Skip to main content
SpringerLink
Log in

The potential impact of early exposures to geohelminth infections on the development of atopy

  • Published:
Clinical Reviews in Allergy & Immunology Aims and scope Submit manuscript

Abstract

Microbial exposures in early life may provide important signals for immune maturation and the development of an antiinflammatory network thereby preventing the development of dysregulated immune responses such as that associated with allergic disease. The human immune system has evolved in the presence of intense helminth infections and has developed regulatory mechanisms to limit the harmful inflammation that can be caused by the potent allergens secreted by these chronic pathogens. Geohelminth infections are highly prevalent childhood infections, and these is strong evidence that chronic geohelminth infections provide protection against atopy in the rural tropics. Because the early environmental exposures that may lead to the development of atopy are likely to occur in the first few years of life, geohelminth infections may exert their protective effects at this time. Early exposures to geohelminth antigens could occur transplacentally, through breast milk, or through early infant exposures, and could induce tolerance to parasite antigens resulting in suppressed allergic responses to the parasite. Tolerization to parasite antigens could suppress allergic responses to inhalant allergens through by stander effects or through tolerization of crossreactive epitopes that are shared between geohelminth parasites and inhalant allergens. Tolerization to crossreactive allergens could occur by thymic deletion or through peripheral mechanisms such as regulatory T cells. Immunologic studies of the mechanisms by which early exposures to geohelminth infections affect immune polarization to inhalant allergens are likely to provide important insights into the early regulation of the immune response and may lead to the design of novel interventions for the prevention of allergic disease.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Holgate, S.T. (1999), Nature 402, B2-B4.

    Article  PubMed  CAS  Google Scholar 

  2. Jarrett, E.E.E. and Miller, H.R.P. (1982), Prog. Allergy 31, 178–233.

    PubMed  CAS  Google Scholar 

  3. Le Soeuf, P.N., Goldblatt, J., and Lynch, N.R. (2000), Lancet 356, 242–244.

    Article  Google Scholar 

  4. Sutton, B.J. and Gould, H. (1993), Nature 366, 421–428.

    Article  PubMed  CAS  Google Scholar 

  5. Masters, M. and Barrett-Connor, E. (1985), Epidemiol. Rev. 7, 49–58.

    PubMed  CAS  Google Scholar 

  6. Hagel, I., Lynch, N.R., Perez, M., et al. (1993b), Parasite Immunol. 15, 311–315.

    PubMed  CAS  Google Scholar 

  7. Lynch, N.R., Hagel, I.A., Palenque, M.E., et al. (1998), J. Allergy Clin. Immunol. 101, 217–221.

    Article  PubMed  CAS  Google Scholar 

  8. van den Bigelaar, A.H.J., van Ree, R., Rodrigues, L.C., et al. (2000), Lancet 356, 1723–1727.

    Article  Google Scholar 

  9. Scrivener, S., Yemanerbhan, H., Zebenigus, M., et al. (2001), Lancet 358, 1493–1499.

    Article  PubMed  CAS  Google Scholar 

  10. Palmer, L.J., Celedon, J.C., Weiss, S.T., et al. (2002), Am. J. Respir. Crit. Care Med. 165, 1489–1493.

    Article  PubMed  Google Scholar 

  11. Backer, V., Groth, S., Dirksen, A., et al. (1991), Eur. Respir. J. 4, 1093–1100.

    PubMed  CAS  Google Scholar 

  12. Burrows, B., Martinez, F.D., Halonen, M., et al. (1989), N. Engl. J. Med. 320, 271–277.

    Article  PubMed  CAS  Google Scholar 

  13. Ohman, J., Sparrow, D., and McDonald, M.R. (1993), J. Allergy Clin. Immunol. 91, 752–757.

    Article  PubMed  Google Scholar 

  14. Strachan, D.P. (1989), Br. Med. J. 299, 1259–1260.

    Article  CAS  Google Scholar 

  15. Strachan, D.P., Harkins, L.S., Johnston, I.D., and Anderson, H.R. (1997), J. Allergy Clin. Immunol. 99, 6–12.

    Article  PubMed  CAS  Google Scholar 

  16. von Mutius, E., Martinez, F.D., Fritzsch, C., et al. (1994), BMJ 308, 692–695.

