The Association between Helminth Infections and Atopic Diseases

  • L. A. H. Hermsen
Part of the Advanced Topics in Science and Technology in China book series (ATSTC)


Worldwide, allergies are increasingly becoming a public health problem. Several studies have indicated a relation between allergies and a “western” lifestyle. These observations have contributed to the formulation of the hygiene hypothesis, which suggests that low levels of exposure to infections in early childhood increase the risk of developing allergic diseases, which is mainly due to insufficient stimulation of the Th1 immune response. This is in favor of the Th2 response and results in a higher frequency of chronic diseases like allergies, which are characterized by a specific hyperactive Th2 immune response. Helminth infections and allergens both have similar Th2 immune responses. However, it has been noticed that helminth endemic areas are often associated with a lower prevalence of allergic diseases. Therefore, helminth infections are thought to play an important role in the process of allergic disorders, and indicate a relation between helminth infections and allergens. However, studies showed controversial results with both positive and negative associations between helminths and allergens. This indicates a dual or controversial influence of helminth infections on the immune system. Different studies indicate that helminth infections interfere with the predictive value of diagnostic tests for atopy. Generally, atopy is defined by measuring the total level of IgE by the presence of specific IgE for allergens or by the evidence of hypersensitivity by skin prick test (SPT). However, in developing countries, high serum IgE could also indicate chronic helminth infections. Therefore, the use of serum IgE might lead to conflicting results in atopic diagnostics, especially in areas where helminth infections are endemic. In this chapter, the controversial effects of helminth infections on the occurrence of allergies and on the related consequences for atopy diagnostics will be elaborated, with an emphasis on the situations in countries at different stages of economic development.


