Reduced helminth burden increases allergen skin sensitization but not clinical allergy: a randomized, double‐blind, placebo‐controlled trial in Vietnam

<p style="text-align:justify;"> <b>Background:</b> Observational evidence suggests that infection with helminths protects against allergic disease and allergen skin sensitization. It is postulated that such effects are mediated by helminth‐induced cytokine responses, in...

Descripción completa

Detalles Bibliográficos
Autores principales: Flohr, C, Tuyen, L, Quinnell, R, Lewis, S, Minh, T, Campbell, J, Simmons, C, Telford, G, Brown, A, Hien, T, Farrar, J, Williams, H, Pritchard, D, Britton, J
Formato: Journal article
Lenguaje:English
Publicado: Blackwell Publishing 2009
_version_ 1826279608728682496
author Flohr, C
Tuyen, L
Quinnell, R
Lewis, S
Minh, T
Campbell, J
Simmons, C
Telford, G
Brown, A
Hien, T
Farrar, J
Williams, H
Pritchard, D
Britton, J
author_facet Flohr, C
Tuyen, L
Quinnell, R
Lewis, S
Minh, T
Campbell, J
Simmons, C
Telford, G
Brown, A
Hien, T
Farrar, J
Williams, H
Pritchard, D
Britton, J
author_sort Flohr, C
collection OXFORD
description <p style="text-align:justify;"> <b>Background:</b> Observational evidence suggests that infection with helminths protects against allergic disease and allergen skin sensitization. It is postulated that such effects are mediated by helminth‐induced cytokine responses, in particular IL‐10.<br/> <b>Objective:</b> We tested this hypothesis in a rural area of central Vietnam where hookworm infection is endemic.<br/> <b>Methods:</b> One thousand five hundred and sixty‐six schoolchildren aged 6–17 were randomly allocated to receive either anti‐helminthic therapy or a placebo at 0, 3, 6, and 9 months. We compared changes in the prevalence of exercise‐induced bronchoconstriction, allergen skin sensitization, flexural eczema on skin examination, questionnaire‐reported allergic disease (wheeze and rhinitis symptoms), and immunological parameters (hookworm‐induced IFN‐γ, IL‐5, IL‐10) between 0 and 12 months.<br/> <b>Results:</b> One thousand four hundred and eighty‐seven children (95% of these randomized) completed the study. The most common helminth infections were hookworm (65%) and Ascaris lumbricoides (7%). There was no effect of the therapy on the primary outcome, exercise‐induced bronchoconstriction (within‐participant mean percent fall in peak flow from baseline after anti‐helminthic treatment 2.25 (SD 7.3) vs. placebo 2.19 (SD 7.8, P=0.9), or on the prevalence of questionnaire‐reported wheeze [adjusted odds ratio (OR)=1.16, 95% confidence interval (CI) 0.35–3.82, P=0.8] and rhinitis (adjusted OR=1.39, 0.89–2.15, P=0.1), or flexural dermatitis on skin examination (adjusted OR=1.15, 0.39–3.45, P=0.8). However, anti‐helminthic therapy was associated with a significantly higher allergen skin sensitization risk (adjusted OR=1.31, 1.02–1.67, P=0.03). This effect was particularly strong for children infected with A. lumbricoides at baseline (adjusted OR=4.90, 1.48–16.19, P=0.009). Allergen skin sensitization was inversely related to hookworm‐specific IL‐10 at baseline (adjusted OR=0.76, 0.59–0.99, P=0.04). No cytokine tested, including IL‐10, changed significantly after the anti‐helminthic therapy compared with the placebo.<br/> <b>Conclusion:</b> A significant reduction in worm burden over a 12‐month period in helminth‐infected children increases the risk of allergen skin sensitization but not of clinical allergic disease. The effect on skin sensitization could not be fully explained by any of the immunological parameters tested. </p>
first_indexed 2024-03-07T00:01:18Z
format Journal article
id oxford-uuid:760caff0-1be7-4aa4-ac65-5fc147a93f87
institution University of Oxford
language English
last_indexed 2024-03-07T00:01:18Z
publishDate 2009
publisher Blackwell Publishing
record_format dspace
spelling oxford-uuid:760caff0-1be7-4aa4-ac65-5fc147a93f872022-03-26T20:13:09ZReduced helminth burden increases allergen skin sensitization but not clinical allergy: a randomized, double‐blind, placebo‐controlled trial in VietnamJournal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:760caff0-1be7-4aa4-ac65-5fc147a93f87EnglishSymplectic Elements at OxfordBlackwell Publishing2009Flohr, CTuyen, LQuinnell, RLewis, SMinh, TCampbell, JSimmons, CTelford, GBrown, AHien, TFarrar, JWilliams, HPritchard, DBritton, J <p style="text-align:justify;"> <b>Background:</b> Observational evidence suggests that infection with helminths protects against allergic disease and allergen skin sensitization. It is postulated that such effects are mediated by helminth‐induced cytokine responses, in particular IL‐10.<br/> <b>Objective:</b> We tested this hypothesis in a rural area of central Vietnam where hookworm infection is endemic.<br/> <b>Methods:</b> One thousand five hundred and sixty‐six schoolchildren aged 6–17 were randomly allocated to receive either anti‐helminthic therapy or a placebo at 0, 3, 6, and 9 months. We compared changes in the prevalence of exercise‐induced bronchoconstriction, allergen skin sensitization, flexural eczema on skin examination, questionnaire‐reported allergic disease (wheeze and rhinitis symptoms), and immunological parameters (hookworm‐induced IFN‐γ, IL‐5, IL‐10) between 0 and 12 months.