The DOI matches its Crossref record.
Reduced helminth burden increases allergen skin sensitization but not clinical allergy: a randomized, double-blind, placebo-controlled trial in Vietnam
Abstract
Summary: Background: 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. Objective: We tested this hypothesis in a rural area of central Vietnam where hookworm infection is endemic. Methods: 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. Results: 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. Conclusion: 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. Cite this as: C. Flohr, L. N. Tuyen, R. J. Quinnell, S. Lewis, T. T. Minh, J. Campbell, C. Simmons, G. Telford, A. Brown, T. T. Hien, J. Farrar, H. Williams, D. I. Pritchard and J. Britton, Clinical & Experimental Allergy, 2010 (40) 131–152.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“2 showed an increase in either the incidence 22 or frequency 23 of a positive SPT response after at least 1 year of treatment.”
From Global issues in allergy and immunology: Parasitic infections and allergy (2017) · cites this paper as [23]
Citations
Cites
No references could be resolved yet.
Research works printed but not linked: 51
- 10.1016/S0140-6736(97)07302-9 · DOI
- 10.1034/j.1399-3038.2003.00043.x · DOI
- Addo Yobo EOD, 1997, Exercise‐induced bronchospasm in Ghana, differences in prevalence between urban and rural schoolchildren, 52, 161
- 10.1111/j.1365-2222.2004.1946.x · DOI
- 10.1067/mai.2003.1348 · DOI
- Scrivener S, 2001, Independent effects of intestinal parasite infection and domestic allergen exposure on risk of wheeze in Ethiopia, a nested case–control study, 358, 1493
- 10.1164/rccm.200210-1204OC · DOI
- 10.1111/j.1365-2222.2005.02181.x · DOI
- 10.1046/j.1365-2745.2002.01424.x · DOI
- 10.1111/j.1365-2222.2006.02479.x · DOI
- 10.1111/j.1398-9995.2005.00801.x · DOI
- 10.1164/rccm.200603-331OC · DOI · Paper page
- 10.1016/S1471-4922(01)01941-9 · DOI
- 10.1016/0035-9203(91)90038-Z · DOI
- 10.1016/0091-6749(93)90119-Z · DOI
- 10.1086/381767 · DOI · Paper page
- 10.1164/ajrccm.156.1.9606081 · DOI
- Cooper PJ, 2006, Effect of albendazole treatment on the prevalence of atopy in children living in communities endemic for geohelminth parasites, a cluster-randomised trial, 367, 1598
- Flohr C, 2006, Poor sanitation and helminth infection protect against skin sensitisation in Vietnamese children, a cross-sectional study, 118, 1305
- 10.1016/S0022-3476(80)80039-4 · DOI
- 10.1016/S0140-6736(01)06521-7 · DOI
- 10.1111/j.1365-3024.1993.tb00600.x · DOI
- Faulkner H, 2002, Age‐ and infection intensity‐dependent cytokine and antibody production in human trichuriasis, the importance of IgE, 185, 665
- 10.1111/j.1365-3024.1991.tb00274.x · DOI
- Flohr C, 2007, Low efficacy of mebendazole against hookworm in Vietnam, two randomised controlled trials, 76, 732
- Burr ML, 1989, Changes in asthma prevalence, two surveys 15 years apart, 64, 1118
- Elliott AM, 2005, Helminth infection during pregnancy and development of infantile eczema, JAMA, 294, 2032
- 10.1111/j.1365-3024.1993.tb00615.x · DOI
- 10.1111/j.1365-2222.2004.01958.x · DOI
- 10.1164/rccm.200211-1320OC · DOI
- 10.1046/j.1365-2222.2001.00987.x · DOI
- Van Den Biggelaar AH, 2000, Decreased atopy in children infected with Schistosoma haematobium, a role for parasite-induced interleukin-10, 356, 1723
- 10.1159/000024433 · DOI
- Lynch NR, 1984, Incidence of atopic disease in a tropical environment, partial independence from intestinal helminthiasis, 73, 229
