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Helminth-Induced IgE and Protection Against Allergic Disorders

  • Firdaus Hamid
  • Abena S. Amoah
  • Ronald van Ree
  • Maria YazdanbakhshEmail author
Chapter
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 388)

Abstract

The immune response against helminths and allergens is generally characterized by high levels of IgE and increased numbers of Th2 cells, eosinophils, and mast cells, yet the clinical outcome with respect to immediate hypersensitivity and inflammation is clearly not the same. High levels of IgE are seen to allergens during helminth infections; however, these IgE responses do not translate into allergy symptoms. This chapter summarizes the evidence of the association between helminth infections and allergic disorders. It discusses how helminth infection can lead to IgE cross-reactivity with allergens and how this IgE has poor biological activity. This information is important for developing new diagnostic methods and treatments for allergic disorders in low-to-middle-income countries.

Keywords

Skin Prick Test Helminth Infection Mast Cell Degranulation Allergic Disorder Skin Prick Test Positivity 
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.

References

  1. Aalberse RC, Koshte V, Clemens JG (1981) Immunoglobulin E antibodies that crossreact with vegetable foods, pollen, and Hymenoptera venom. J Allergy Clin Immunol 68:356–364PubMedCrossRefGoogle Scholar
  2. Aalberse RC, Akkerdaas J, van Ree R (2001) Cross-reactivity of IgE antibodies to allergens. Allergy 56:478–490PubMedCrossRefGoogle Scholar
  3. Aalberse RC, Stapel SO, Schuurman J et al (2009) Immunoglobulin G4: an odd antibody. Clin Exp Allergy 39:469–477PubMedCrossRefGoogle Scholar
  4. Acevedo N, Caraballo L (2011) IgE cross-reactivity between Ascaris lumbricoides and mite allergens: possible influences on allergic sensitization and asthma. Parasite Immunol 33:309–321PubMedCrossRefGoogle Scholar
  5. Acevedo N, Sanchez J, Erler A et al (2009) IgE cross-reactivity between Ascaris and domestic mite allergens: the role of tropomyosin and the nematode polyprotein ABA-1. Allergy 64:1635–1643PubMedCrossRefGoogle Scholar
  6. Acevedo N, Mohr J, Zakzuk J et al (2013) Proteomic and immunochemical characterization of glutathione transferase as a new allergen of the nematode Ascaris lumbricoides. PLoS ONE 8:e78353PubMedCentralPubMedCrossRefGoogle Scholar
  7. Altmann F (2007) The role of protein glycosylation in allergy. Int Arch Allergy Immunol 142:99–115PubMedCrossRefGoogle Scholar
  8. Amberbir A, Medhin G, Erku W et al (2011) Effects of Helicobacter pylori, geohelminth infection and selected commensal bacteria on the risk of allergic disease and sensitization in 3-year-old Ethiopian children. Clin Exp Allergy 41:1422–1430PubMedCrossRefGoogle Scholar
  9. Amoah AS, Boakye DA, van Ree R et al (2013a) Parasitic worms and allergies in childhood: insights from population studies 2008–2013. Pediatr Allergy Immunol 25:208–217Google Scholar
  10. Amoah AS, Obeng BB, Larbi IA et al (2013b) Peanut-specific IgE antibodies in asymptomatic Ghanaian children possibly caused by carbohydrate determinant cross-reactivity. J Allergy Clin Immunol 132:639–647PubMedCentralPubMedCrossRefGoogle Scholar
  11. Araujo MI, Lopes AA, Medeiros M et al (2000) Inverse association between skin response to aeroallergens and Schistosoma mansoni infection. Int Arch Allergy Immunol 123:145–148PubMedCrossRefGoogle Scholar
  12. Arkestal K, Sibanda E, Thors C et al (2011) Impaired allergy diagnostics among parasite-infected patients caused by IgE antibodies to the carbohydrate epitope galactose-alpha 1,3-galactose. J Allergy Clin Immunol 127:1024–1028PubMedCrossRefGoogle Scholar
  13. Arruda LK, Santos AB (2005) Immunologic responses to common antigens in helminthic infections and allergic disease. Curr Opin Allergy Clin Immunol 5:399–402PubMedCrossRefGoogle Scholar
