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Original Articles International Patterns of Tuberculosis and the Prevalence of Symptoms of Asthma, Rhinitis, and Eczema

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Original Articles International Patterns of Tuberculosis and the Prevalence of Symptoms of Asthma, Rhinitis, and Eczema Thorax 2000;55:449–453 449 Original articles Thorax: first published as 10.1136/thorax.55.6.449 on 1 June 2000. Downloaded from International patterns of tuberculosis and the prevalence of symptoms of asthma, rhinitis, and eczema Erika von Mutius, Neil Pearce, Richard Beasley, Soo Cheng, Ondine von Ehrenstein, Bengt Björkstén, Stephan Weiland, on behalf of the ISAAC Steering Committee Abstract national patterns of the prevalence of these Background—An ecological analysis was diseases2 are largely unknown. In particular, conducted of the relationship between they cannot be explained by the established tuberculosis notification rates and the putative risk factors such as allergen exposure prevalence of symptoms of asthma, aller- and air pollution which do not appear to be gic rhinoconjunctivitis, and atopic eczema strongly related to the underlying population in 85 centres from 23 countries in which prevalence.2–5 This has led to consideration of standardised data are available. These factors that may programme the initial suscep- essentially comprised countries in Europe tibility to asthma and/or atopy which have as well as the USA, Canada, Australia, and changed in temporal association with the New Zealand. increasing trends in prevalence worldwide, are Methods—Tuberculosis notification rates consistent with international prevalence pat- were obtained from the World Health terns, and for which biological plausibility exists Organization. Data on the prevalence of with respect to an underlying mechanism. symptoms of asthma, rhinitis, and eczema One such hypothesis is that the lack of expo- in 235 477 children aged 13–14 years were sure in early childhood to infections such as University Children’s based on the responses to the written and tuberculosis, measles, and diphtheria may Hospital, Klinikum video questionnaires from the Inter- increase the risk of developing atopic disorders http://thorax.bmj.com/ Innenstadt, Munich, national Study of Asthma and Allergies in 67 Germany such as asthma. Interest has focused particu- E von Mutius Childhood (ISAAC). The analysis was larly on the role of Mycobacterium tuberculosis O von Ehrenstein adjusted for gross national product (GNP) which is known to induce Th1 type immune as an estimate of the level of aZuence. responses, suppressing the development of Wellington School of Results—Tuberculosis notification rates Th2 type immune responses that are character- Medicine, University were significantly inversely associated istic of atopic disorders.8–10 Epidemiological of Otago, Wellington, with the lifetime prevalence of wheeze and New Zealand evidence for the association of this immuno- N Pearce asthma and the 12 month period preva- logical response with a reduced risk of R Beasley lence of wheeze at rest as assessed by the developing asthma comes from the study by on October 1, 2021 by guest. Protected copyright. S Cheng video questionnaire. An increase in the Shirakawa et al11 who reported that, among tuberculosis notification rates of 25 per Japanese schoolchildren aged 12–13 years, University Hospital, 100 000 was associated with an absolute asthmatic symptoms were one half to one third Linköping, Sweden decrease in the prevalence of wheeze ever B Björkstén as likely in positive tuberculin responders as in of 4.7%. Symptoms of allergic rhinocon- negative responders, and that remission of Institute of junctivitis in the past 12 months were atopic symptoms between the ages of seven and Epidemiology and inversely associated with tuberculosis no- 12 years was 6–9 times more likely in positive Social Medicine, tification rates, but there were no other tuberculin responders. The positive tuberculin University of Münster, significant associations with other ISAAC responders had significantly lower levels of the Germany questions on allergic rhinoconjunctivitis S Weiland Th2 cytokines interleukin (IL)-4, IL-10, and or atopic eczema. IL-13 and higher levels of the Th1 cytokine Correspondence to: Conclusions—These findings are consist- interferon (IFN)-ã. The interpretation of these Dr E von Mutius, Dr von ent with recent experimental evidence findings has been debated intensively. The Haunersche Kinderklinik, which suggests that exposure to Mycobac- Klinikum Innenstadt, inverse association between allergic status and Lindwurmstrasse 4, D-80337 terium tuberculosis may reduce the risk tuberculin reactivity may simply reflect the München, Germany of developing asthma. imbalance of Th1/Th2 responsiveness charac- email: erika.von.mutius@ (Thorax 2000;55:449–453) kk-i.med.uni-muenchen.de teristic of atopic individuals who have been shown to express