    Google Scholar 

  17. Forastiere, F., Agabiti, N., Corbo, G.M., et al. (1997), Epidemiology, 8, 566–570.

    Article  PubMed  CAS  Google Scholar 

  18. Matricardi, P.M., Rosmini, F., Ferrigno, L., et al. (1997), Br. Med. J. 314, 999–1003.

    CAS  Google Scholar 

  19. Matricardi, P.M., Franzinelli, F., Franco A., et al. (1998), J. Allergy Clin. Immunol. 101, 439–444.

    Article  PubMed  CAS  Google Scholar 

  20. Wahn, V., Lau, S., Bergmann, R., et al. (1997), J. Allergy Clin. Immunol. 99, 763–769.

    Article  PubMed  CAS  Google Scholar 

  21. Moffatt, M.F. and Cookson, W.O. (1998), Clin. Exp. Allergy 28, S56-S61.

    Article  Google Scholar 

  22. Kramer, U., Heinrich, J., Wjst, M., and Wichmann, H.E. (1999), Lancet 353, 45–454.

    Google Scholar 

  23. Braun-Fahrlander, C., Riedler, J., Herz, U., et al. (2002), N. Engl. J. Med. 347, 869–877.

    Article  PubMed  Google Scholar 

  24. von Ehrenstein, O.S., Von Mutius, E., Illi, S., et al. (2000), Clin. Exp. Allergy 30, 187–193.

    Article  Google Scholar 

  25. Riedler, J., Braun-Fahrlander, C., Eder, et al. (2001), Lancet 358, 1129–1133.

    Article  PubMed  CAS  Google Scholar 

  26. Hagel, I., Lynch, N.R., DiPrisco, M.C., et al. (1993a), Int. Arch. Allergy Immunol. 101, 209–214.

    Article  PubMed  CAS  Google Scholar 

  27. Lynch, N.R. (1992), in Allergy and Immunity to Helminths. Moqbel, R., ed. Taylor and Francis, London, pp. 51–62.

    Google Scholar 

  28. Shaheen, S.O., Aaby, P., Hall, A.J., et al. (1996), Lancet 347, 1792–1796.

    Article  PubMed  CAS  Google Scholar 

  29. van den Bigelaar, A.H.J., Lopuhaa, C., van Ree, R., et al. (2001), Int. Arch. Allergy Immunol. 126, 231–238.