Skin Prick Test Helminth Infection Chronic Helminth Infection Human Parasitic Disease 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Buijs, J., Borsboom, G., Renting, M., et al. (1997). Relationship between allergic manifestations and Toxocara seropositivity: A cross-sectional study among elementary school children. Eur Respir J, 10, 1467–1475.PubMedCrossRefGoogle Scholar
  2. Carosso, A., Bugiani, M., Migliore, E., et al. (2007). Reference values of total serum IgE and their significance in the diagnosis of allergy in young european adults. Int Arch Allergy Immunol, 142, 230–238.PubMedCrossRefGoogle Scholar
  3. Cooper, P.J. (2002). Can intestinal helminth infections (geohelminths) affect the development and expression of asthma and allergic disease? Clin Exp Immunol, 128, 398–404.PubMedCrossRefGoogle Scholar
  4. Cooper, P.J., Chico, M.E., Griffin, G.E., et al. (2003). Allergy symptoms, atopy, and geohelminth infections in a rural area of Ecuador. Am J Respir Crit Care Med, 168, 313–317.PubMedCrossRefGoogle Scholar
  5. Cooper, P.J., Chico, M.E., Rodriques, L.C., et al. (2003). Reduced risk of atopy among school-aged children infected with geohelminth parasites in a rural area in the tropics. J Allergy Clin Immunol, 111(5), 995–1000.PubMedCrossRefGoogle Scholar
  6. Cooper, P.J. (2004). Intestinal worms and human allergy. Parasite Immunology, 26, 455–467. Int J Biochem Cell Biol, 38, 1031–1035.PubMedCrossRefGoogle Scholar
  7. Cooper, P.J., Barreto, M.L., Rodrigues, L.C. (2006). Human allergy and geohelminth infections: a review of the literature and a proposed conceptual model to guide the investigation of possible causal association. Brit Med Bulletin, 79–80, 203–218.CrossRefGoogle Scholar
  8. Cooper, P.J., Alexander, N., Moncayo, A.L., et al. (2008). Environmental determinants of total IgE among school children living in the rural Tropics: Importance of geohelminth infection and effect of anthelminth treatment. BMC Immunology, 9, 33.PubMedCrossRefGoogle Scholar
  9. Coordinating Office of the National Survey on the Important Human Parasitic Diseases (2005). A national survey on current status of the important parasitic disease in human population. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi, 23(5 Suppl), 332–340.Google Scholar
  10. Dagoye, D., Bekele, Z., Woldemichael, K., et al. (2003). Wheezing, allergy, and parasite infection in children in urban and rural ethiopia. Am J of Resp and Critical Med, 167, 1369–1373.CrossRefGoogle Scholar
  11. Davey, G., Venn, A., Belete, H., et al. (2005). Wheeze, allergic sensitization and geohelminth infection in Butajira, Ethiopia. Clin Exp Allergy, 35, 301–307.PubMedCrossRefGoogle Scholar
  12. Elliott, A.M., Mpairwe, H., Quigley, M.A., et al. (2005). Helminth infection during pregnancy and development of infantile eczema. JAMA, 294, 2032–2034.PubMedCrossRefGoogle Scholar
  13. Hagel, I., Lynch, N.R., Di Prisco, M.C., et al. (1993). Ascaris reinfection of slum children: Relation with the IgE response. Clin Exp Immunol, 94, 80–83.PubMedCrossRefGoogle Scholar
  14. Hermsen, L.A.H. (2008) Correlations of skin prick test and IgE levels with atopy and atopic disease in Cuban schoolchildren living in helminth endemic areas. MSc thesis.Google Scholar
  15. International Study of Asthma and Allergies in Childhood (ISAAC) Steering Committee (1998). Worldwide variation in prevalence of symptoms of asthma, allergic rhinoconjunctivitis, and atopic eczema. Lancet, 351, 1125–1132.Google Scholar
  16. Leung, R., Wong, G., Lau, J., et al. (1997). Prevalence of asthma and allergy in Hong Kong schoolchildren: An ISAAC study. Eur Respir J, 10, 354–360.PubMedCrossRefGoogle Scholar
  17. Levin, M.E., Le Souëf, P.N., Motala, C. (2008). Total IgE in urban Black South African teenagers: The influence of atopy and helminth infection. Pediatr Allergy Immunol, 22.Google Scholar
  18. Li, T., He, S.Y., Zhao, H., et al. (2010). Major trends in human parasitic diseases in China. Trends in Parasitdogy, 26, 264–270.CrossRefGoogle Scholar
  19. Medeiros, D., Silva, A.R., Rizzo, J.A., et al. (2006). Total IgE level in respiratory allergy: Study of patients at high risk for helminthic infection. Jornal de Pediatria.Google Scholar
  20. Ministry of Health, People’s Democratic Republic of China (2008). Current status and control of schistosomiasis, soil transmitted helminths, foodborne trematodes and echinococcosis in China. Personal communication.Google Scholar
  21. Moncayo, A.L., Cooper, P.J. (2006). Geohelminth infections: Impact on allergic diseases. The International Journal of Biochemistry Cell Biology, 38(7): 1031–1035.PubMedCrossRefGoogle Scholar
