Asia Pac Allergy.  2012 Apr;2(2):122-128. 10.5415/apallergy.2012.2.2.122.

Impact of helminth infection on childhood allergic diseases in an area in transition from high to low infection burden

Affiliations
  • 1Department of Physiology, Faculty of Medicine, University of Kelaniya, Ragama 11010, Sri Lanka. manori_a@yahoo.com
  • 2Department of Parasitology, Faculty of Medicine, University of Kelaniya, Ragama 11010, Sri Lanka.
  • 3Department of Allergy, Immunology and Respiratory Medicine, Alfred Hospital, Melbourne VIC 3004, Australia.

Abstract

BACKGROUND
The effect of helminth infections on allergic diseases is still inconclusive. Furthermore, the effect of helminth infections on childhood allergic diseases in a tropical area where prevalence of helminth infections has undergone dramatic changes is not well documented.
OBJECTIVE
To investigate the relationship between allergic diseases and helminth infection in a cohort of schoolchildren in an area that has undergone dramatic changes in intensity of helminth infections.
METHODS
Children attending grade 5 were recruited from 17 schools in Western Province of Sri Lanka. They were assessed for allergic diseases using the International Study of Asthma and Allergies in Childhood questionnaire. Their serum total IgE (tIgE) and allergen-specific IgE (sIgE) for five common aeroallergens were measured by ImmunoCAP® method and stools were examined for the presence of helminth infections.
RESULTS
A total of 640 children (mean age 10 years) were recruited to the study. Of them, 33.7% had evidence of allergic disease and 15.5% had helminth infections. Majority of infections (68.9%) were of low intensity. A significant relationship between allergic disease and helminth infections was not observed, however, a trend toward protective role of helminth infections against allergic diseases was noted. Multivariate analysis showed helminth infections to be an independent predictor of high tIgE levels whereas allergic disease was not. Allergic sensitization (atopy) was a significant risk factor for allergic disease only among non-infected children (odds ratio 3.025, p = 0.022) but not in infected children. The ratio of sIgE to tIgE was higher in non-infected children.
CONCLUSION
Though not significant, a reduced risk of allergy in helminth-infected children was observed in this population. A Decrease in intensity of helminth infections may have contributed to the reduced capacity of immune-modulation by helminths in this paediatric population.

Keyword

Allergy; Atopy; Children; IgE; Helminth infections

MeSH Terms

Asthma
Child
Cohort Studies
Helminths*
Humans
Hypersensitivity
Immunoglobulin E
Methods
Multivariate Analysis
Prevalence
Risk Factors
Sri Lanka
Immunoglobulin E

Figure

  • Fig. 1 Ratio of allergen-specific IgE (sIgE) to total IgE (tIgE) for different allergens in infected and uninfected children. Vertical bars represent the mean and 95% confidence interval.


Cited by  1 articles

Asia Pacific Allergy: a successful first year and the future
Yoon-Seok Chang
Asia Pac Allergy. 2012;2(2):91-92.    doi: 10.5415/apallergy.2012.2.2.91.


