Absence of Relationships Between Tuberculin Responses and Development of Adult Asthma Observations

This study demonstrates that the magnitude of tuberculin response was similar among asthma-rhinitis and healthy, atopic and nonatopic Chinese adults in the Guangdong area. There was no association between tuberculin response, presence of BCG scars, and asthma and rhinitis as well as atopy. These results were consistent in both the univariate and multivariate analyses.

We employed allergen SPT, serum-total, and serum-specific IgE levels as markers to indicate atopic status of our study subjects. These markers are widely used and well recognized and have been applied widely in many epidemiologic studies. A significant relationship between serum-total IgE and specific IgE as atopic markers in a randomly drawn population from Norway indicates that serum IgE measurements are highly related to atopy in Western environments. One recent study also showed that serum-total IgE and serum-specific IgE correlated significantly with allergen SPT in Indian asthmatics with food allergy. We therefore believe that serum-total and serum-specific IgE, like allergen skin testing, are useful markers of atopy in our study.

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Asthma and rhinitis patients were enrolled from our outpatient clinic, and age-matched healthy control subjects were selected from the subjects who came to our hospital for a routine health check-up. According to the report of Guangdong Centre of Disease Control and Prevention, the prevalence of tuberculous disease in Guangdong area has been approximately 42 per 100,000 population, which is much higher than in Western countries. The policy of BCG vaccination of all newborn children at 24 h or no later than 1 year after birth in China has long been established. The study subjects were born between 1960 and 1987, when > 95% of population had received BCG vaccination. During their 20 to 45 years of life, it is likely for them to be exposed to viral and bacterial infections including Mycobacterium tuberculosis. Therefore, it allowed us to investigate whether tuberculin responses, early BCG vaccination, and history of tuberculosis infection have an impact on the development of asthma and rhinitis, as well as atopic status in this group of adults. From history review and chest radiography, we could not find differences in the percentage of BCG vaccination (99.1% vs 98.6%), past tuberculosis infection (1.4% vs 1.9%), and pulmonary fibrous and calcified tuberculosis focus (2.3% vs 1.9%) between healthy and asthma-rhinitis subjects, which suggests that early BCG vaccination and tuberculosis infection do not influence the occurrence of allergic symptoms and diseases.

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The Th2 hypothesis for asthma states that atopy is caused by a relative increase in Th2 response in combination with a decrease in Th1 response. Shirakawa et al observed an inverse association in Japanese children between tuberculin responses and atopic disorders. They showed that a strongly positive PPD response was associated with a lower incidence of allergic disease, lower levels of serum IgE, and higher levels of Th1 cytokines. However, other epidemiologic studies from areas with a low prevalence and high incidence of tuberculosis showed no differences between allergic and healthy children with respect to PPD induration and PPD positivity rates, which suggests that the Th1 response is not completely suppressed in atopic subjects. However, one study in Turkey showed that PPD induration in atopic asthmatic children was statistically significantly greater than in healthy children, indicating that when the relationship between tuberculin response and atopy is studied in tuberculosis-prevalent countries, it should be taken into consideration that the PPD response can be stronger and overemphasized as an active infection in atopic asthmatic subjects.

The PPD response is variable and depends not only on BCG vaccination in early life, but also on tuberculosis infection later in life, or sensitization to environmental mycobacteria. The PPD response is mediated by primary Th1 response, which is expected to be suppressed in atopic asthmatics and rhinitis Chest Radiographypatients. However, we did not find any evidence that it induces less or weaker tuberculin responses or lower proportion of previous tuberculosis exposure and infection in our atopic subjects. Several factors could have accounted for this. A high prevalence of tuberculosis infection and ubiquitous exposure to mycobacteria in our environment could have diluted its effect on atopy, and one would expect to demonstrate its impact in settings with lower levels of exposure. It is also likely that the time and route of BCG vaccination or duration of exposure to mycobacteria might be critical in influencing the development of atopy. It is speculated that the memory of cellular immunity induced by BCG vaccination in infancy in our study subjects was attenuated 20 to 45 years later, and did not provide enough protection for them from atopic diseases. Evidence obtained from animal models shows that vaccines administered via the mucosa are able to elicit neutralizing serum antibodies and cell-mediated immune responses as well as mucosal secretory IgA antibodies. Thus, it is possible that vaccines delivered by mucosal surfaces would stimulate vigorous cell-mediated immune responses similarly in humans and efficaciously protect against tuberculosis infection as well as atopic diseases. However, currently available BCG vaccination administered intradermally in humans has not shown any protective effect against atopic diseases. However, some studies showed that a progressive increase in type 1 diabetes, a Thl-related disease, in the face of increasing prevalence of atopy in developed countries suggests that the pathogenesis of atopy could be more complicated than only a shift in Th1/Th2 balance. It has also been reported that there is an increased frequency of interferon-7-producing CD4 and CD8 T-cells in asthmatics compared with normal subjects. In contrast to the Th2 hypothesis, these results suggest that Th1 responses may have a role in atopy pathogenesis.

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In conclusion, we did not observe significant relationships between history of tuberculosis infection, tuberculin responses, and development of adult bronchial asthma, allergic rhinitis and atopy. Our study suggests that the protection provided by BCG vaccination intradermally in infancy from atopic diseases may be limited in early childhood, when a substantial memory of cellular immune modulation still exits.

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