scholar 

  54. Mahanty, S., Abrams, J. S., King, C. L., Limaye, A. P. & Nutman, T. B. J. Immun. 148, 3567–3571 (1992).

    CAS  PubMed  Google Scholar 

  55. Sturrock, R. F. et al. Trans. R. Soc. Trop. Med. Hyg. 77, 363–371 (1983).

    CAS  PubMed  Google Scholar 

  56. Hagan, P., Wilkins, H. A., Blumenthal, U. J., Hayes, R. J. & Greenwood, B. M. Parasite Immun. 7, 625–632 (1985).

    CAS  Google Scholar 

  57. Kurniawan, A. et al. J. Immun. 150, 3941–3950 (1993).

    CAS  PubMed  Google Scholar 

  58. Cooper, E. S. et al. Lancet 338, 1104–1107 (1991).

    CAS  PubMed  Google Scholar 

  59. Gusmāo, R. de, Stanley, A. M. & Ottesen, E. A. Expl Parasit. 52, 147–159 (1981).

    Google Scholar 

  60. Dessein, A. J., Parker, W. L., James, S. L. & David, J. R. J. exp. Med. 153, 423–436 (1981).

    CAS  PubMed  Google Scholar 

  61. Sher, A., Coffman, R. L., Hieny, S. & Cheever, A. W. J. Immun. 145, 3911–3916 (1990).

    CAS  PubMed  Google Scholar 

  62. Butterworth, A. E. Adv. Parasit. 23, 143–235 (1984).

    CAS  Google Scholar 

  63. Yazdanbakhsh, M., Tai, P.-C., Spry, C. J. F., Gleich, G. J. & Roos, D. J. Immun. 138, 3443–3447 (1987).

    CAS  PubMed  Google Scholar 

  64. Mahmoud, A. A. F., Warren, K. S. & Peters, P. A. J. exp. Med. 142, 805–813 (1975).

    CAS  PubMed  Google Scholar 

  65. Korenaga, M. et al. Immunology 72, 502–507 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Moqbel, R. & MacDonald, A. J. in Parasites: Immunity and Pathology. The Consequences of Parasitic Infection in Mammals (eds Behnke, J. M.) 249–282 (Taylor and Francis, London, 1990).

    Google Scholar 

  67. Moqbel, R. et al. Immunology 60, 425–430 (1987).

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Smith, N. C. Parasit. Res. 75, 423–438 (1989).

    ADS  CAS  Google Scholar 

  69. Dehlawi, M. S., Wakelin, D. & Behnke, J. M. Parasite Immun. 9, 187–194 (1987).

    CAS  Google Scholar 

  70. Miller, H. R. P., Huntley, J. F. & Wallace, G. R. Immunology 44, 419–429 (1981).

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Esparza, I., Männel Ruppel, A., Falk, W. & Krammer, P. H. J. exp. Med. 166, 589–594 (1987).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. James, S. L. & Glaven, J. J. Immun. 143, 4208–4212 (1989).

    CAS  PubMed  Google Scholar 

  73. Cottrell, B. J., Pye, C., Glauert, A. M. & Butterworth, A. E. J. Cell Sci. 94, 733–741 (1989).

    PubMed  Google Scholar 

  74. Scott, P., James, S. & Sher, A. Eur. J. Immun. 15, 553–558 (1985).

    CAS  Google Scholar 

  75. Mosmann, T. R. & Coffman, R. L. A. Rev. Immun. 9, 145–173 (1989).

    Google Scholar 

  76. Sher, A. F. & Coffman, R. L. A. Rev. Immun. 10, 385–409 (1992).

    CAS  Google Scholar 

  77. Zwingenberger, K., Hohmann, A., Cardoso de Brito, M. & Ritter, M. Scand. J. Immun. 34, 243–251 (1991).

    CAS  Google Scholar 

  78. Del Prete, G. et al. J. Clin. Invest. 88, 346–350 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Pearce, E. J., Caspar, P., Grzych, J.-M., Lewis, F. A. & Sher, A. J. exp. Med. 173, 159–166 (1991).

    CAS  PubMed  Google Scholar 

  80. Caulada-Benedetti, Z., Al-Zamel, F., Sher, A. & James, S. J. Immun. 146, 1655–1660 (1991).

    CAS  PubMed  Google Scholar 

  81. Else, K. J. & Grencis, R. K. Immunology 72, 508–513 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Urban, J. F. Jr, Katona, I. M., Paul, W. E. & Finkelman, F. D. Proc. natn. Acad. Sci. U.S.A. 88, 5513–5517 (1991).

    ADS  CAS  Google Scholar 

  83. Pritchard, D. I., Williams, D. J. L., Behnke, J. M. & Lee, T. D. G. Immunology 49, 353–365 (1983).

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Pond, L., Wassom, D. L. & Hayes, C. E. J. Immun. 143, 4232–4237 (1989).