    Article  Google Scholar 

  30. Nyan, O.A., Walraven, G.E.L., Banya, W.A.S., et al. (2001), Clin. Exp. Allergy, 31, 1672–1678.

    Article  PubMed  CAS  Google Scholar 

  31. Cooper, P.J., Chico, M.E., Rodrigues, L.C., et al. (2003), J. Allergy Clin. Immunol., 111, 995–1000.

    Article  PubMed  Google Scholar 

  32. Strachan, D.P. (2000), Thorax, 55, S2-S10.

    Article  PubMed  Google Scholar 

  33. Holt, P.G. and Macaubas, C. (1997), Curr. Opin. Immunol. 9, 782–787.

    Article  PubMed  CAS  Google Scholar 

  34. Holt, P.G., Sly, P.D., and Bjorksten, B. (1997), Pediatr. Allergy Immunol. 8, 53–58.

    PubMed  CAS  Google Scholar 

  35. Ball, T.M., Castro-Rodriguez, J.A., Griffith, K.A., et al. (2000), N. Engl. J. Med. 343, 538–543.

    Article  PubMed  CAS  Google Scholar 

  36. Bottcher, M.F., Nordin, E.K., Sandin, A., et al. (2000), Clin. Exp. Allergy, 30, 1590–1596.

    Article  PubMed  CAS  Google Scholar 

  37. Bjorksten, B., Naaber, P., Sepp, E., and Mikelsaar, M. (1999), Clin. Exp. Allergy, 29, 342–346.

    Article  PubMed  CAS  Google Scholar 

  38. Kalliomaki, M., Salminen, S., Arvilommi, H., et al. (2001), Lancet 357, 1076–1079.

    Article  PubMed  CAS  Google Scholar 

  39. Kalliomaki, M., Kirjavainen, P., Eerola, E., et al. (2001), J. Allergy Clin. Immunol. 107, 129–134.

    Article  PubMed  CAS  Google Scholar 

  40. Matricardi, P.M. and Bonini, S. (2000), Clin. Exp. Allergy, 30, 1506–1510.

    Article  PubMed  CAS  Google Scholar 

  41. Sudo, N., Sawamura, S., Tanaka, K., et al. (1997), J. Immunol. 159, 1739–1745.

    PubMed  CAS  Google Scholar 

  42. Wickens, K., Pearce, N., Crane, J., and Beasley, R. (1999), Clin. Exp. Allergy 29, 766–771.

    Article  PubMed  CAS  Google Scholar 

  43. Farooqi, I.S. and Hopkin, J.M. (1998), Thorax 53, 927–932.

    Article  PubMed  CAS  Google Scholar 

  44. Reynolds, J.D. and Morris, B. (1983) Eur. J. Immunol. 13, 627–635.

    Article  PubMed  CAS  Google Scholar 

  45. Savioli, L., Stansfield, S., Bundy, D.A.P., et al. (2002), Trans. R. Soc. Trop. Med. Hyg. 96, 577–579.

    Article  PubMed  Google Scholar 

  46. Bundy, D.A.P. and Cooper, E.S. (2001), in Hunter’s Tropical Medicine and Emerging Infectious Diseases, (Strickland, G.T., ed.) 8th ed. WB Saunders, Philadelphia, PA, pp. 722–724.

    Google Scholar 

  47. Bundy, D.A.P., and DeSilva, N. (2001), in Hunter’s Tropical Medicine and Emerging Infectious Diseases, (Strickland, G.T., ed.) 8th ed. WB Saunders, Philadelphia, PA, pp. 726–730.

    Google Scholar 

  48. Gilman RH (2001), in Hunter’s Tropical Medicine and Emerging Infectious Diseases, 8th ed. WB Saunders, Philadelphia, PA, pp. 730–735.

    Google Scholar 

  49. Cooper, P.J. and Nutman, T.B. (2002), in IgE and Anti-IgE Therapy in Asthma and Allergic Disease, vol. 164. Fick, R.B. and Jardieu, P., eds., Marcel Dekker, New York, pp. 409–425.

    Google Scholar 

  50. Cooper, P.J. (2002), Clin. Exp. Immunol. 128, 398–404.

    Article  PubMed  CAS  Google Scholar 

  51. Cooper, P.J., Schwartz, L., Irani, A.M., et al. (2002), J. Infect. Dis. 186, 1307–1313.

    Article  PubMed  CAS  Google Scholar 

  52. Cooper, P.J. (2002), in The Geohelminths: Ascaris, Trichuris, and Hookworm, vol. 2. Kennedy, M.W., and Holland, C.V., eds. Kluwer Academic Press, Boston, MA, pp. 89–104.