<br/> <b>Results:</b> One thousand four hundred and eighty‐seven children (95% of these randomized) completed the study. The most common helminth infections were hookworm (65%) and Ascaris lumbricoides (7%). There was no effect of the therapy on the primary outcome, exercise‐induced bronchoconstriction (within‐participant mean percent fall in peak flow from baseline after anti‐helminthic treatment 2.25 (SD 7.3) vs. placebo 2.19 (SD 7.8, P=0.9), or on the prevalence of questionnaire‐reported wheeze [adjusted odds ratio (OR)=1.16, 95% confidence interval (CI) 0.35–3.82, P=0.8] and rhinitis (adjusted OR=1.39, 0.89–2.15, P=0.1), or flexural dermatitis on skin examination (adjusted OR=1.15, 0.39–3.45, P=0.8). However, anti‐helminthic therapy was associated with a significantly higher allergen skin sensitization risk (adjusted OR=1.31, 1.02–1.67, P=0.03). This effect was particularly strong for children infected with A. lumbricoides at baseline (adjusted OR=4.90, 1.48–16.19, P=0.009). Allergen skin sensitization was inversely related to hookworm‐specific IL‐10 at baseline (adjusted OR=0.76, 0.59–0.99, P=0.04). No cytokine tested, including IL‐10, changed significantly after the anti‐helminthic therapy compared with the placebo.<br/> <b>Conclusion:</b> A significant reduction in worm burden over a 12‐month period in helminth‐infected children increases the risk of allergen skin sensitization but not of clinical allergic disease. The effect on skin sensitization could not be fully explained by any of the immunological parameters tested. </p>
spellingShingle Flohr, C
Tuyen, L
Quinnell, R
Lewis, S
Minh, T
Campbell, J
Simmons, C
Telford, G
Brown, A
Hien, T
Farrar, J
Williams, H
Pritchard, D
Britton, J
Reduced helminth burden increases allergen skin sensitization but not clinical allergy: a randomized, double‐blind, placebo‐controlled trial in Vietnam
title Reduced helminth burden increases allergen skin sensitization but not clinical allergy: a randomized, double‐blind, placebo‐controlled trial in Vietnam
title_full Reduced helminth burden increases allergen skin sensitization but not clinical allergy: a randomized, double‐blind, placebo‐controlled trial in Vietnam
title_fullStr Reduced helminth burden increases allergen skin sensitization but not clinical allergy: a randomized, double‐blind, placebo‐controlled trial in Vietnam
title_full_unstemmed Reduced helminth burden increases allergen skin sensitization but not clinical allergy: a randomized, double‐blind, placebo‐controlled trial in Vietnam
title_short Reduced helminth burden increases allergen skin sensitization but not clinical allergy: a randomized, double‐blind, placebo‐controlled trial in Vietnam
title_sort reduced helminth burden increases allergen skin sensitization but not clinical allergy a randomized double blind placebo controlled trial in vietnam
work_keys_str_mv AT flohrc reducedhelminthburdenincreasesallergenskinsensitizationbutnotclinicalallergyarandomizeddoubleblindplacebocontrolledtrialinvietnam
AT tuyenl reducedhelminthburdenincreasesallergenskinsensitizationbutnotclinicalallergyarandomizeddoubleblindplacebocontrolledtrialinvietnam
AT quinnellr reducedhelminthburdenincreasesallergenskinsensitizationbutnotclinicalallergyarandomizeddoubleblindplacebocontrolledtrialinvietnam
AT lewiss reducedhelminthburdenincreasesallergenskinsensitizationbutnotclinicalallergyarandomizeddoubleblindplacebocontrolledtrialinvietnam
AT minht reducedhelminthburdenincreasesallergenskinsensitizationbutnotclinicalallergyarandomizeddoubleblindplacebocontrolledtrialinvietnam
AT campbellj reducedhelminthburdenincreasesallergenskinsensitizationbutnotclinicalallergyarandomizeddoubleblindplacebocontrolledtrialinvietnam
AT simmonsc reducedhelminthburdenincreasesallergenskinsensitizationbutnotclinicalallergyarandomizeddoubleblindplacebocontrolledtrialinvietnam
AT telfordg reducedhelminthburdenincreasesallergenskinsensitizationbutnotclinicalallergyarandomizeddoubleblindplacebocontrolledtrialinvietnam
AT browna reducedhelminthburdenincreasesallergenskinsensitizationbutnotclinicalallergyarandomizeddoubleblindplacebocontrolledtrialinvietnam
AT hient reducedhelminthburdenincreasesallergenskinsensitizationbutnotclinicalallergyarandomizeddoubleblindplacebocontrolledtrialinvietnam
AT farrarj reducedhelminthburdenincreasesallergenskinsensitizationbutnotclinicalallergyarandomizeddoubleblindplacebocontrolledtrialinvietnam
AT williamsh reducedhelminthburdenincreasesallergenskinsensitizationbutnotclinicalallergyarandomizeddoubleblindplacebocontrolledtrialinvietnam
AT pritchardd reducedhelminthburdenincreasesallergenskinsensitizationbutnotclinicalallergyarandomizeddoubleblindplacebocontrolledtrialinvietnam
AT brittonj reducedhelminthburdenincreasesallergenskinsensitizationbutnotclinicalallergyarandomizeddoubleblindplacebocontrolledtrialinvietnam