    CAS  PubMed  Google Scholar 

  85. Yazdanbakhsh, M. et al. J. infect. Dis. 167, 925–931 (1993).

    CAS  PubMed  Google Scholar 

  86. Romagnani, S. Immun. Today 12, 256–257 (1991).

    CAS  PubMed  Google Scholar 

  87. Wierenga, E. A. et al. J. Immun. 147, 2942–2949 (1991).

    CAS  PubMed  Google Scholar 

  88. Gooding, L. R. Cell 71, 5–7 (1992).

    CAS  Google Scholar 

  89. Dessaint, J.-P. & Capron, A. R. in Immunology and Molecular Biology of Parasitic Infections 3rd edn (ed. Warren, K. S.) 87–99 (Blackwell Scientific, Boston, 1993).

    Google Scholar 

  90. Behnke, J. M., Barnard, C. J. & Wakelin, D. Int. J. Parasit. 22, 861–907 (1992).

    CAS  Google Scholar 

  91. Sher, A. & Moser, G. Am. J. Path. 102, 121–126 (1981).

    CAS  PubMed  Google Scholar 

  92. Pearce, E. J., Hall, B. F. & Sher, A. J. Immun. 144, 2751–2756 (1990).

    CAS  PubMed  Google Scholar 

  93. Modha, J., Parikh, V., Gauldie, J. & Doenhoff, M. J. Parasitology 96, 99–109 (1988).

    CAS  PubMed  Google Scholar 

  94. Chiang, C.-P. & Caulfield, J. P. Am. J. Path. 134, 1007–1018 (1989).

    CAS  PubMed  Google Scholar 

  95. Stadecker, M. J., Kamisato, J. K. & Chikunguwo, S. M. J. Immun. 145, 2697–2700 (1990).

    CAS  PubMed  Google Scholar 

  96. Pritchard, D. I., Ali, N. M. H. & Behnke, J. M. Immunology 51, 633–642 (1984).

    CAS  PubMed  PubMed Central  Google Scholar 

  97. Leyva-Cobian, F. & Unanue, E. R. J. Immun. 141, 1445–1450 (1988).

    CAS  PubMed  Google Scholar 

  98. Lal, R. B., Kumaraswami, V., Steel, C. & Nutman, T. B. Am. J. Trop. Med. Hyg. 42, 56–64 (1990).

    CAS  PubMed  Google Scholar 

  99. Diment, S. J. Immun. 145, 417–422 (1990).

    CAS  PubMed  Google Scholar 

  100. Lustigman, S., Brotman, B., Huima, T. & Prince, A. M. Molec. Biochem. Parasit. 45, 65–76 (1991).

    CAS  Google Scholar 

  101. Bennett, K. et al. Eur. J. Immun. 22, 1519–1524 (1992).

    CAS  Google Scholar 

  102. Leid, R. W., Suquet, C. M., Bouwer, H. G. A. & Hinrichs, D. J. J. Immun. 137, 2700–2702 (1986).

    CAS  PubMed  Google Scholar 

  103. Schwartz, R. H. Science 248, 1349–1356 (1990).

    ADS  CAS  Google Scholar 

  104. Ramsdell, F. & Fowlkes, B. J. Science 257, 1130–1134 (1992).

    ADS  CAS  PubMed  Google Scholar 

  105. Auriault, C., Ouaissi, M. A., Torpier, G., Eisen, H. & Capron, A. Parasite Immun. 3, 33–41 (1981).

    CAS  Google Scholar 

  106. Chapman, C. B. & Mitchell, G. F. Vet. Parasit. 11, 165–178 (1982).

    CAS  Google Scholar 

  107. Tamashiro, W. K., Rao, M. & Scott, A. L. J. Parasit. 73, 149–154 (1987).

    CAS  PubMed  Google Scholar 

  108. Hammerberg, B. & Williams, J. F. J. Immun. 120, 1033–1037 (1978).

    CAS  PubMed  Google Scholar 

  109. Shepherd, J. C., Aitken, A. & McManus, D. P. Molec. Biochem. Parasit. 44, 81–90 (1991).

    CAS  Google Scholar 

  110. Blackburn, C. C. & Selkirk, M. E. Immunology 75, 41–46 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  111. Liu, L. X., Serhan, C. N. & Weller, P. F. J. exp. Med. 172, 993–996 (1990).

    CAS  PubMed  Google Scholar 

  112. Leid, R. W. & McConnell, L. A. Prostagland. Leukotri. Med. 11, 317–323 (1983).

    CAS  Google Scholar 

  113. Nutman, T. B., Kumaraswami, V. & Ottesen, E. A. J. Clin. Invest. 79, 1516–1523 (1987).

    CAS  PubMed  PubMed Central  Google Scholar 

  114. Maizels, R. M. & Lawrence, R. A. Parasit. Today 7, 271–276 (1991).

    CAS  Google Scholar 

  115. Ottesen, E. A., Kumaraswami, V., Paranjape, R., Poindexter, R. W. & Tripathy, S. P. J. Immun. 127, 2014–2020 (1981).

