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Parasites and the hygiene hypothesis

Regulating the immune system?

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Abstract

The hygiene hypothesis proposes that the stimulation of the immune system by microbes or microbial products protects from the development of inflammatory diseases; therefore a reduced exposure to infectious agents may explain the rise in allergic and autoimmune diseases in industrialized countries. The contribution of studies on parasites and allergy to our understanding of the hygiene hypothesis has been two-fold. First, several studies have shown an inverse association between exposure to (Toxplasma gondii) or harbouring of parasites (Schistosoma or Intestinal helminths) and allergy. Second, the mechanisms behind such protective effects have provided new insights and theories on the ability of parasite derived molecules to down-regulate immune responses and thereby to control inflammatory diseases such as allergies. In this review, recent findings and new concepts relating to the associations between parasites and allergies at the epidemiological, cellular and molecular level are discussed.

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References

  1. Gerrard, J.W., Geddes, C.A., Reggin, P.L., et al. (1976), Ann. Allergy 37, 91–100.

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  3. ISAAC (1998), Lancet 351, 1225–1232.

    Article  Google Scholar 

  4. Faniran, A.O., Peat, J.K., and Woolcock, A.J. (1999), Thorax 54, 606–610.

    Article  PubMed  CAS  Google Scholar 

  5. Bjorksten, B., Dumitrascu, D., Foucard, T., et al. (1998), Eur. Respir. J. 12, 432–437.

    Article  PubMed  CAS  Google Scholar 

  6. von Mutius, E., Martinez, F.D., Fritzsch, C., et al. (1994), Am. J. Respir. Crit. Care Med. 149, 358–364.

    Google Scholar 

  7. Priftanji, A., Strachan, D., Burr, M., et al. (2001), Lancet 358, 1426–1427.

    Article  PubMed  CAS  Google Scholar 

  8. Kramer, U., Heinrich, J., Wjst, M., and Wichmann, H. E. (1999), Lancet 353, 450–454.

    Article  PubMed  CAS  Google Scholar 

  9. Alm, J.S., Swartz, J., Lilja, G., et al. (1999), Lancet 353, 1485–1488.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  12. Matricardi, P.M., Rosmini, F., Riondino, S., et al. (2000), Br. Med. J. 320, 412–417.

    Article  CAS  Google Scholar 

  13. Matricardi, P.M., Rosmini, F., Rapicetta, M., et al. (1999), Lancet 354, 430.

    Article  PubMed  CAS  Google Scholar 

  14. Matricardi, P.M., Rosmini, F., Panetta, V., et al. (2002), J. Allergy Clin. Immunol. 110, 381–387.

    Article  PubMed  Google Scholar 

  15. Linneberg, A., Ostergaard, C., Tvede, M., et al. (2003), J. Allergy Clin. Immunol. 111, 847–853.

    Article  PubMed  CAS  Google Scholar 

  16. McIntire, J.J., Umetsu, S.E., Akbari, O., et al. (2001), Nat. Immunol. 2, 1109–1116.

    Article  PubMed  CAS  Google Scholar 

  17. Sepp, E., Julge, K., Vasar, M., et al. (1997), Acta Paediatr. 86, 956–961.

    PubMed  CAS  Google Scholar 

  18. Wold, A.E. (1998), Allergy 53, 20–25.

    PubMed  CAS  Google Scholar 

  19. Adlerberth, I., Jalil, F., Carlsson, B., et al. (1998), Epidemiol. Infect. 121, 587–598.

    Article  PubMed  CAS  Google Scholar 

  20. Adlerberth, I., Carlsson, B., de Man, P., et al. (1991), Acta Paediatr. Scand. 80, 602–610.

    PubMed  CAS  Google Scholar 

  21. Wannemuehler, M.J., Kiyono, H., Babb, J.L., et al. (1982), J. Immunol. 129, 959–965.

    PubMed  CAS  Google Scholar 

  22. Bluestone, J.A. and Abbas, A.K. (2003), Nat. Rev. Immunol. 3, 253–257.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  24. Lynch, N.R., Hagel, I., Perez, M., et al. (1993), J. Allergy Clin. Immunol. 92, 404–411.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  27. Cooper, P.J., Chico, M.E., Bland, M., et al. (2003), J. Allergy Clin. Immunol. 111, 995–1000.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  29. Araujo, M.I., Lopes, A.A., Medeiros, M., et al. (2000), Int. Arch. Allergy Immunol. 123, 145–148.

    Article  PubMed  CAS  Google Scholar 

  30. Buijs, J., Borsboom, G., van Gemund, J.J., et al. (1994), Am. J. Epidemiol. 140, 839–847.

    PubMed  CAS  Google Scholar 

  31. Yazdanbakhsh, M., van den, B. A., and Maizels, R.M. (2001), Trends Immunol. 22, 372–377.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  34. van den Biggelaar, A.H.J., Rodrigues, L.C., van Ree, R., et al. (2004), J. Infect. Dis. in press.

  35. Barton, G.M. and Medzhitov, R. (2002), Curr. Top. Microbiol. Immunol. 270, 81–92.

    PubMed  CAS  Google Scholar 

  36. Akira, S., Takeda, K., and Kaisho, T. (2001), Nat. Immunol. 2, 675–680.

    Article  PubMed  CAS  Google Scholar 

  37. Aliberti, J., Serhan, C., and Sher, A. (2002), J. Exp. Med. 196, 1253–1262.

    Article  PubMed  CAS  Google Scholar 

  38. Allen, J.E. and Maizels, R.M. (1996), Int. Arch. Allergy Immunol. 109, 3–10.

    Article  PubMed  CAS  Google Scholar 

  39. MacGlashan, D.W., Jr., Bochner, B.S., Adelman, D.C., et al. (1997), J. Immunol. 158, 1438–1445.

    PubMed  CAS  Google Scholar 

  40. de Jong, E.C., Vieira, P.L., Kalinski, P., et al. (2002), J. Immunol. 168, 1704–1709.