Reference

1. Strachan DP. Hay fever, hygiene, and household size. BMJ. 1989. 299:1259–1260.
Article
2. Shirakawa T, Enomoto T, Shimazu S, Hopkin JM. The inverse association between tuberculin responses and atopic disorder. Science. 1997. 275:77–79.
Article
3. Shaheen SO, Aaby P, Hall AJ, Barker DJ, Heyes CB, Shiell AW, Goudiaby A. Measles and atopy in Guinea-Bissau. Lancet. 1996. 347:1792–1796.
Article
4. Matricardi PM, Rosmini F, Riondino S, Fortini M, Ferrigno L, Rapicetta M, Bonini S. Exposure to foodborne and orofecal microbes versus airborne viruses in relation to atopy and allergic asthma: epidemiological study. BMJ. 2000. 320:412–417.
Article
5. Leonardi-Bee J, Pritchard D, Britton J. Asthma and current intestinal parasite infection: systematic review and meta-analysis. Am J Respir Crit Care Med. 2006. 174:514–523.
6. Cooper PJ. Intestinal worms and human allergy. Parasite Immunol. 2004. 26:455–467.
Article
7. Smits HH, Everts B, Hartgers FC, Yazdanbakhsh M. Chronic helminth infections protect against allergic diseases by active regulatory processes. Curr Allergy Asthma Rep. 2010. 10:3–12.
Article
8. Calvert J, Burney P. Ascaris, atopy, and exercise-induced bronchoconstriction in rural and urban South African children. J Allergy Clin Immunol. 2010. 125:100–105.e1-e5.
Article
9. Rodrigues LC, Newcombe PJ, Cunha SS, Alcantara-Neves NM, Genser B, Cruz AA, Simoes SM, Fiaccone R, Amorim L, Cooper PJ, Barreto ML. Early infection with Trichuris trichiura and allergen skin test reactivity in later childhood. Clin Exp Allergy. 2008. 38:1769–1777.
Article
10. Amarasekera ND, Gunawardena NK, de Silva NR, Weerasinghe A. Prevalence of childhood atopic diseases in the Western Province of Sri Lanka. Ceylon Med J. 2010. 55:5–8.
Article
11. WHO. Bench aids for the diagnosis of intestinal parasites. 1994. Geneva: World Health Organization.
12. Medical Statistics Unit, Ministry of Health Sri Lanka. Annual Health Bulletin of Sri Lanka. 2004. Colombo: Ministry of Health Sri Lanka.
13. Pathmeswaran A, Jayatissa R, Samarasinghe S, Fernando A, de Silva RP, Thattil RO, de Silva NR. Health status of primary schoolchildren in Sri Lanka. Ceylon Med J. 2005. 50:46–50.
Article
14. Asher MI, Montefort S, Björkstén B, Lai CK, Strachan DP, Weiland SK, Williams H. Worldwide time trends in the prevalence of symptoms of asthma, allergic rhinoconjunctivitis, and eczema in childhood: ISAAC Phases One and Three repeat multicountry cross-sectional surveys. Lancet. 2006. 368:733–743.
Article
15. Sherrill DL, Stein R, Halonen M, Holberg CJ, Wright A, Martinez FD. Total serum IgE and its association with asthma symptoms and allergic sensitization among children. J Allergy Clin Immunol. 1999. 104:28–36.
Article
16. Sunyer J, Antó JM, Castellsagué J, Soriano JB, Roca J. Total serum IgE is associated with asthma independently of specific IgE levels. The Spanish Group of the European Study of Asthma. Eur Respir J. 1996. 9:1880–1884.
17. Backer V, Ulrik CS, Wendelboe D, Bach-Mortensen N, Hansen KK, Laursen EM, Dirksen A. Distribution of serum IgE in children and adolescents aged 7 to 16 years in Copenhagen, in relation to factors of importance. Allergy. 1992. 47:484–489.
Article
18. Levin ME, Le Souëf PN, Motala C. Total IgE in urban Black South African teenagers: the influence of atopy and helminth infection. Pediatr Allergy Immunol. 2008. 19:449–454.
Article
19. Wilson PB, Fairfield JE, Beech N. Detection of IgG subclass-specific anti-IgE antibodies in normal and atopic individuals. Int Arch Allergy Appl Immunol. 1987. 84:198–204.
Article
20. Wickman M, Ahlstedt S, Lilja G, van Hage Hamsten M. Quantification of IgE antibodies simplifies the classification of allergic diseases in 4-year-old children. A report from the prospective birth cohort study--BAMSE. Pediatr Allergy Immunol. 2003. 14:441–447.
21. Cooper PJ, Chico ME, Bland M, Griffin GE, Nutman TB. Allergic symptoms, atopy, and geohelminth infections in a rural area of Ecuador. Am J Respir Crit Care Med. 2003. 168:313–317.
Article
22. Yemaneberhan H, Bekele Z, Venn A, Lewis S, Parry E, Britton J. Prevalence of wheeze and asthma and relation to atopy in urban and rural Ethiopia. Lancet. 1997. 350:85–90.
Article
23. Nyan OA, Walraven GE, Banya WA, Milligan P, Van Der Sande M, Ceesay SM, Del Prete G, McAdam KP. Atopy, intestinal helminth infection and total serum IgE in rural and urban adult Gambian communities. Clin Exp Allergy. 2001. 31:1672–1678.
Article
24. Cooper PJ, Alexander N, Moncayo AL, Benitez SM, Chico ME, Vaca MG, Griffin GE. Environmental determinants of total IgE among school children living in the rural Tropics: importance of geohelminth infections and effect of anthelmintic treatment. BMC Immunol. 2008. 9:33.
Article
25. Graves PE, Kabesch M, Halonen M, Holberg CJ, Baldini M, Fritzsch C, Weiland SK, Erickson RP, von Mutius E, Martinez FD. A cluster of seven tightly linked polymorphisms in the IL-13 gene is associated with total serum IgE levels in three populations of white children. J Allergy Clin Immunol. 2000. 105:506–513.
Article
26. Marsh DG, Neely JD, Breazeale DR, Ghosh B, Freidhoff LR, Ehrlich-Kautzky E, Schou C, Krishnaswamy G, Beaty TH. Linkage analysis of IL4 and other chromosome 5q31.1 markers and total serum immunoglobulin E concentrations. Science. 1994. 264:1152–1156.
27. Yazdanbakhsh M, Kremsner PG, van Ree R. Allergy, parasites, and the hygiene hypothesis. Science. 2002. 296:490–494.
Article
Full Text Links
  • APA
Actions
Cited
CITED
export Copy
Close
Share
  • Twitter
  • Facebook
Similar articles
Copyright © 2024 by Korean Association of Medical Journal Editors. All rights reserved.     E-mail: koreamed@kamje.or.kr