    CAS  PubMed  Google Scholar 

  116. Butterworth, A. E. et al. Parasitology 94, 281–300 (1987).

    PubMed  Google Scholar 

  117. Dessein, A. et al. Parasitology 82, 357–374 (1981).

    CAS  PubMed  Google Scholar 

  118. Blaxter, M. L., Page, A. P., Rudin, W. & Maizels, R. M. Parasit. Today 8, 243–247 (1992).

    CAS  Google Scholar 

  119. Hanna, R. E. B. Expl Parasit. 50, 103–114 (1980).

    CAS  Google Scholar 

  120. Callahan, H. L., Crouch, R. K. & James, E. R. Parasit. Today 4, 218–225 (1988).

    CAS  Google Scholar 

  121. Simurda, M. C., van Keulen, H., Rekosh, D. & LoVerde, P. T. Expl Parasit. 67, 73–84 (1988).

    CAS  Google Scholar 

  122. Cookson, E., Blaxter, M. L. & Selkirk, M. E. Proc. natn. Acad. Sci. U.S.A. 89, 5837–5841 (1992).

    ADS  CAS  Google Scholar 

  123. Smith, D. B. et al. Proc. natn. Acad. Sci. U.S.A. 83, 8703–8707 (1986).

    ADS  CAS  Google Scholar 

  124. Balloul, J. M. et al. Nature 326, 149–153 (1987).

    ADS  CAS  PubMed  Google Scholar 

  125. Taylor, J. B. et al. EMBO J. 7, 456–472 (1988).

    Google Scholar 

  126. Nare, B., Smith, J. M. & Prichard, R. K. Expl Parasit. 70, 389–397 (1990).

    CAS  Google Scholar 

  127. Kwan-Lim, G.-E., Forsyth, K. P. & Maizels, R. M. J. Immun. 145, 4298–4305 (1990).

    CAS  PubMed  Google Scholar 

  128. Dissanayake, S., Xu, M. & Piessens, W. F. Molec. Biochem. Parasit. 56, 269–278 (1992).

    CAS  Google Scholar 

  129. Maddox, J. Nature 363, 13 (1993).

    ADS  CAS  Google Scholar 

  130. Anderson, R. M. J. Anim. Ecol. 60, 1–50 (1991).

    CAS  Google Scholar 

  131. Muller, R. Worms and Disease, a Manual of Medical Helminthology (Heinemann Medical, London, 1975).

    Google Scholar 

  132. Muller, R. in Immunology and Molecular Biology of Parasitic Infections 3rd edn (ed. Warren, K. S.) 567–598 (Blackwell Scientific, Boston, 1993).

    Google Scholar 

  133. Joseph, M., Capron, A., Butterworth, A. E., Sturrock, R. F. & Houba, V. Clin. Exp. Immunol. 33, 48–56 (1978).

    CAS  PubMed  PubMed Central  Google Scholar 

  134. Capron, M. et al. J. Immun. 132, 462–468 (1984).

    CAS  PubMed  Google Scholar 

  135. Khalife, J. et al. J. Immun. 142, 4422–4427 (1989).

    CAS  PubMed  Google Scholar 

  136. Rzepczyk, C. M. & Bishop, C. J. Parasite Immun. 6, 443–457 (1984).

    CAS  Google Scholar 

  137. Joseph, M., Auriault, C., Capron, A., Vorng, H. & Viens, P. Nature 303, 810–812 (1983).

    ADS  CAS  PubMed  Google Scholar 

  138. Bout, D. et al. Science 231, 153–156 (1986).

    ADS  CAS  PubMed  Google Scholar 

  139. Mitchell, G. F. Adv. Immun. 28, 451–511 (1979).

    CAS  PubMed  Google Scholar 

  140. Henkle, K. J., Liebau, E., Müller, S., Bergmann, B. & Walter, R. D. Infect. Immun. 59, 2063–2069 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  141. Mazingue, C. et al. Int. Arch. Allerg. appl. Immun. 83, 12–18 (1987).

    CAS  Google Scholar 

  142. Laclette, J. P. et al. J. Immun. 148, 124–128 (1992).

    CAS  PubMed  Google Scholar 

  143. Webber, R. H. S. E. Asian J. trop. Med. Pub. Hlth 27, 59–85 (1975).

    Google Scholar 

  144. Elkins, D. B., Haswell-Elkins, M. & Anderson, R. M. Trans. R. Soc. Trop. Med. Hyg. 80, 774–792 (1986).

    CAS  PubMed  Google Scholar 

  145. Bundy, D. A. P. Phil. Trans. R. Soc. Lond. B 321, 405–420 (1988).

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Maizels, R., Bundy, D., Selkirk, M. et al. Immunological modulation and evasion by helminth parasites in human populations. Nature 365, 797–805 (1993). https://doi.org/10.1038/365797a0

Download citation

  • Issue date:

  • DOI: https://doi.org/10.1038/365797a0

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing