Abstract
Obesity is a major risk factor for poorly controlled asthma, but the reasons for poor asthma control in this patient population are unclear. Symptoms of depression have been associated with poor asthma control, and increase with higher body mass index (BMI). The purpose of this study was to assess whether depressive symptoms underlie poor asthma control in obesity.
Methods
We determined the relationship between BMI, psychological morbidity and asthma control at baseline in a well-characterized patient population participating in a clinical trial conducted by the American Lung Association-Asthma Clinical Research Centers.
Results
Obese asthmatic participants had increased symptoms of depression (Center for Epidemiologic Studies Depression Scale score in lean 10·1±8·1, overweight 10·0±8·1, obese 12·4±9·9; p=0·03), worse asthma control (Juniper Asthma Control Questionnaire score in lean 1·43±0·68, overweight 1·52±0·71, obese 1·76±0·75; p<0·0001), and worse asthma quality of life (scores in lean 5·21±1·08, overweight 5·08±1·05, obese 4·64±1·09; p<0·0001). Asthmatics with obesity and those with symptoms of depression both had a higher risk of having poorly controlled asthma (adjusted odds ratio of 1·83 CI 1·23-3·52 for obesity, and 2·08 CI 1·23-3·52 for depression), but there was no interaction between the two.
Conclusion
Obesity and symptoms of depression are independently associated with poor asthma control. As depression is increased in obese asthmatics it may be an important co-morbidity contributing to poor asthma control in this population, but factors other than depression also contribute to poor asthma control in obesity.
Keywords: obesity, asthma, depression
Introduction
Obesity is a significant risk factor for developing asthma and is associated with poor asthma control.1, 2 Depression and anxiety are likewise associated with poor asthma control, and the prevalence of depression and anxiety are dramatically increased in obesity. The underlying interaction between obesity, depression, and asthma is not well understood, yet may have critical implications for asthma control in the setting of obesity.
Obesity is associated with decreased responsiveness to controller medication and poor asthma control.3 One study found that obese asthmatics are hospitalized at nearly five times the rate of lean asthmatics.4 Given the ever increasing prevalence of obesity,5 obesity is contributing to an epidemic of poorly controlled asthma.
A number of studies suggest that anxiety and depression adversely affect asthma symptom severity and there is a significant correlation between severity of depressive symptoms and poor asthma control.6, 7 Depressed asthmatics also have an increased risk of asthma-related emergency department visits and poor adherence to asthma medication regimens.8
Depression is a very common comorbidity associated with obesity.9 The strong association between high BMI and depressive symptoms is more pronounced in women, the demographic group with the highest rate of asthma related to obesity.3 This relationship is reversible as weight reduction surgery significantly reduces symptoms of anxiety and depression among obese asthmatics,10 this surgery also improves asthma control.11 Considering that depression is increased in obesity, such psychological comorbidity may contribute significantly to the poor asthma control characteristic of obese asthmatics.
The purpose of this study was first to determine if depression and obesity were associated with poor asthma control, and then to determine if depression could explain poor asthma control in obesity. We evaluated the relationship of both markers of depression and measures of asthma control with obesity, hypothesizing that a significant interaction between obesity and depression would contribute to worse asthma control among obese asthmatics. This study was completed in a well characterized, patient population participating in a clinical trial of the placebo response in asthma.
Methods
Data on obesity and symptoms of depression were derived from participants in a multicenter clinical trial designed to assess the placebo effect in asthma performed by the American Lung Association Asthma Clinical Research Centers. Details of the main study and eligibility criteria have been published elsewhere, and are summarized below.12 The study was approved by the Institutional Review Boards at all participating centers, and all participants signed informed consent.
Males and females at least 15 years of age who had been diagnosed with asthma by a physician, regularly used any prescribed asthma medication in the last 12 months, and had a post-bronchodilator forced expiratory volume (FEV1) ≥ 75% predicted were included in the trial. Participants had inadequate control of asthma symptoms indicated by one of the following: short-acting β2 agonist use two or more times per week for relief of asthma symptoms, nocturnal awakenings once or more per week due to asthma symptoms, or a Juniper Asthma Control Questionnaire (ACQ) score of ≥ 1·5 at their enrollment visit.