  22. Mutius, E. (2004). Influences in allergy: Epidemiology and the environment. American Academy of Allergy, Asthma and Immunology.Google Scholar
  23. Nyan, O.A., Walraven, G.E.L., Banya, W.A.S., et al. (2001). Atopy, intestinal helminth infection and total serum IgE in rural and urban adult Gambian communities. Clin Exp Allergy, 31, 1672–1678.PubMedCrossRefGoogle Scholar
  24. Obihara, C.C., Beyers, N., Gie, R.P., et al. (2006). Respiratory atopic disease, ascaris-immunoglobulin E and tuberculin testing in urban South African children. Clin Exp Allergy, 36, 640–648.PubMedCrossRefGoogle Scholar
  25. Palmer, L.J., Celedon, J.C., Weiss, S.T., et al. (2002). Ascaris lumbricoides infection is associated with increased risk of childhood asthma and atopy in rural China. Am J of Respir Crit Care Med, 165, 1489–1493.CrossRefGoogle Scholar
  26. Rorke, S., Holgate, S.T. (2006). The atopy phenotype revisited. Journal of the American Academy of Dermatology, 54(1), 172–179.CrossRefGoogle Scholar
  27. Scrivener, S., Yemaneberhan, H., Zebenigus, M., et al. (2001). Independent effects of intestinal parasite infection and domestic allergen exposure on risk of wheeze in Ethiopia: A nested case control study. Lancet, 358, 1493–1499.PubMedCrossRefGoogle Scholar
  28. Söderström, L., Kober, A., Ahlstedt, S., et al. (2003). A further evaluation of the clinical use of specific IgE antibody testing in allergic diseases. Allergy, 58, 921–928.PubMedCrossRefGoogle Scholar
  29. Steerenberg, P.A., Loveren, van H., Vandebriel, R.J., et al. (2001). The prevalence of asthma and allergy increases; a world wide problem. RIVM rapport, 640250004.Google Scholar
  30. Strachan, D.P. (1989). Hayfever, hygiene and household size. Brit Med J, 299, 1259–1260.PubMedCrossRefGoogle Scholar
  31. van den Biggelaar, A.H.J.R., van den, R., Rodrigues, L.C., et al. (2000). Decreased atopy in children infected with Schistosoma haematobium: A role for parasite-induced interleukin-10. Lancet, 356, 1723–1727.Google Scholar
  32. van den Biggelaar, van den A.H., Lopuhaa, C., et al. (2001). The prevalence of parasite infestation and House Dust Mite sensitization in Gabonese schoolchildren. Int. Arch Allergy Immunol, 126(3), 231–238.Google Scholar
  33. van Riet, E., Hartgers, F.C., Yazdanbakhsh, M. (2007). Chronic helminth infections induce immunomodulation: Consequences and mechanisms. Immunobiology, 212, 475–490.PubMedCrossRefGoogle Scholar
  34. Wills-Karp, M., Santeliz, J., Karp, C.L. (2001). The germless theory of allergic disease: Revisiting the hygiene hypothesis. Nature Rev Immunol, 1, 69–75.CrossRefGoogle Scholar
  35. Wong, G.W.K., Hui, D.S.C., Chan, H.H., et al. (2001). Prevalence of respiratory and atopic disorders in Chinese schoolchildren. Clinical and Eexperimental Aallergy, 31, 1225–1231.CrossRefGoogle Scholar
  36. Wong, G.W.K., Ko, F.W.S., Hui, D.S.C., et al. (2004). Factors associated with difference in prevalence of asthma in children from three cities in China: Multicentre epidemiological survey. BMJ, 329(7464), 486.PubMedCrossRefGoogle Scholar
  37. Wordemann, M., Diaz, R.J., Heredia, L.M., et al. (2008). Association of atopy, asthma allergic rhinoconjunctivitis, atopic dermatitis and intestinal helminth infections in Cuban children. Trop Med Int Health, 13(2), 180–186.PubMedCrossRefGoogle Scholar
  38. Xu, L.O., Yu, S.H., Jiang, Z.X., et al. (1995). Soiltransmitted helminthiases: Nationwide survey in China. Bull WHO, 73, 507–513.PubMedGoogle Scholar
  39. Yazdanbakhsh, M., et al. (2002). Allergy, parasites and the hygiene hypotheses. Science, 296, 490.PubMedCrossRefGoogle Scholar
  40. Yazdanbakhsh, M., van den Biggelaar, A., Maizels, R.M., et al. (2001). Th2 responses without atopy: Immunoregulation in chronic helminth infections and reduced allergic diseases. Trends Immunol, 22(7).Google Scholar
  41. Yemaneberhan, H., Bekele, Z., Venn, A., et al. (1997). Prevalence of wheeze and asthma and relation to atopy in urban and rural Ethiopia. Lancet, 350(9071), 85–90.PubMedCrossRefGoogle Scholar
  42. Zhou, P., Chen, N., Zhang, R.L., et al. (2008). Food-borne parasitic zoonoses in China: Perspective for control. Trends in Parasitology, 24, 190–196.PubMedCrossRefGoogle Scholar

Copyright information

© Zhejiang University Press, Hangzhou and Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • L. A. H. Hermsen
    • 1
  1. 1.Faculty of Earth and Life ScienceVU University of AmsterdamAmsterdamthe Netherlands

Personalised recommendations