    PubMed  Google Scholar 

  41. Okano, M., Satoskar, A.R., Nishizaki, K., et al. (1999), J. Immunol. 163, 6712–6717.

    PubMed  CAS  Google Scholar 

  42. Okano, M., Satoskar, A.R., Nishizaki, K., and Harn, D.A., Jr. (2001), J. Immunol. 167, 442–450.

    PubMed  CAS  Google Scholar 

  43. van der Kleij, D., Latz, E., Brouwers, J.F., et al. (2002), J. Biol. Chem. 277, 48,122–48,129.

    Article  Google Scholar 

  44. Mottet, C., Uhlig, H.H., and Powrie, F. (2003), J. Immunol. 170, 3939–3943.

    PubMed  CAS  Google Scholar 

  45. Jeannel, D., Niel, G., Costagliola, D., et al. (1988), Int. J. Epidemiol. 17, 595–602.

    Article  PubMed  CAS  Google Scholar 

  46. Walker, J., Nokes, D.J., and Jennings, R. (1992), Epidemiol. Infect. 108, 99–106.

    Article  PubMed  CAS  Google Scholar 

  47. Nokes, D.J., Forsgren, M., Gille, E., and Ljungstrom, I. (1993), Parasitology 107, 33–40.

    Article  PubMed  Google Scholar 

  48. Elliott, D.E., Urban, J.F., Jr., Argo, C.K., and Weinstock, J.V. (2000), FASEB J. 14, 1848–1855.

    Article  PubMed  CAS  Google Scholar 

  49. Platts-Mills, T.A., Woodfolk, J.A., and Sporik, R.B. (2001), Am. J. Respir. Crit. Care Med. 164, 1107–1108.

    PubMed  CAS  Google Scholar 

  50. Schuurmans Stekhoven, J.H. (1931), Ned Tijd v Geneeskunde 75, 859–873.

    Google Scholar 

  51. Holt, P.G. (1995), Pediatr. Allergy Immunol. 6, 1–10.

    PubMed  Google Scholar 

  52. Romagnani, S. (1994), Curr. Opin. Immunol. 6, 838–846.

    Article  PubMed  CAS  Google Scholar 

  53. Stene, L.C. and Nafstad, P. (2001), Lancet 357, 607–608.

    Article  PubMed  CAS  Google Scholar 

  54. Holt, P.G., Macaubas, C., Stumbles, P.A., and Sly, P.D. (1999), Nature 402, B12-B17.

    Article  PubMed  CAS  Google Scholar 

  55. Nakagomi, T., Itaya, H., Tominaga, T., et al. (1994), Lancet 343, 121–122.

    Article  PubMed  CAS  Google Scholar 

  56. Krause, T., Koch, A., Friborg, J., et al. (2002), Lancet 360, 691–692.

    Article  PubMed  Google Scholar 

  57. Platts-Mills, T., Vaughan, J., Squillace, S., et al. (2001), Lancet 357, 752–756.

    Article  PubMed  CAS  Google Scholar 

  58. Jeannin, P., Lecoanet, S., Delneste, Y., et al. (1998), J. Immunol. 160, 3555–3561.

    PubMed  CAS  Google Scholar 

  59. Royer, B., Varadaradjalou, S., Saas, P., Guillosson, J.J., Kantelip, J.P., and Arock, M. (2001), Clin. Exp. Allergy 31, 694–704.

    Article  PubMed  CAS  Google Scholar 

  60. Koppelman, B., Neefjes, J.J., de Vries, J.E., and de Waal, M.R. (1997), Immunity 7, 861–871.

    Article  PubMed  CAS  Google Scholar 

  61. Akbari, O., DeKruyff, R.H., and Umetsu, D.T. (2001), Nat. Immunol. 2, 725–731.

    Article  PubMed  CAS  Google Scholar 

  62. Brown, V., Warke, T.J., Shields, M.D., and Ennis, M. (2003), Thorax 58, 311–316.

    Article  PubMed  CAS  Google Scholar 

  63. Hansen, G., Berry, G., DeKruyff, R.H., and Umetsu, D.T. (1999), J. Clin. Invest. 103, 175–183.

    Article  PubMed  CAS  Google Scholar 

  64. Zuany-Amorim, C., Manlius, C., Trifilieff, A., et al. (2002), J. Immunol. 169, 1492–1499.

    PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Parasitology, Leiden University Medical Center, Leiden, The Netherlands

    Maria Yazdanbakhsh

  2. Allergy and Asthma Research Unit, Ospedale Pediatrico Bambino Gesu Research Institute (IRCCS), Rome, Italy

    Paolo M. Matricardi

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  1. Maria Yazdanbakhsh
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  2. Paolo M. Matricardi
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Correspondence to Maria Yazdanbakhsh.

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Yazdanbakhsh, M., Matricardi, P.M. Parasites and the hygiene hypothesis. Clinic Rev Allerg Immunol 26, 15–23 (2004). https://doi.org/10.1385/CRIAI:26:1:15

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  • DOI: https://doi.org/10.1385/CRIAI:26:1:15

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