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(Chest. 2005;127:1928-1934.)
© 2005 American College of Chest Physicians

The Incidence of Asthma in Young Adults*

Simon F. Thomsen, MD; Charlotte S. Ulrik, MD, DMSci; Kirsten O. Kyvik, MD, PhD; Klaus Larsen, MSc, PhD; Lars R. Skadhauge, MD, PhD; Ida Steffensen, MD, PhD and Vibeke Backer, MD, DMSci

* From the Department of Internal Medicine (Drs. Thomsen and Backer), Bispebjerg Hospital, Copenhagen, Denmark; the Department of Respiratory Medicine (Dr. Ulrik), and the Clinical Research Unit (Dr. Larsen), Hvidovre Hospital, Hvidovre, Denmark; The Danish Twin Registry (Dr. Kyvik), University of Southern Denmark, Odense, Denmark; the Department of Occupational and Environmental Medicine (Dr. Skadhauge), Odense University Hospital, Odense, Denmark; and the Department of Respiratory Medicine (Dr. Steffensen), Holbæk Hospital, Holbæk Denmark.

Correspondence to: Simon F. Thomsen, MD, Department of Internal Medicine I, Bispebjerg Hospital, DK-2400 Copenhagen NV, Denmark; e-mail: sft{at}city.dk


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objectives: Longitudinal data on adult asthma are sparse. The objectives of this study were to determine the incidence of asthma and to establish the risk factors for the development of asthma in subjects who were 12 to 41 years old over an 8-year period.

Design: From birth cohorts over the period 1953 to 1982 in The Danish Twin Registry, 19,349 subjects with no history of asthma, as determined by a questionnaire-based survey in 1994, answered a follow-up questionnaire in 2002. The subjects were regarded as incident asthma cases when answering "yes" to the question "Do you have, or have you ever had asthma?" in 2002, and "no" to the same question in 1994.

Results: A total of 838 cases (4.3%) of new asthma were identified in 2002. The incidence rates of asthma were 4.5 and 6.4 per 1,000 person-years, respectively, among male and female subjects. For all ages, the probability of adult-onset asthma was greater for female subjects (odds ratio [OR], 1.49; p < 0.001), and for both sexes there was a slow decline in probability with increasing age. There was a positive association between increasing body mass index (BMI) and risk of adult-onset asthma applying to both sexes (OR, 1.05 per unit; p < 0.001). Furthermore, positive associations were found between incident asthma and a history of hay fever (OR: male subjects, 4.2; female subjects, 3.7; p < 0.001), eczema (OR: male subjects, 3.5; female subjects, 2.0; p < 0.001), and both (OR: male subjects, 6.9; female subjects, 8.0; p < 0.001).

Conclusions: There is a continuing high incidence of asthma past childhood that is most pronounced among female subjects. Increasing levels of BMI are associated with a greater likelihood of developing asthma for both sexes. A substantial portion of cases of adult asthma is preceded by upper airway allergic symptoms and/or eczema, thus indicating a shared pathogenesis.

Key Words: asthma • body mass index • hay fever • incidence • sex


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
The prevalence of asthma and allergic disease has increased substantially during recent decades, and to a large extent the causes for this increase are still imperfectly understood. It is well recognized that the incidence of asthma is greater in childhood compared to adulthood, and that the male subject/female subject ratio of incident asthma diminishes with increasing age.1 However, an interest in adult-onset asthma has emerged, not in the least due to reports coming from several large-scale longitudinal studies from Europe (European Community Respiratory Health Survey2) and the and United States (National Health and Nutrition Examination Study3), pointing out the growing impact of adult respiratory allergic disease morbidity. No single hypothesis can explain this widened distribution of disease, but a biologically plausible model is likely to include environmental risk factors associated with a westernized lifestyle interacting with individual susceptibility genotypes. In a search for factors fitting such a model, several environmental determinants have been shown be part of the cause of adult-onset wheezing illness, including female sex,1 upper airway allergic disease,14 sensitization to aeroallergens,45 obesity,6 exposures encountered at work,7 and perhaps hormone replacement therapy.8 Still, longitudinal data on incident asthma among adults are sparse,39 and the study of these data may therefore provide new insight into the development and natural history of the disease.