Participants were excluded if they had a significant smoking history (≥ 10 pack years or active smoking in the past 6 months), or had used montelukast or other leukotriene antagonists within the past 14 days. Participants were also excluded if they reported a history of hospitalization, emergency department visits, or prednisone use for asthma within the past 3 months, past respiratory failure secondary to asthma, or prior adverse reaction to montelukast. At baseline, participants were extensively evaluated for their asthma characteristics with the Juniper Asthma Control Questionnaire,13 and the Juniper Asthma Quality of Life Questionnaire.14 Spirometry was performed according to ATS guidelines.15 Symptoms of depression were measured by the Center for Epidemiological Studies Depression Score (CES-D).16, 17 Participants’ asthma knowledge and sense of asthma self-efficacy were measured by the Knowledge, Attitude, and Self-efficacy Asthma Questionnaire (KASE-AQ).18
Statistical Approach
Descriptive statistics were used to summarize baseline characteristics of the study subjects, divided into three categories according to body mass index (BMI): lean (BMI 18·5-24·9 kg/m2), overweight (BMI 25-29·9 kg/m2), and obese (BMI ≥ 30 kg/m2). Continuous variables were compared using analysis of variance, with log transformations for non-parametric variables, and proportions were compared using χ2 analysis. Post-hoc comparison of groups was performed using the Bonferroni procedure.
We determined the risk of poor asthma control associated with obesity (defined as a BMI ≥ 30) compared to non-obese (defined as those with a BMI < 30) and depression (defined as a CES-D score ≥ 16 compared to those with a score < 16). We performed multiple logistic regression including sex, age, race, education, income and employment status in the final model. We evaluated the relationship between asthma control and symptoms of depression, using an interaction term for obesity (BMI > 30 kg/m2) and significant symptoms of depression (defined as a CES-D score ≥ 16). Analyses were performed with STATA 10·0 (College Station, Texas).
Role of Funding Source
The study sponsors had no role in study design, data collection, data analysis, data interpretation or decision to submit manuscript. The corresponding author had full access to all the data, and the final responsibility for the decision to submit for publication.
Results
Participant characteristics
A total of 601 unique participants were enrolled in the primary study. Participant demographic characteristics are summarized in Table 1. The mean age of participants was 32 years in the lean group, overweight and obese asthmatic participants were significantly older. Most participants were female, constituting nearly 82% of the obese group. There was a higher proportion of African American participants in the obese category. Obese asthmatics reported completing less education than leaner participants, though there was no overall difference in reported income. Employment status differed among the BMI categories, with a higher proportion of students in the lean category.
Table 1.
Baseline characteristics of participants
| Lean | Overweight | Obese | p value | |
|---|---|---|---|---|
| n (%) | 205 (34%) | 164 (27%) | 232 (39%) | |
| Demographic characteristics | ||||
| Age (years) | 32.4±13.3 | 40.5±14.9* | 41.1±12.6* | <0.0001 |
| BMI (kg/m2) | 22.3 (20.9-23.7) | 27.2 (26.0 – 28.3) | 35.0 (32.6-41.1) | < 0.001 |
| Women | 140 (68) | 106 (63) | 191 (82) | |
| Race or ethnic group (%) | ||||
| White | 144 (69) | 104 (64) | 114 (49) | <0.001 |
| Black | 45 (22) | 54 (32) | 102 (44) | |
| Hispanic | 6 (3) | 1 (1) | 1 (0) | |
| Other | 10 (6) | 5 (3) | 15 (7) | |
| Highest level of Education (%) | ||||
| < High school | 19 (9) | 11 (7) | 19(8) | <0.001 |
| High school | 20 (10) | 22 (13) | 45 (20) | |
| Some college | 81 (39) | 62 (37) | 117(50) | |
| Bachelor’s degree | 48 (23) | 38 (23) | 27 (12) | |
| Some post-graduate | 15 (7) | 10 (6) | 11 (5) | |
| Post-graduate degree | 22(11) | 21 (13) | 13 (6) | |
| Employment status (%) | ||||
| Student | 64 (30) | 19 (12) | 16 (7) | <0.001 |
| Not working | 16 (8) | 15 (9) | 30 (13) | |
| Full time | 86 (42) | 94 (57) | 114 (49) | |
| Part time | 25 (12) | 16 (9) | 29 (13) | |
| Retired | 6 (3) | 12 (7) | 12(5) | |
| Disabled | 3 (1) | 3 (2) | 19 (8) | |
| Other | 5 (2) | 5 (3) | 12 (5) | |
| Household Income (%) | ||||
| < $20,000 | 48 (23) | 21 (13) | 59 (25) | 0.22 |
| $20,000 - $50,000 | 57 (28) | 52 (31) | 74 (32) | |
| $50,000 - $75,000 | 24 (12) | 21 (13) | 23 (10) | |
| > $75,000 | 23 (11) | 23 (14) | 20 (9) | |
| Declined to answer | 37 (18) | 36 (22) | 42 (18) | |
| Don’t know | 16 (8) | 11 (7) | 14 (6) | |
Values shown are mean ± SD or median (IQR) for continuous variables, and n (%) for proportions. P values shown are for analysis of variance for continuous variables, and χ2 test for proportions.