- 10.1111/j.1365-2222.1987.tb02004.x · DOI
- 10.1126/science.296.5567.490 · DOI
- 10.1046/j.1365-2249.2002.01908.x · DOI
- Montresor A, 2002, Helminth control in school‐age children: a guide for managers of control programmes
- 10.1111/j.1365-2222.2008.03134.x · DOI · Paper page
- 10.1086/425017 · DOI
- Pit D, 2000, Prenatal immune priming with helminth infections, parasite-specific cellular reactivity and Th1 and Th2 cytokine responses in neonates, 55, 732
- 10.1111/j.1365-2249.2004.02449.x · DOI
- King CL, 1996, Cytokine control of parasite‐specific anergy in human urinary schistosomiasis. IL‐10 modulates lymphocyte reactivity, J Immunol, 156, 4715, 10.4049/jimmunol.156.12.4715 · DOI
- 10.1016/j.jaci.2005.08.047 · DOI
- Maizels RM, 2003, Immune regulation by helminth parasites, cellular and molecular mechanisms, 3, 733
- 10.1046/j.1365-2222.2001.01069.x · DOI
- 10.4049/jimmunol.172.5.3181 · DOI
- 10.1086/586904 · DOI
- 10.1086/591945 · DOI
- 10.1016/0035-9203(91)90239-U · DOI
- 10.1016/j.jaci.2006.04.001 · DOI
Cited by
Sorted by citations
New insights into the epidemiology of childhood atopic dermatitis
Flohr, C., & Mann, J. (2014) · Allergy · doi:10.1111/all.12270 · Cited by 499
Self-citationExperimental hookworm infection: a randomized placebo-controlled trial in asthma
Feary, J. R., Venn, A. J., Mortimer, K., Brown, A. P., Hooi, D., Falcone, F. H., Pritchard, D. I., & Britton, J. R. (2010) · Clinical & Experimental Allergy · doi:10.1111/j.1365-2222.2009.03433.x · Cited by 188
Self-citationThe exposome in atopic dermatitis
Stefanovic, N., Flohr, C., & Irvine, A. D. (2020) · Allergy · doi:10.1111/all.13946 · Cited by 181
Self-citationHygiene and other early childhood influences on the subsequent function of the immune system
Rook, G. A. W., Lowry, C. A., & Raison, C. L. (2015) · Brain Research · doi:10.1016/j.brainres.2014.04.004 · Cited by 109
Global issues in allergy and immunology: Parasitic infections and allergy
Cruz, A. A., Cooper, P. J., Figueiredo, C. A., Alcantara-Neves, N. M., Rodrigues, L. C., & Barreto, M. L. (2017) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2017.09.005 · Cited by 82
Metadata
- Authors
- Flohr, C., Tuyen, L. N., Quinnell, R. J., Lewis, S., Minh, T. T., Campbell, J., Simmons, C., Telford, G., Brown, A., Hien, T. T., Farrar, J., Williams, H., Pritchard, D. I., & Britton, J.
- Venue
- Clinical & Experimental Allergy
- Publisher
- Wiley
- Published
- 2009-12-15
- Volume
- 40
- Issue
- 1
- Pages
- 131-142
- ISSN
- 0954-7894
- 1365-2222
- Cited by
- 93
- References
- 0
- Language
- en
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
How to cite
Cite CoChat for the checks on this page, and the paper for its own findings.
- This page
- CoChat. (2026). Citation check: Reduced helminth burden increases allergen skin sensitization but not clinical allergy: a randomized, double-blind, placebo-controlled trial in Vietnam. https://app.cochat.ai/papers/10.1111/j.1365-2222.2009.03346.x
- The paper
- Flohr, C., Tuyen, L. N., Quinnell, R. J., Lewis, S., Minh, T. T., Campbell, J., Simmons, C., Telford, G., Brown, A., Hien, T. T., Farrar, J., Williams, H., Pritchard, D. I., & Britton, J. (2010). Reduced helminth burden increases allergen skin sensitization but not clinical allergy: a randomized, double-blind, placebo-controlled trial in Vietnam. Clinical & Experimental Allergy. https://doi.org/10.1111/j.1365-2222.2009.03346.x