  14. Arruda LK, Vailes LD, Platts-Mills TA et al (1997) Induction of IgE antibody responses by glutathione S-transferase from the German cockroach (Blattella germanica). J Biol Chem 272:20907–20912PubMedCrossRefGoogle Scholar
  15. Bager P, Arnved J, Ronborg S et al (2010) Trichuris suis ova therapy for allergic rhinitis: a randomized, double-blind, placebo-controlled clinical trial. J Allergy Clin Immunol 125:123–130PubMedCrossRefGoogle Scholar
  16. Bethony J, Brooker S, Albonico M et al (2006) Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 367:1521–1532PubMedCrossRefGoogle Scholar
  17. Burke W, Fesinmeyer M, Reed K et al (2003) Family history as a predictor of asthma risk. Am J Prev Med 24:160–169PubMedCrossRefGoogle Scholar
  18. Carvalho EM, Bastos LS, Araujo MI (2006) Worms and allergy. Parasite Immunol 28:525–534PubMedCrossRefGoogle Scholar
  19. Carvalho KA, de Melo-Neto OP, Magalhaes FB et al (2013) Blomia tropicalis Blo t 5 and Blo t 21 recombinant allergens might confer higher specificity to serodiagnostic assays than whole mite extract. BMC Immunol 14:11PubMedCentralCrossRefGoogle Scholar
  20. Chung CH, Mirakhur B, Chan E et al (2008) Cetuximab-induced anaphylaxis and IgE specific for galactose-alpha-1,3-galactose. N Engl J Med 358:1109–1117PubMedCentralPubMedCrossRefGoogle Scholar
  21. Commins SP, Platts-Mills TA (2013) Delayed anaphylaxis to red meat in patients with IgE specific for galactose alpha-1,3-galactose (alpha-gal). Curr Allergy Asthma Rep 13:72–77PubMedCentralPubMedCrossRefGoogle Scholar
  22. Commins SP, James HR, Kelly LA et al (2011) The relevance of tick bites to the production of IgE antibodies to the mammalian oligosaccharide galactose-alpha-1,3-galactose. J Allergy Clin Immunol 127:1286–1293PubMedCentralPubMedCrossRefGoogle Scholar
  23. Cooper PJ (2009) Interactions between helminth parasites and allergy. Curr Opin Allergy Clin Immunol 9:29–37PubMedCentralPubMedCrossRefGoogle Scholar
  24. Cooper PJ, Chico ME, Bland M et al (2003a) Allergic symptoms, atopy, and geohelminth infections in a rural area of Ecuador. Am J Respir Crit Care Med 168:313–317PubMedCrossRefGoogle Scholar
  25. Cooper PJ, Chico ME, Rodrigues LC et al (2003b) Reduced risk of atopy among school-age children infected with geohelminth parasites in a rural area of the tropics. J Allergy Clin Immunol 111:995–1000PubMedCrossRefGoogle Scholar
  26. Cooper PJ, Chico ME, Rodrigues LC et al (2004) Risk factors for atopy among school children in a rural area of Latin America. Clin Exp Allergy 34:845–852PubMedCrossRefGoogle Scholar
  27. Cooper PJ, Chico ME, Vaca MG et al (2006) Effect of albendazole treatments on the prevalence of atopy in children living in communities endemic for geohelminth parasites: a cluster-randomised trial. Lancet 367:1598–1603PubMedCrossRefGoogle Scholar
  28. Dagoye D, Bekele Z, Woldemichael K et al (2003) Wheezing, allergy, and parasite infection in children in urban and rural Ethiopia. Am J Respir Crit Care Med 167:1369–1373PubMedCrossRefGoogle Scholar
  29. De Knop KJ, Bridts CH, Verweij MM et al (2010) Component-resolved allergy diagnosis by microarray: potential, pitfalls, and prospects. Adv Clin Chem 50:87–101PubMedCrossRefGoogle Scholar
  30. Feary JR, Venn AJ, Mortimer K et al (2010) Experimental hookworm infection: a randomized placebo-controlled trial in asthma. Clin Exp Allergy 40:299–306PubMedCentralPubMedCrossRefGoogle Scholar
  31. Feary J, Britton J, Leonardi-Bee J (2011) Atopy and current intestinal parasite infection: a systematic review and meta-analysis. Allergy 66:569–578PubMedCrossRefGoogle Scholar
  32. Fitzsimmons CM, Falcone FH, Dunne DW (2014) Helminth allergens, parasite-specific IgE, and its protective role in human immunity. Front Immunol 5:61PubMedCentralPubMedCrossRefGoogle Scholar