    Chapter  Google Scholar 

  53. Loeffler, P. (1956), Arch. Int. Allergy 8, 54–59.

    Google Scholar 

  54. Gelpi, A.P. and Mustafa, A. (1967), Am. J. Trop. Med. Hyg. 16, 646–657.

    PubMed  CAS  Google Scholar 

  55. Spillman, R.K. (1975), Am. J. Trop. Med. Hyg. 24, 791–800.

    Google Scholar 

  56. Holloway, J.A., Warner, J.O., Vance, G.H., et al. (2000), Lancet 356, 1900–1902.

    Article  PubMed  CAS  Google Scholar 

  57. Marks, G.B., Zhou, J., Yang, H.S., et al. (2002), Clin. Exp. Allergy 32, 355–360.

    Article  PubMed  CAS  Google Scholar 

  58. Miller, D.L., Hirvonen, T., and Gitlin, D. (1973), J. Allergy Clin. Immunol. 52, 182.

    Article  PubMed  CAS  Google Scholar 

  59. Johnson, C.C., Ownby, D.R., and Peterson, E.L. (1996), Clin. Exp. Allergy 26, 624–629.

    Article  PubMed  CAS  Google Scholar 

  60. Bergmann, R.L., Schulz, J., Gunther, S., et al. (1995), Allergy 50, 65–71.

    PubMed  CAS  Google Scholar 

  61. Haus, M., De V. Heese, H., Weinberg, E.G., et al. (1988), J. Allergy Clin. Immunol. 82, 179–189.

    Article  PubMed  CAS  Google Scholar 

  62. Weil, G.J., Hussain, R., Kumaraswami, V., et al. (1983) J. Clin. Invest. 71, 1124–1129.

    PubMed  CAS  Google Scholar 

  63. King, C.L., Malhotra, I., Mungai, P., et al. (1998), J. Immunol. 160, 3578–3584.

    PubMed  CAS  Google Scholar 

  64. Tanaka, K., Kawamura, H., Tohgi, N., et al. (1983), Parasitology 86, 291–300.

    Article  PubMed  Google Scholar 

  65. Hitch, W.L., Eberhard, M.L., and Lammie, P.J. (1997), Ann. Trop. Med. Parasitol. 91, 461–469.

    Article  PubMed  CAS  Google Scholar 

  66. Malhotra, I., Ouma, J., Wamachi, A., et al. (1997), J. Clin. Invest. 99, 1759–1766.

    PubMed  CAS  Google Scholar 

  67. Lewert, R.M. and Mandlowitz, S. (1969), Nature 224, 1029–1030.

    Article  PubMed  CAS  Google Scholar 

  68. Camus, D., Carliere, Y., Bina, J.C., et al. (1976), J. Infect. Dis. 134, 405–408.

    PubMed  CAS  Google Scholar 

  69. Tachon, P. and Borojevic, R. (1978), Trans. R. Soc. Trop. Med. Hyg. 72, 605–609.

    Article  PubMed  CAS  Google Scholar 

  70. Haque, A. and Capron, A. (1982), Nature 299, 361–363.

    Article  PubMed  CAS  Google Scholar 

  71. Steel, C., Guinea, A., McCarthy, L., and Ottesen, E.A. (1994), Lancet 343, 890–893.

    Article  PubMed  CAS  Google Scholar 

  72. Hightower, A.W., Lammie, P.J., and Eberhard, M.L. (1993), Parasitol. Today 9, 418–421.

    Article  PubMed  CAS  Google Scholar 

  73. Elson, L.H., Days, A., Calvopina, M., et al. (1996), Infect. Immun. 64, 5061–5065.