By means of a prospective questionnaire study, the objective of this survey was to determine the incidence of asthma and to examine the age-dependent and sex-dependent risk for adolescent-onset and adult-onset asthma from 1994 through 2002. Furthermore, we wanted to provide risk estimates for incident asthma during the intervening 8-year period given information on hay fever, eczema, body mass index (BMI), smoking, and leisure time physical activity.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Study Design
The study population is based on the birth cohorts from 1953 to 1982 that were ascertained from The Danish Twin Registry.10 In 1994, a mailed questionnaire was answered by 29,180 twin individuals (86%),11 and for an 8-year follow-up analysis in 2002, 21,162 of those twin individuals (73%) participated. We observed similar response rates in the different age and sex groups across surveys. Of those participating in both surveys (21,162 subjects), a total of 19,349 subjects with no reported history of asthma in 1994 were identified, and analyses of incident asthma were based on this sample.

A questionnaire with items aimed at identifying multiple phenotypes, including identical questions on asthma, was used to assess subjects on both occasions. Affected cases were identified on the basis of responses to the question "Do you have, or have you ever had asthma?" Individuals answering "yes" to that question were classified as having or having had asthma. This procedure has previously been shown12 to be reliable with respect to identifying subjects with asthma in population-based studies that use questionnaire responses as the sole diagnostic criterion. Similar questions were applied to detect subjects with hay fever and eczema.

Subjects were stratified into the following four separate categories on the basis of answers to questions on smoking history: (1) current daily smokers (subjects who smoked more than one cigarette, one cigar, one cheroot, and/or 1 g of pipe tobacco per day); (2) occasional smokers (subjects who smoked less than one cigarette, one cigar, one cheroot, or 1 g of pipe tobacco per day on average); (3) former smokers (subjects who have stopped smoking any time prior to the date of assessment); and (4) never smokers (subjects who have never smoked).

Subjects were divided into the following three categories owing to the quantity of weekly leisure time physical activity: (1) light physical activity (subjects who spend < 2 h per week on light exercise activities); (2) moderate physical activity (subjects who spend between 2 h per week on light exercise activities and 4 h per week on heavy exercise activities); and (3) heavy physical activity (subjects who spend > 4 h per week on heavy exercise activities).

Statistical Analysis
The data were analyzed with a statistical software package (R: A Language for Data Analysis and Graphics; R. Gentleman, GNU Project, Free Software Foundation; Boston, MA).13 Overdispersion could be expected to a certain extent due to intrapair correlation of asthma.14 The overdispersion parameter was estimated to be equal to 1.068, which means that the intrapair correlation of asthma in this cohort is very small. Furthermore, the studied cohort comprised 35% single twins, which also provides us with ample authority to consider the entire sample of twins as if it was composed of single uncorrelated individuals (ie, the confidence intervals [CIs] reported fall 2 to 3% narrow of that ideal situation).

Since we did not know the exact time of the onset of asthma in each subject, we calculated the incidence rates of asthma under the assumption that each incident case of asthma on average acquired asthma in the middle of the study period (ie, after 4 years). This approach gave us a total of 151,440 person-years under observation.

The probability of acquiring asthma depends on age and BMI in a fashion that is still poorly understood. We analyzed the age-dependent and BMI-dependent risk of new asthma by means of a generalized additive model,15 which allowed us to handle age and BMI as continuous variables when the analyses were performed separately for subjects 12 to 19 and 20 to 41 years of age.

Logistic regression modeling was applied to investigate associations among risk factors for having asthma. Separate analyses were performed for the age groups 12 to 19 years and 20 to 41 years, with incident asthma from 1994 through 2002 as response, and with sex, age, smoking, and leisure time physical activity as explanatory variables. BMI was also included in the older age group. BMI was calculated as weight in kilograms divided by the square of height in meters.