smaller delayed type hyper- Received 20 May 1999 Keywords: tuberculosis; atopy; asthma Returned to authors sensitivity skin reactions to recall antigens than 8 July 1999 non-atopic subjects.12 This imbalance may Revised manuscript received The reasons for the increase in the prevalence relate to genetic or other constitutional factors 25 August 1999 Accepted for publication of asthma and other atopic disorders such as rather than to exposure to mycobacteria. How- 7 September 1999 eczema and allergic rhinitis1 and the inter- ever, the alternative hypothesis which suggests 450 von Mutius, Pearce, Beasley, et al that exposure to M tuberculosis reduces the risk tions used were those on wheeze ever and of developing asthma and/or atopy is equally wheeze in the last 12 months, and on asthma conceivable. The reduction in the incidence of ever from the written questionnaire.213 The Thorax: first published as 10.1136/thorax.55.6.449 on 1 June 2000. Downloaded from tuberculosis in many countries during the video asthma question used was the sequence 1900s may have contributed to the concurrent on wheeze at rest in the last 12 months. These increase in the prevalence of asthma and other questions were chosen because they have been atopic diseases. shown to have the greatest validity19 and To investigate these hypotheses further we because the video question on wheeze at rest have conducted an ecological analysis of the was used in both versions of the asthma video. relationship between tuberculosis notification The questions on rhinitis used were those on rates and the prevalence of symptoms of symptoms of rhinitis ever, rhinitis in the last 12 asthma, allergic rhinitis, and atopic eczema in months, and rhinoconjunctivitis in the last 12 countries in which standardised data are avail- months.14 The questions on atopic eczema able. used were those on eczema ever, and on symp- toms of an itchy rash ever and in the last 12 15 Methods months. The analysis was based on the data for 13–14 For each of these questions the data were year olds from the International Study of analysed by multiple linear regression with one Asthma and Allergies in Childhood data point for each centre, weighted by the (ISAAC).2 13–15 ISAAC involved 463 801 chil- inverse variance of the prevalence estimate for dren in this age group in 155 collaborating the centre, and adjusted for the gross national product (GNP) of the country in which the centres in 56 countries, of which 304 796 were 20 in the 99 centres in 42 countries which used the centre was based. The level of aZuence of a optional asthma video questionnaire. The country was considered to be a potential analyses in this paper were, however, confined confounder since increasing industrialisation to those countries in which the tuberculosis and aZuence involve changes in lifestyle and notification rates were considered to be of suf- environmental exposures which could be re- 16 lated to asthma risk, as well as to the decreased ficient validity —namely, countries in western, 21 northern, central and eastern Europe as well as risk of tuberculosis infections. Inclusion of the USA, Canada, Australia and New Zealand GNP in the model only led to a minor increase (a full list is given at the end of the paper). in the standard errors for the tuberculosis coef- These involved 235 477 children in 85 centres ficients, indicating that multicollinearity was in 23 countries, of which 143 551 were in 52 not a significant problem. centres in 17 countries which used the optional video questionnaire. The first centre survey Results took place in 1991, but most of the data were Table 1 shows the findings for the 85 centres collected during the period 1994–5. from 23 countries considered to have valid http://thorax.bmj.com/ For each country the annual tuberculosis tuberculosis notification data and comparable notification rates per 100 000 during 1980–2 prevalence data for symptoms of asthma, aller- were obtained from the World Health gic rhinoconjunctivitis, and atopic eczema. Organization17 and were averaged over these Tuberculosis rates were significantly inversely three years. This time period was chosen associated with the prevalence of all four because it corresponded to the period during asthma questions considered in the univariate which participants in the ISAAC study were analyses (table 1, fig 1). All of these inverse infants. associations were reduced when the analysis The analyses involved the key questions of was adjusted for GNP, but three of the four on October 1, 2021 by guest. Protected copyright. symptoms of asthma, allergic rhinoconjunctivi- asthma questions (wheeze ever, asthma ever, tis, and atopic eczema from the ISAAC written and the video question) still showed significant and video questionnaires.18 The asthma ques- inverse associations. These analyses showed, Table 1 Regression analysis of the prevalence of symptoms of asthma, rhinitis and eczema
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