    PubMed  CAS  Google Scholar 

  74. Kjellman, N.I. and Croner, S. (1984), Ann. Allergy 53, 167–171.

    PubMed  CAS  Google Scholar 

  75. Prost, A. and Gorim de Ponsay, E. (1979), Tropenmedizin. Parasitol. 30, 477–481.

    CAS  Google Scholar 

  76. Guderian, R.H., Beck, B.J., and Proano, R. (1990), Trans. R. Soc. Trop. Med. Hyg. 84, 109–112.

    Article  PubMed  CAS  Google Scholar 

  77. Eloi-Santos, S.M., Novata-Silva, E., Maselli, V.M., et al. (1989), J. Clin. Invest. 84, 1028–1031.

    PubMed  CAS  Google Scholar 

  78. Petralanda, I., Yarzabal, L., and Piessens, W.F. (1988), Am. J. Trop. Med. Hyg. 38, 372–379.

    PubMed  CAS  Google Scholar 

  79. Klei, T.R., Blanchard, D.P., and Coleman, S.U. (1986), Trans. R. Soc. Trop. Med. Hyg. 80, 214–216.

    Article  PubMed  CAS  Google Scholar 

  80. Colley, D.G. (1990), in Idiotypic Network and Diseases. Cerney, J. and Hiernaux, J., eds. American Society for Microbiology. Washington DC, pp. 71–105.

    Google Scholar 

  81. Soboslay, P.T., Geiger, S.M., Drabner, B., et al. (1999), Clin. Exp. Immunol. 117, 130–137.

    Article  PubMed  CAS  Google Scholar 

  82. Pit, D.S., Polderman, A.M., Schulz-Key, H., and Soboslay, P.T. (2000), Allergy 55, 732–739.

    Article  PubMed  CAS  Google Scholar 

  83. Das, P.K., Sirvidya, A., Vanamail, P., et al. (1997), Trans. R. Soc. Trop. Med. Hyg. 91, 677–679.

    Article  PubMed  CAS  Google Scholar 

  84. Terhell, A.J., Wahyuni, S., Pryce, A., et al. (2002), Trans. R. Soc. Trop. Med. Hyg. 96, 334–339.

    Article  PubMed  CAS  Google Scholar 

  85. Dagoye, D., Bekele, Z., Woldemichael, K., et al. (2003), Am. J. Resp. Crit. Care Med., 167, 1369–1373.

    Article  PubMed  Google Scholar 

  86. Lynch, N.R., Palenque, M., Hagel, I., and DiPrisco, M.C. (1997), Am. J. Respir. Crit. Care Med. 156, 50–54.

    PubMed  CAS  Google Scholar 

  87. Cooper, P.J., Espinel, I., Paredes, W., et al. (1998) J. Infect. Dis. 178, 1133–1138.

    PubMed  CAS  Google Scholar 

  88. Cooper, P.J., Espinel, I., Wieseman, M., et al. (1999), Infect. Immun. 67, 5951–5957.

    PubMed  CAS  Google Scholar 

  89. Joubert, J.R., van Schalkwyk, D.J., and Turner, K.J. (1980), S.A. Med. J. 57, 409–412.

    CAS  Google Scholar 

  90. Khedr, M.S., Al-Shishtawi, M.M., and El Kafass, E.A. (1989), East. Med. Reg. Health Serv. J. 7, 29–35.

    Google Scholar 

  91. Alshishtawy, M. M., Abdella, A.M., Gelber, L.E., and Chapman, M.D. (1991), Int. Arch. Allergy Appl. Immunol. 96, 348–354.