The analyses of incident asthma in relation to eczema and hay fever were done by means of two-way tables stratified on sex, for the entire cohort. Results are reported as odds ratios (ORs). A p value of < 0.05 was considered to be statistically significant. The protocol was evaluated and approved by the local ethics committee.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
The subjects with no history of asthma in 1994 comprised 8,701 male subjects (45.0%) and 10,648 female subjects (55.0%). In this sample, a total of 838 cases (4.3%) of new asthma were identified in 2002 (male subjects, 307 [3.5%]; female subjects, 531 [5.0%]), corresponding to an overall incidence rate of 5.5 cases per 1,000 person-years with incidence rates for male subjects and female subjects being 4.5 and 6.4 per 1,000 person-years, respectively. The crude prevalence rates for asthma were 6.1% (1,777 cases) in 1994 and 9.2% (1,938 cases) in 2002.

The relationship between age and the probability of acquiring asthma for male subjects and female subjects is shown in Figure 1 . For all ages, the likelihood of new asthma is greater for female subjects than for male subjects, with a remarkably higher probability for the development of asthma among young adult female subjects.



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  		Figure 1. The probability of incident asthma from 1994 to 2002 by age, for male subjects and female subjects who were 12 to 41 years of age. The full lines are the smoothed-out probabilities, the fragmented lines are the raw prevalence numbers, and the dotted lines are ± SD.

 
In Figure 2 , the probability of incident asthma vs BMI is shown for male subjects and female subjects. The probability for women is higher for all levels of BMI until 31, above which male subjects are at a greater risk of acquiring asthma.



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  		Figure 2. The probability of incident asthma from 1994 to 2002 by BMI, for male subjects and female subjects who were 20 to 41 years of age. The full lines are the smoothed-out probabilities, the fragmented lines are the raw prevalence numbers, and the dotted lines are ± SD.

 
The results of the logistic regression analyses are shown in Table 1 for the group of subjects 20 to 41 years of age, and in Table 2 for the group of subjects 12 to 19 years of age. We found a statistically significant effect of sex and BMI on the risk of adult-onset asthma, and no such effect for age, smoking, and leisure time physical activity. There were no statistically significant interactions among the variables considered. We found, though, a statistically significant interaction between sex and age on adolescent-onset asthma. This means that the more pronounced positive association found between female sex and the risk of new asthma, compared to that for male sex, in this younger age group is dependent on age.


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  		Table 1. Associations Between Variables and Risk of Development of Asthma From 1994 to 2002, Among Danish Twins 20 to 41 Years of Age*

 

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  		Table 2. Associations Between Sex/Age and Risk of Development of Asthma From 1994 to 2002 Among Danish Twins 12 to 19 Years of Age*

 
The association between hay fever and eczema, and the occurrence of new asthma is considered in Table 3 . Having a history of hay fever and no history of eczema compared to having had no symptoms in 1994 increased the risk for the development of asthma by a factor of 4.2 among male subjects and of 3.7 among female subjects. A slightly smaller but considerable increase in the risk for new asthma was observed among subjects reporting that they had ever had eczema but no history of hay fever. Having, or having had, both hay fever and eczema compared to having had no symptoms increased the likelihood for the later development of asthma by 6.9-fold among male subjects, and by eightfold among female subjects.


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  		Table 3. Associations Between Hay Fever Ever, Eczema Ever, and Eczema Plus Hay Fever Ever in 1994, and the Risk of Development of Asthma From 1994 to 2002 Among Danish Twins 12 to 41 Years of Age (n = 19,067)*

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
The main finding of this study was a remarkably high incidence of asthma among young adults. Additionally, we found substantial evidence of a positive association between increasing body weight and the development of asthma applying to both sexes. Finally, we provided longitudinal data, which gave proof of a strong relationship between a history of hay fever and later occurrence of asthma.