  33. Flohr C, Tuyen LN, Lewis S et al (2006) Poor sanitation and helminth infection protect against skin sensitization in Vietnamese children: a cross-sectional study. J Allergy Clin Immunol 118:1305–1311PubMedCrossRefGoogle Scholar
  34. Flohr C, Tuyen LN, Quinnell RJ et al (2010) Reduced helminth burden increases allergen skin sensitization but not clinical allergy: a randomized, double-blind, placebo-controlled trial in Vietnam. Clin Exp Allergy 40:131–142PubMedGoogle Scholar
  35. Gadisseur R, Chapelle JP, Cavalier E (2011) A new tool in the field of in-vitro diagnosis of allergy: preliminary results in the comparison of ImmunoCAP(c) 250 with the ImmunoCAP(c) ISAC. Clin Chem Lab Med 49:277–280PubMedCrossRefGoogle Scholar
  36. Godfrey RC (1975) Asthma and IgE levels in rural and urban communities of the Gambia. Clin Allergy 5:201–207PubMedCrossRefGoogle Scholar
  37. Gronlund H, Adedoyin J, Commins SP et al (2009) The carbohydrate galactose-alpha-1,3-galactose is a major IgE-binding epitope on cat IgA. J Allergy Clin Immunol 123(5):1189–1191PubMedCentralPubMedCrossRefGoogle Scholar
  38. Hamid F, Wiria AE, Wammes LJ et al (2013) Risk factors associated with the development of atopic sensitization in Indonesia. PLoS ONE 8:e67064PubMedCentralPubMedCrossRefGoogle Scholar
  39. Jenkins JA, Breiteneder H, Mills EN (2007) Evolutionary distance from human homologs reflects allergenicity of animal food proteins. J Allergy ClinImmunol 120:1399–1405CrossRefGoogle Scholar
  40. Jouvin MH, Kinet JP (2012) Trichuris suis ova: testing a helminth-based therapy as an extension of the hygiene hypothesis. J Allergy Clin Immunol 130:3–10PubMedCrossRefGoogle Scholar
  41. Lancet editorial (1976) Editorial: IgE, parasites, and allergy. Lancet 24:894–895Google Scholar
  42. Larson D, Cooper PJ, Hubner MP et al (2012a) Helminth infection is associated with decreased basophil responsiveness in human beings. J Allergy Clin Immunol 130:270–272PubMedCentralPubMedCrossRefGoogle Scholar
  43. Larson D, Hubner MP, Torrero MN et al (2012b) Chronic helminth infection reduces basophil responsiveness in an IL-10-dependent manner. J Immunol 188:4188–4199PubMedCentralPubMedCrossRefGoogle Scholar
  44. Lynch NR, Hagel I, Perez M et al (1993) Effect of anthelmintic treatment on the allergic reactivity of children in a tropical slum. J Allergy Clin Immunol 92:404–411PubMedCrossRefGoogle Scholar
  45. Lynch NR, Palenque M, Hagel I et al (1997) Clinical improvement of asthma after anthelminthic treatment in a tropical situation. Am J Respir Crit Care Med 156:50–54PubMedCrossRefGoogle Scholar
  46. Lynch NR, Hagel IA, Palenque ME et al (1998) Relationship between helminthic infection and IgE response in atopic and nonatopic children in a tropical environment. J Allergy Clin Immunol 101:217–221PubMedCrossRefGoogle Scholar
  47. Macaubas C, Sly PD, Burton P et al (1999) Regulation of T-helper cell responses to inhalant allergen during early childhood. Clin Exp Allergy 29:1223–1231PubMedCrossRefGoogle Scholar
  48. MacGlashan DW Jr, Bochner BS, Adelman DC et al (1997) Down-regulation of Fc(epsilon)RI expression on human basophils during in vivo treatment of atopic patients with anti-IgE antibody. J Immunol 158:1438–1445PubMedGoogle Scholar
  49. Mari A (2002) IgE to cross-reactive carbohydrate determinants: analysis of the distribution and appraisal of the in vivo and in vitro reactivity. Int Arch Allergy Immunol 129:286–295PubMedCrossRefGoogle Scholar
  50. Mari A, Iacovacci P, Afferni C et al (1999) Specific IgE to cross-reactive carbohydrate determinants strongly affect the in vitro diagnosis of allergic diseases. J Allergy Clin Immunol 103:1005–1011PubMedCrossRefGoogle Scholar
  51. Mari A, Ooievaar-de HP, Scala E et al (2008) Evaluation by double-blind placebo-controlled oral challenge of the clinical relevance of IgE antibodies against plant glycans. Allergy 63:891–896PubMedCrossRefGoogle Scholar