P < 0.05 compared with lean group
Asthma characteristics
Data on asthma characteristics in the distinct BMI groups are reported in Table 2. Obese and overweight asthmatics reported significantly later-onset asthma than lean asthmatics. Obese asthmatics tended to report more frequent use of oral prednisone for asthma. Obese participants had worse asthma control as assessed by the Juniper Asthma Control Questionnaire (ACQ) and worse asthma-related quality of life as assessed by the Asthma Quality of Life Questionnaire (AQLQ) compared with both lean and overweight asthmatics.
Table 2.
Asthma characteristics & pulmonary function
| Lean | Overweight | Obese | p value | |
|---|---|---|---|---|
| Age asthma onset (years) | 14.9±16.7 | 21.7±22.73 | 22.1±20.83 | 0.0001 |
| Pack years | 3.6±2.8 | 4.1±3.0 | 4.0±3.1 | 0.8 |
| Number of Courses of Prednisone use in last 12 months (n{%}) | ||||
| 0 | 177 (78) | 146 (77) | 183 (69) | 0.09 |
| 1 | 32 (14) | 28 (15) | 45 (17) | |
| ≥2 | 17 (8) | 15 (8) | 36 (14) | |
| Asthma questionnaires , mean ± SD | ||||
| ACQ (↓ score range, 0-6) 1 | 1.43±0.68 | 1.52±0.71 | 1.76±0.753,4 | <0.0001 |
| AQLQ (↑ score range, 1-7) 3 | 5.21±1.08 | 5.08±1.05 | 4.64±1.093,4 | <0.0001 |
| Pulmonary function measures, mean ± SD | ||||
| PEF (L/min) | 404.2±96.1 | 398.6±95.1 | 385.9±93.4 | 0.12 |
| FEV1 (% predicted pre BD) 2 | 88.4±13.5 | 85.6±13.2 | 84.6±13.43 | 0.01 |
| FVC (% predicted pre BD) 2 | 97.7±13.0 | 94.4±12.83 | 91.8±13.03 | <0.0001 |
| FEV1/FVC (pre BD) | 75.6±9.2 | 74.3±9.1 | 75.7±7.6 | 0.16 |
| FEV1 % change after BD | 8.9±10.2 | 9.9±10.9 | 8.8±13.0 | 0.63 |
| FVC % change after BD | 2.5±6.1 | 4.5±9.13 | 4.5±11.13 | < 0.001 |
Values shown are mean and SD, and are compared by analysis of variance and n (%) for proportions
ACQ, Asthma Control Questionnaire
AQLQ, Asthma Quality of Life Questionnaire
PEF, morning peak expiratory flow
FEV1, forced expiratory volume in 1 second
FVC, forced vital capacity
BD, bronchodilator
↓, Lower score is better; ↑Higher score is better
Predicted values for FEV1 and FVC are taken from Hankinson et al.32
p< 0.05 compared with lean group
p < 0.01 compared with overweight group
Data on pulmonary function are also provided in Table 2, and differed among participants. Obese asthmatics had significantly lower FEV1 and FVC than lean asthmatics, and obese and overweight asthmatics had greater change in FVC in response to bronchodilator than lean asthmatics.
Psychological morbidity
Obese asthmatics had higher depression scores as assessed by the Center for Epidemiologic Studies Depression Scale (CES-D) and more frequently surpassed the reported thresholds for mild depressive symptoms (a score of 16 and above) as well as probable depression (a score of 23 and above) (Table 3).17 Obese asthmatics also reported significantly lower self-efficacy related to asthma compared with lean and obese asthmatics, and both obese and overweight asthmatics had lower asthma knowledge, as assessed by the Knowledge, Attitude, and Self-Efficacy Asthma Questionnaire (KASE-AQ).
Table 3.