In the 8-year study period, 3.5% of the male subjects and 5.0% of the female subjects developed asthma. The probability was higher for younger subjects, especially for adolescent girls. This sex difference has been pointed out in several previous studies,16 among which, another Scandinavian study emphasized the high incidence among adolescent girls. We found incidence rates of relatively high magnitude compared to previously reported findings. In a retrospective study of 15,813 individuals who were 16 to 50 years of age (period under study, 1959 to 1993) by Torén and Hermansson,17 overall incidence rates of physician-diagnosed asthma of 1.1 per 1,000 person-years among male subjects and 1.3 per 1,000 person years among female subjects were noted. Another study from Sweden18 among 4,754 subjects who were 36 to 67 years of age and were studied from 1986 to 1996 showed a 10-year cumulative incidence of self-reported asthma of 3.2% in male subjects and 4.5% in female subjects. A comparable finding was reported by Eagan and colleagues19 from Norway for subjects studied from 1986 to 1997, yet with a trend toward lowest incidence among female subjects, and concluding with an 11-year cumulative incidence of 4.0% among male subjects and 3.5% among female subjects who were 15 to 70 years of age. Additionally, several other studies342021 on adult-onset asthma, mainly American, have reported incidence rates of a comparably lower scale compared to ours. Heterogeneity among the earlier reported findings could reflect differences in diagnostic tools, discrepancies between studied age groups and the time of the surveys, as well as diagnostic mix-up with COPD.

We used self-reported asthma (ie, asking the question "Do you have, or have you ever had asthma?") as the diagnostic approach, which is a method that has proven to have a high specificity for the diagnosis of asthma and, hence, is suitable for excluding false-positive cases.12 The high incidence found in our study could therefore reflect a true increase in the prevalence of asthma among Danish adults.22 Thus, despite other factors possibly influencing the outcome, such as lack of recall regarding asthma in childhood, as well as heightened awareness due to asthma being discussed extensively in public, both of which give rise to an overestimation of the actual number of incident cases, we concluded that asthma is a disease with a continuing high incidence past childhood.

It has been shown that obesity and increasing levels of BMI are associated with incident asthma, especially among adult women,6 but also among men.23 However, it has been argued2425 that the relationship between overweight and the occurrence of asthma is a spurious one, emphasizing the fact that objective signs of airflow obstruction are lacking in obese populations despite increased reporting of respiratory symptoms and increased use of bronchodilators. We found an increasing probability of incident asthma for all levels of BMI from 20 to about 30 (ie, in the normal weight to lightly overweight range of the spectrum), with a constant greater risk among female subjects. From BMI levels of about ≥ 28, however, the SDs became so large, due to the few subjects in these BMI categories, that the effect of BMI on the risk of asthma was difficult to interpret. We found no association of statistical significance between sedentary lifestyle (ie, low levels of leisure time physical activity) and asthma. In line with this, it has been shown that low energy expenditure from leisure time physical activity cannot explain the positive association between obesity and asthma.26 Still, ß2-adrenoceptor polymorphisms are found to be positively associated with adult-onset asthma in sedentary women compared to physically active women with the same genotype.27 That finding showed that risk alleles might only become observable in risk environments, thus explaining why small but causal associations can be left unnoticed when studying genetically and environmentally heterogeneous populations. We concluded that if the relationship between overweight and asthma is causal, this heightened susceptibility is most likely to be explained by inadequately understood biochemical changes associated with weight gain, or by the changes in lifestyle accompanying it. Further, a possible, but not yet documented, pleiotropic effect of genes conferring risk to the development of both phenotypes needs to be taken into account.

We found no statistically significant impact of smoking on the development of asthma. Previous findings in this area have been conflicting. Including older subjects (ie, those > 50 years of age) in surveys with self-reported asthma as a diagnostic criterion could lead to misclassification owing to confusion about COPD and asthma, thus overestimating the number of affected subjects. On the basis of our data, we are still, however, not able to find any proof of a causal relationship between smoking and the development of asthma.