  52. Mitre E, Norwood S, Nutman TB (2005) Saturation of immunoglobulin E (IgE) binding sites by polyclonal IgE does not explain the protective effect of helminth infections against atopy. Infect Immun 73:4106–4111PubMedCentralPubMedCrossRefGoogle Scholar
  53. Mpairwe H, Webb EL, Muhangi L et al (2011) Anthelminthic treatment during pregnancy is associated with increased risk of infantile eczema: randomised-controlled trial results. Pediatr Allergy Immunol 22:305–312PubMedCentralPubMedCrossRefGoogle Scholar
  54. Obeng BB, Amoah AS, Larbi IA et al (2014) Schistosoma infection is negatively associated with mite atopy, but not wheeze and asthma in Ghanaian Schoolchildren. Clin Exp Allergy 44:965–975Google Scholar
  55. Obihara CC, Beyers N, Gie RP et al (2006) Respiratory atopic disease, Ascaris-immunoglobulin E and tuberculin testing in urban South African children. Clin Exp Allergy 36:640–648PubMedCrossRefGoogle Scholar
  56. Palmer LJ, Celedon JC, Weiss ST et al (2002) Ascaris lumbricoides infection is associated with increased risk of childhood asthma and atopy in rural China. Am J Respir Crit Care Med 165:1489–1493PubMedCrossRefGoogle Scholar
  57. Pawankar R, Canonica GW, Holgate ST et al (2011) Introduction and executive summary: allergic diseases as a global public health issue. In: Pawankar R et al (eds) World Allergy Organization (WAO) white book on allergy. pp 11–20Google Scholar
  58. Perzanowski MS, Ng'ang'a LW, Carter MC et al (2002) Atopy, asthma, and antibodies to Ascaris among rural and urban children in Kenya. J Pediatr 140:582–588PubMedCrossRefGoogle Scholar
  59. Ponte EV, Lima F, Araujo MI et al (2006) Skin test reactivity and Der p-induced interleukin 10 production in patients with asthma or rhinitis infected with Ascaris. Ann Allergy Asthma Immunol 96:713–718PubMedCrossRefGoogle Scholar
  60. Priftanji A, Strachan D, Burr M et al (2001) Asthma and allergy in Albania and the UK. Lancet 358:1426–1427PubMedCrossRefGoogle Scholar
  61. Royer B, Varadaradjalou S, Saas P et al (2001) Inhibition of IgE-induced activation of human mast cells by IL-10. Clin Exp Allergy 31:694–704PubMedCrossRefGoogle Scholar
  62. Santiago HC, Bennuru S, Boyd A et al (2011) Structural and immunologic cross-reactivity among filarial and mite tropomyosin: implications for the hygiene hypothesis. J Allergy Clin Immunol 127:479–486PubMedCentralPubMedCrossRefGoogle Scholar
  63. Santiago HC, LeeVan E, Bennuru S et al (2012) Molecular mimicry between cockroach and helminth glutathione S-transferases promotes cross-reactivity and cross-sensitization. J Allergy Clin Immunol 130:248–256PubMedCentralPubMedCrossRefGoogle Scholar
  64. Santos AB, Rocha GM, Oliver C et al (2008) Cross-reactive IgE antibody responses to tropomyosins from Ascaris lumbricoides and cockroach. J Allergy Clin Immunol 121:1040–1046PubMedCrossRefGoogle Scholar
  65. Satoguina JS, Adjobimey T, Arndts K et al (2008) Tr1 and naturally occurring regulatory T cells induce IgG4 in B cells through GITR/GITR-L interaction, IL-10 and TGF-beta. Eur J Immunol 38:3101–3113PubMedCrossRefGoogle Scholar
  66. 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 358:1493–1499PubMedCrossRefGoogle Scholar
  67. Sereda MJ, Hartmann S, Lucius R (2008) Helminths and allergy: the example of tropomyosin. Trends Parasitol 24:272–278PubMedCrossRefGoogle Scholar
  68. Sheehan D, Meade G, Foley VM et al (2001) Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. Biochem J 360:1–16PubMedCentralPubMedCrossRefGoogle Scholar
  69. Smits HH, Hammad H, van Nimwegen M et al (2007) Protective effect of Schistosoma mansoni infection on allergic airway inflammation depends on the intensity and chronicity of infection. J Allergy Clin Immunol 120:932–940PubMedCrossRefGoogle Scholar