Measures of psychological morbidity
| Lean | Overweight | Obese | p value | |
|---|---|---|---|---|
| CES-D ( 1 ↓ score range, 0-60) median (IQR) | ||||
| 8 (4-24) | 8 (4-24.5) | 10 (5-16) | 0.03 | |
| CES-D level of depression 2 n (%) | ||||
| CES-D no depression | 163 (80) | 129 (79) | 169 (73) | 0.01 |
| CES-D mild symptoms | 26 (13) | 25 (15) | 26 (11) | |
| CES-D probable depression | 16 (7) | 10 (6) | 37 (16) | |
| KASE-AQ ( 1 ↑ score range, 5-100) mean ± SD | ||||
| Self-efficacy | 82.4±8.4 | 82.8±9.2 | 79.8±9.33,4 | 0.001 |
| Attitude | 85.4±7.2 | 85.5±7.6 | 85.3±6.4 | 0.96 |
| Knowledge | 12.0±2.8 | 11.1±2.93 | 11.0±3.03 | 0.0005 |
↓, Lower score is better
CES-D, Center for Epidemiologic Studies Depression Scale, threshold for mild depressive symptoms ≥ 16, probable depression ≥ 23.
KASE-AQ, Knowledge, Attitude, and Self-Efficacy Asthma Questionnaire
↑, Higher score is better
p< 0.05 compared to lean group
p < 0.05 compared to overweight group
Combined effect of depression and obesity
Both obesity and having symptoms of depression increased the risk of having poorly controlled asthma, as defined by a score of 1·5 or greater on the Juniper Asthma Control Score (311 out of 605 participants had a score of 1·5 or greater when depression symptoms were assessed at the second study visit) (Table 4).
Table 4.
Risk of Poor Asthma Control in those with Obesity and/or Depression
| Odds Ratio | CI | |
|---|---|---|
| Obesity 1 | 2.06 | 1.48-2.88 |
| Depression 1 | 2.44 | 1.65-3.63 |
| Obesity 2 | 1.83 | 1.23-3.52 |
| Depression 2 | 2.08 | 1.23-3.52 |
Poor Asthma control was defined as a score of ≥ 1.5 on the Juniper Asthma Control questionnaire
Uni-variate analysis for depression (using threshold of CES-D ≥ C16) and obesity separately.
multivariate analysis combining depression and obesity in the same model, which also includes age, sex, race, education, employment, and income an interaction value for presence of obesity and depression (p = 0.58).
When both obesity and depression were considered in the same model, there was little change in the odds of having poorly controlled asthma, and the interaction between obesity and asthma was not significant (p = 0·58), suggesting that obesity and depression contribute independently to poor asthma control. Depressed patients had worse asthma control in all BMI groups, suggesting that the contribution of depression to poor asthma control was not unique to obesity (Table 5).
Table 5.
Asthma control in relation to symptoms of depression in participants of differing BMI groups
| No Depression | Mild Depression | Probable depression | p | |
|---|---|---|---|---|
| Lean | ||||
| Asthma Control | 1.36 ± 0.67 | 1.58 ± 0.56 | 1.89 ± 0.721 | <0.01 |
| Overweight | ||||
| Asthma Control | 1.46 ± 0.66 | 1.62 ± 0.66 | 1.97± 1.21 | 0.07 |
| Obese | ||||
| Asthma Control | 1.67 ± 0.74 | 2.05 ± 0.651 | 1.96 ± 0.77 | 0.01 |
Values shown are mean ± SD from ACQ, Asthma Control Questionnaire
Mild depression was defined using a threshold of CES-D ≥ 16, probable depression as CES-D ≥ 23
p < 0.05 compared with lean group
Discussion
This study demonstrates that obese asthmatics have poor asthma control, worse asthma-specific quality of life, and suffer a greater burden of symptoms of depression than leaner asthmatics. Obesity and symptoms of depression are both independently related to poor asthma control, without a significant interaction between the two comorbidities. This suggests that depression should be considered in managing obese patients with poor asthma control as the prevalence of depression increases with BMI, but that poor asthma control in obesity is also related to factors other than depression. This study has important clinical implications with regard to understanding the physical and mental underpinnings of poor asthma control among obese asthmatics.
The present study provides further evidence of the relationship between obesity and poor asthma control as well as worse asthma-related quality of life. Obesity is not only a risk factor for incident asthma, but is also associated with worse control characterized by increased symptoms, more frequent use of rescue bronchodilator medications, increased risk of hospitalizations for asthma, and missed work days.2, 7, 19 Obesity is a significant cause of poorly controlled asthma due to many factors such as altered lung mechanics, altered responses to medications, elevated airway oxidative stress, effects of adipokines and cytokines, and other comorbidities which occur in obesity such depression and obstructive sleep apnea.3 We have previously reported that symptoms of obstructive sleep apnea are associated with worse asthma control,20 but few studies have investigated the role of psychological morbidity in the poor asthma control of obesity.