    PubMed  CAS  Google Scholar 

  92. Yazdanbakhsh, M., Kremsner, P.G., and van Ree, R. (2002). Science 296, 490–494.

    Article  PubMed  CAS  Google Scholar 

  93. Godfrey, R.D. and Gradidge, C.F. (1976), Nature 259, 484–486.

    Article  PubMed  CAS  Google Scholar 

  94. Bazaral, M., Orgel, H.A., and Hamburder, R.N. (1973), Clin. Exp. Immunol. 14, 117–125.

    PubMed  CAS  Google Scholar 

  95. Lynch, N.R., Lopez, R.I., Di Prisco-Fuenmayor, M.C., et al. (1987), Clin. Allergy 17, 199–207.

    Article  PubMed  CAS  Google Scholar 

  96. Shakib, F., Pritchard, D.I., Walsh, E.A., et al. (1993), Parasite Immunol. 15, 47–53.

    PubMed  CAS  Google Scholar 

  97. Fick, Jr. R.B. (1999), Curr. Opin. Pulmon. Med. 5, 76–80.

    Article  Google Scholar 

  98. Milgrom, H., Fick, Jr. R.B., Su, J.Q., et al. (1999), N. Engl. J. Med. 341, 1966–1973.

    Article  PubMed  CAS  Google Scholar 

  99. Ottesen, E.A., Kumaraswami, V., Paranjape, V. R., et al. (1981), J. Immunol. 127, 2014–2020.

    PubMed  CAS  Google Scholar 

  100. Hussain, R., Poindexter, R.W., and Ottesen, E.A. (1992), J. Immunol. 148, 2731–2737.

    PubMed  CAS  Google Scholar 

  101. Culley, F.J., Brown, A., Conroy, D.M., et al. (2000), J. Immunol. 165, 6447–6453.

    PubMed  CAS  Google Scholar 

  102. Chow, S.C., Brown, A., and Pritchard, D. (2000), Parasite Immunol. 22, 21–29.

    Article  PubMed  CAS  Google Scholar 

  103. Pritchard, D.I., Brown, A., Kasper, G., et al. (1999), Parasite Immunol. 21, 21–29.

    Article  Google Scholar 

  104. Maizels, R.M. and Lawrence, R.A. (1991), Parasitol. Today 7, 271–276.

    Article  PubMed  CAS  Google Scholar 

  105. Pascual, C.Y., Crespo, J.F., San Martin, S., et al. (1997), Allergy 52, 514–520.

    PubMed  CAS  Google Scholar 

  106. Johanssen, E., Aponno, M., Lundberg, M., and van Hage-Hamsten, M. (2001), Allergy 56, 660–666.

    Article  Google Scholar 

  107. King, C.L., Medhat, A., Malhotra, I., et al. (1996), J. Immunol. 156, 4715–4721.

    PubMed  CAS  Google Scholar 

  108. Mahanty, S. and T.B. Nutman. (1995), Parasite Immunol. 17, 385–392.

    PubMed  CAS  Google Scholar 

  109. Doetze, A., Satoguina, J., Burchard, G., et al. (2000), Int. Immunol. 12, 623–630.

    Article  PubMed  CAS  Google Scholar 

  110. Macabaus, C., Sly, P.D., Burton, P., et al. (1999), Clin. Exp. Allergy 29, 1233–1231.

    Google Scholar 

  111. Royer, B., Varadaradjalou, S., Saas, P., et al. (2001), Clin. Exp. Immunol. 31, 694–704.

    CAS  Google Scholar 

  112. King, C.L., Kumaraswami, V., Poindexter, R.W., et al. (1992), J. Clin. Invest. 89, 1403–1410.

    Article  PubMed  CAS  Google Scholar 

  113. Shevach, E.M. (2001), J. Exp. Med. 193, F41-F45.

    Article  PubMed  CAS  Google Scholar 

  114. McGuirk, P. and Mills, K.H.G. (2002), Trends Immunol. 23, 450–455.

    Article  PubMed  CAS  Google Scholar 

  115. Sato, M.N., Oliveira, C.R., Futata, E.A., et al. (2002), Clin. Exp. Allergy 32, 1667–1674.

    Article  PubMed  CAS  Google Scholar 

  116. Smith, K.M., Eaton, A.D., Finlayson, L.M. and Garside, P. (2000), Am. J. Respir. Crit. Care Med. 162, S175-S178.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratorio de Investigaciones, Hospital Pedro Vicente Maldonado, Pichincha Province, Ecuador

    Philip J. Cooper

  2. Department of Infectious Diseases, St George’s Hospital Medical School, Tooting, SW17 ORE, London, UK

    Philip J. Cooper

Authors
  1. Philip J. Cooper
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cooper, P.J. The potential impact of early exposures to geohelminth infections on the development of atopy. Clinic Rev Allerg Immunol 26, 5–14 (2004). https://doi.org/10.1385/CRIAI:26:1:5

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1385/CRIAI:26:1:5

Index Entries

Search

Navigation