  70. Smits HH, Everts B, Hartgers FC et al (2010) Chronic helminth infections protect against allergic diseases by active regulatory processes. Curr Allergy Asthma Rep 10:3–12PubMedCentralPubMedCrossRefGoogle Scholar
  71. Supali T, Djuardi Y, Wibowo H et al (2010) Relationship between different species of helminths and atopy: a study in a population living in helminth-endemic area in Sulawesi, Indonesia. Int Arch Allergy Immunol 153:388–394PubMedCrossRefGoogle Scholar
  72. Treudler R, Simon JC (2013) Overview of component resolved diagnostics. Curr Allergy Asthma Rep 13:110–117PubMedCrossRefGoogle Scholar
  73. Valenta R, Niederberger V (2007) Recombinant allergens for immunotherapy. J Allergy Clin Immunol 119:826–830PubMedCrossRefGoogle Scholar
  74. Valenta R, Lidholm J, Niederberger V et al (1999) The recombinant allergen-based concept of component-resolved diagnostics and immunotherapy (CRD and CRIT). Clin Exp Allergy 29:896–904PubMedCrossRefGoogle Scholar
  75. Valmonte GR, Cauyan GA, Ramos JD (2012) IgE cross-reactivity between house dust mite allergens and Ascaris lumbricoides antigens. Asia Pac Allergy 2:35–44PubMedCentralPubMedCrossRefGoogle Scholar
  76. van den Biggelaar AH, van Ree R, Rodrigues LC et al (2000) Decreased atopy in children infected with Schistosoma haematobium: a role for parasite-induced interleukin-10. Lancet 356:1723–1727PubMedCrossRefGoogle Scholar
  77. van den Biggelaar AH, Lopuhaa C, van Ree R et al (2001) The prevalence of parasite infestation and house dust mite sensitization in Gabonese schoolchildren. Int Arch Allergy Immunol 126:231–238PubMedCrossRefGoogle Scholar
  78. van der Veen MJ, van Ree R, Aalberse RC et al (1997) Poor biologic activity of cross-reactive IgE directed to carbohydrate determinants of glycoproteins. J Allergy Clin Immunol 100:327–334PubMedCrossRefGoogle Scholar
  79. van Ree R, Cabanes-Macheteau M, Akkerdaas J et al (2000) Beta(1,2)-xylose and alpha(1,3)-fucose residues have a strong contribution in IgE binding to plant glycoallergens. J Biol Chem 275:11451–11458PubMedCrossRefGoogle Scholar
  80. von Mutius E (2002) Environmental factors influencing the development and progression of pediatric asthma. J Allergy ClinImmunol 109:S525–S532CrossRefGoogle Scholar
  81. Wilson MS, Taylor MD, Balic A et al (2005) Suppression of allergic airway inflammation by helminth-induced regulatory T cells. J Exp Med 202:1199–1212PubMedCentralPubMedCrossRefGoogle Scholar
  82. Wiria AE, Hamid F, Wammes LJ et al (2013) The effect of three-monthly albendazole treatment on malarial parasitemia and allergy: a household-based cluster-randomized, double-blind, placebo-controlled trial. PLoS ONE 8:e57899PubMedCentralPubMedCrossRefGoogle Scholar
  83. Wright V, Bickle Q (2005) Immune responses following experimental human hookworm infection. Clin Exp Immunol 142:398–403PubMedCentralPubMedCrossRefGoogle Scholar
  84. Yazdanbakhsh M, van den Biggelaar A, Maizels RM (2001) Th2 responses without atopy: immunoregulation in chronic helminth infections and reduced allergic disease. Trends Immunol 22:372–377PubMedCrossRefGoogle Scholar
  85. Yazdanbakhsh M, Kremsner PG, van Ree R (2002) Allergy, parasites, and the hygiene hypothesis. Science 296:490–494PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Firdaus Hamid
    • 1
    • 2
  • Abena S. Amoah
    • 2
    • 3
  • Ronald van Ree
    • 4
  • Maria Yazdanbakhsh
    • 2
    Email author
  1. 1.Department of Microbiology, Faculty of MedicineHasanuddin UniversityMakassarIndonesia
  2. 2.Department of ParasitologyLeiden University Medical CenterLeidenThe Netherlands
  3. 3.Department of ParasitologyNoguchi Memorial Institute for Medical ResearchAccraGhana
  4. 4.Department of Experimental Immunology and Department of Otorhinolaryngology, Academic Medical CenterAmsterdam UniversityAmsterdamThe Netherlands

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