Asthmatics are more likely to suffer from anxiety and depression than the general population, irrespective of BMI.21 Data from the 2002 World Health Survey collected by the World Health Organization across 54 countries suggested that depression was significantly associated with asthma in 65% of countries.22 There may be a causal link between depression and asthma; in a longitudinal 20 year follow up CARDIA study by Brunner et al, elevated depressive symptoms were associated with a 1.26 increased risk of developing incident asthma (independent of BMI).23 Depression in asthmatics has been associated with poor asthma control,21, 24 with one study reporting that comorbid depression was associated with greater health care utilization and 51% higher health care costs.25 Depression may contribute to poor asthma control through a number of pathways. Asthmatics with psychological comorbidity may perceive a greater intensity of breathlessness.21 Asthmatics with depressive symptoms may also develop cholinergic-mediated airway constriction in the event of psychological stress.26, 27 Depression may also affect medication adherence: high levels of depressive symptoms are associated with an 11-fold increase in odds of poor adherence (measured electronically) to inhaled corticosteroid therapy after hospitalization for an asthma exacerbation.27 It is also possible that poor asthma control contributes to the development of depression. In the current study we found that over 20% of the study population reached the threshold for mild depression on the validated CES-D questionnaire, which is in line with previous reports on the prevalence of depression in asthma.8,6
Asthmatic participants with symptoms of depression were approximately twice as likely to have poor asthma control as those without symptoms of depression. Our data provide further evidence that symptoms of depression are associated with poor asthma control and worse asthma quality of life. Many studies suggest there is a significant relationship between depression and obesity. Meta-analyses of cohort studies suggest a significant association between obesity and depression;9, 28 one meta-analysis of 17 community based studies encompassing 204,507 participants reported a significant association between depression and obesity, particularly among females (OR, 1·26; 95% CI, 1·17-1·36).9 Our current study demonstrates that obese asthmatics had significantly higher scores on the CES-D questionnaire and a higher prevalence of depression. Many factors may contribute to the increased risk of depression with obesity. Obesity and depression share common risk factors such as low socioeconomic status and insufficient physical activity.29 Psychological distress may be worsened by obesity because of social stigmatization which produces low self-worth and self-esteem, a negative body image, guilt, and peer isolation.9, 28, 29 Hypothalamic-pituitary-adrenal axis dysfunction from psychological distress elevates circulating cortisol levels which may contribute to abdominal obesity. Depression and obesity likely share common risk factors and may in part share a common pathophysiology, whether these factors interact with each other to produce the worse asthma control characteristic of obesity is not known.
A few studies have addressed the potential for a concurrent interaction between obesity and depression in mediating poor asthma outcomes. Data collected from the 2006 European National Health and Wellness Survey of 37,476 adults demonstrated that less educated, obese, and depressed asthmatics experience significantly poorer asthma control.30 Acosta-Perez et al examined the effects of obesity and depressive/anxiety disorders co-occurring in a community sample of Puerto Rican youth 10 to 19 years of age diagnosed with asthma: depression/anxiety was three times more common in the obese, but asthma exacerbations were associated with an increased prevalence of psychological comorbidity among the non-obese youth only.31 A recent single center Canadian study reported that depression appeared to explain poor asthma control in obese asthmatics, this differs from our own findings; these differing results are likely related to differences in the two study patient populations (our own being a multi-center study with a younger more diverse U.S. patient population).32 Our current study demonstrates a clinically meaningful effect of obesity and depression independently contributing to significantly poorer asthma control. The presence of depression contributed to poor asthma control in all BMI groups. Contrary to our hypothesis, there was no significant interaction between obesity and depression, suggesting that the mechanisms linking depression and asthma are the same in lean patients as they are in obese patients, though obese patients have a higher prevalence of depression. Awareness of the finding that depression contributes to poor asthma control is likely critical in the management of both lean and obese patients with asthma.
This study does have some limitations. The patient population was recruited for a clinical trial and so may not reflect the general asthma population, although ethnic and economic diversity in the population was strong. This was a cross-sectional study, and so we cannot draw any conclusions about the direction of the association between asthma and depression.
This study shows that depression likely contributes to poor asthma control in obese patients, as obese patients have a higher prevalence of depression than lean asthmatics, and depression is associated with poor asthma control. However, obesity also contributes to poor asthma control independent of depression; understanding poor asthma control in obesity requires research into the pathophysiology of airway disease in obesity. This study suggests that interventions to address psychological comorbidity should be studied in obese asthmatics, and that improving asthma control in obese asthmatics will require a holistic approach to improve asthma outcomes.
Acknowledgments
Funding: Supported by the American Lung Association, and NIH grants R01HL073494 and P30 RR031158-01
Footnotes
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