Our data indicated that a substantial portion of cases of adolescent-onset and adult-onset asthma are preceded by hay fever and/or eczema. This view is supported by Burrows and colleagues,28 who have shown that most, if not all, asthma has an allergic basis. This does not neglect the fact that two different phenotypes, as judged by skin test reactivity, can be distinguished, especially in adulthood, with the nonallergic form, which is often associated with female sex and a poorer prognosis, being the more severe.29 Nevertheless, although we found a statistically significant association between atopic markers, such as hay fever and eczema, and the later development of asthma, we propose that it might be pathophysiologically redundant to state this association, since hay fever, eczema, and asthma are manifestations of the same disease entity.30 This view is supported by data from the bulk of epidemiologic studies53132 and from several studies of cellular biology3334 that outline evidence of rhinitis and asthma being a comorbid disease with systemic inflammatory cross-talk.3536 However, when subjects are asked whether they have, or have had asthma, it is likely that they will refer to a more chronic state of the disease, and it is doubtful that few periodic or infrequent attacks of wheezing occurring concomitantly with an attack of hay fever, in the subject’s perception, will qualify as a diagnosis of asthma. The picture is further blurred by the fact that inflammatory changes are present in the lower airways of atopic nonasthmatic subjects even before the onset of symptoms.37 The searching for risk factors associated with asthma in this setting likely will reveal an association with a persistent wheezing state, and not with early manifestations of the disease.

We need to take into account that conclusions about incidence rates and risk factors for the development of asthma in this study were inferred on the basis of twin data. However, it seems reasonable to extend the results to the general population when there are no differences in the etiology or the prevalence of the disease between twins and singletons. Twins are on average born 3 weeks prior to term with a birth weight that on average is 1,000 g below that of singletons. One might therefore suspect that this would tend to confer an increased risk among twins for the later development of diseases such as asthma and allergy. According to the fetal origins hypothesis, it has been argued38 that a heightened risk for the occurrence of chronic diseases later in life can be partly attributed to intrauterine growth retardation and to suboptimal development during fetal life. Following this, low birth weight has been associated with the subsequent development of wheezing illness in some studies (ie, Schwartz et al39 reported that a 2-SD deficit [1,162 g] in birth weight increased the risk of childhood wheeze by a factor 1.4). It is, however, not clear whether this increased risk also applies to the type of growth retardation observed in multiple pregnancies. In the face of these results, Räsänen et al40 studied the relationship between birth weight and the risk for asthma in adolescent twins and found no increased risk among subjects with low birth weight. In fact, some studies have shown that the prevalence of atopic disease in twins is indeed somewhat lower than that found in the general population. A reduced hospital admission rate due to asthma (rate ratio, 0.47) was found among Scottish twin children,41 and, further, a reduced prevalence of asthma was found among Swedish twin army conscripts (4.9% vs 5.9% in singletons).42 But even with variation in the reported results, and acknowledging that subtle differences may exist, we are still confident in stating that the conclusions drawn from this study can apply to the general population.

In conclusion, we found a notably high incidence of asthma past childhood, which was most pronounced among female subjects. Furthermore, we observed that increasing levels of BMI, even in the normal range of the weight spectrum, are associated with a greater likelihood of developing asthma for both sexes. Finally, we found that a substantial portion of adult asthma is preceded by upper airway allergic symptoms and/or eczema, indicating a shared pathogenesis.


   Acknowledgements
 
We thank Axel Skytthe, MSc, PhD, from The Danish Twin Registry for invaluable help with the management of the data.


   Footnotes
 
Abbreviations: BMI = body mass index; CI = confidence interval; OR = odds ratio

This study was supported by sponsorships from The Health Insurance Foundation, The Copenhagen Hospital Corporation, and The Danish Lung Association.

Received for publication June 3, 2004. Accepted for publication December 7, 2004.


   References
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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Right arrow Articles by Backer, V.

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