Elsevier

The Lancet

Volume 358, Issue 9292, 3 November 2001, Pages 1493-1499
The Lancet

Articles
Independent effects of intestinal parasite infection and domestic allergen exposure on risk of wheeze in Ethiopia: a nested case-control study

https://doi.org/10.1016/S0140-6736(01)06579-5Get rights and content

Summary

Background

Why asthma is rare in rural subsistence societies is not clear. We tested the hypotheses that the risk of asthma is reduced by intestinal parasites or hepatitis A infection, and increased by exposure to dust-mite allergen or organophosphorus insecticides in urban and rural areas of Jimma, Ethiopia.

Methods

From 12 876 individuals who took part in a study of asthma and atopy in urban and rural Jimma in 1996, we identified all who reported wheeze in the previous 12 months, and a random subsample of controls. In 1999, we assessed parasites in faecal samples, Der p 1 levels in bedding, hepatitis A antibodies, serum cholinesterase (a marker of organophosphorus exposure), total and specific serum IgE, and skin sensitisation to Dermatophagoides pteronyssinus in 205 cases and 399 controls aged over 16 years. The effects of parasitosis, Der p 1 level, hepatitis A seropositivity, and cholinesterase concentration on risk of wheeze, and the role of IgE and skin sensitisation in these associations, were analysed by multiple logistic regression.

Findings

The risk of wheeze was independently reduced by hookworm infection by an odds ratio of 0·48 (95% Cl 0·24–0·93, p=0·03), increased in relation to Der p 1 level (odds ratio per quartile 1·26 [1·00–1·59], p=0·05), and was unrelated to hepatitis A seropositivity or cholinesterase concentration. In the urban population, D pteronyssinus skin sensitisation was more strongly related to wheeze (9·45 [5·03–17·75]) than in the rural areas (1·95 [0·58–6·61], p for interaction=0·017), where D pteronyssinus sensitisation was common, but unrelated to wheeze in the presence of high-intensity parasite infection.

Interpretation

High degrees of parasite infection might prevent asthma symptoms in atopic individuals.

Introduction

Asthma is rare in rural subsistence societies but becomes much more prevalent as populations become urbanised and affluent.1, 2, 3, 4, 5, 6 Although the explanation for this fact is not known, one feature that could be important is the lower prevalence of infection with intestinal parasites in more affluent populations, since parasite infection has been postulated to prevent IgE-mediated allergic disease by blocking effector-cell IgE receptors with parasite-induced specific and polyclonal IgE,7, 8 or by production of the anti-inflammatory cytokine interleukin 10.9 Other potential explanations include increased exposure to housedust-mite allergen arising from the adoption of housing and bedding styles that favour dust-mite replication,10, 11 or the effect of the more hygienic affluent lifestyle in reducing childhood infections with agents such as hepatitis A virus,12 resulting in the programming of T helper cells in early life to produce a more allergic phenotype.13 Exposure to organophosphorus insecticides has also been implicated in asthma aetiology, possibly by increasing muscarinic effects in the airway.14

From a previous study in Jimma, Ethiopia, we reported that the prevalence of self-reported wheeze in the previous 12 months was much lower in rural subsistence areas (1·2%) than in the urban population (3·7%).4 We also noted that allergen skin sensitisation to Dermatophagoides pteronyssinus, a strong determinant of wheeze in the urban area, was generally more common and was unrelated to wheeze in the rural population. Various urban lifestyle factors were associated with an increased risk of wheeze or allergen skin sensitisation, including the use of synthetic mattresses and malathion insecticide.4 We now report a nested case-control study in the same study population with objective measures to test hypotheses relating to the roles of parasite infection and exposure to dust-mite allergen, hepatitis A virus, and organophosphorus insecticides in determining the risk of wheeze and allergen skin sensitisation in individuals aged 16 or over in urban and rural areas of Jimma.

Section snippets

Study population

In 1996, we obtained cross-sectional data for respiratory symptoms and lifestyle factors in 9844 people in urban households and 3032 in rural households in Jimma.4 Cases for this study were the 311 individuals who at the time of the 1996 survey were aged 14 or over and reported wheezing in their chest in the previous 12 months. Controls were all those who had not already been identified as cases in a random subsample of 570 people aged 14 or over from the full 1996 study population. This

Results

205 cases and 399 controls, 71% of those selected, took part in the study. 7% (60 of 855) of those selected had died, were too ill, or refused to take part, 9% (79 of 855) had moved from the area, and 13% (112 of 855) could not be contacted. Cases were predominantly from the urban area, were older than controls, and the proportion who were male was higher. Urban participants generally had higher educational attainment than those in rural areas. Less than 6% of the population were current

Discussion

Our results suggest that the increased occurrence of wheeze associated with urbanisation in this population is due partly to a loss of a protective effect from hookworm infection, partly to the effect of increased dust-mite allergen exposure, and partly to unidentified factors. Infection with ascaris was also associated with a reduced risk of wheeze, but this effect was not independently significant. The effect of Der p 1 exposure seems to be mediated through the production of specific IgE, but

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