Abstract
Objective:
We hypothesized that children with obesity-related asthma would have worse self-reported asthma control, report an increased number of asthma symptoms and have lower FEV1/FVC associated with worse clinical asthma outcomes compared to children with asthma only.
Methods:
Cross sectional analyses examined two hundred and eighteen (obesity-related asthma = 109, asthma only = 109) children, ages 7–15 that were recruited from clinics and hospitals within the Bronx, NY. Pulmonary function was assessed by forced expiratory volume in the first second (percent predicted FEV1) and the ratio of FEV1 to the forced vital capacity of the lungs (FEV1/FVC). Structural equation modeling examined if pulmonary function was associated with asthma control and clinical outcomes between groups.
Results:
Lower percent predicted FEV1 was associated with increased hospitalizations (p =.03) and oral steroid bursts in the past 12 months (p =.03) in the obesity-related asthma group but not in the asthma only group. FEV1/FVC was also associated with increased hospitalizations (p = .02) and oral steroid bursts (p = .008) in the obesity-related asthma group but not the asthma only group. Lower FEV1/FVC was associated with the number of asthma symptoms endorsed in the asthma only group but not in the obesity-related asthma group. Percent predicted FEV1 and FEV1/FVC was not associated with asthma control in either group.
Conclusions:
Pulmonary function was associated with oral steroid bursts and hospitalizations but not self-reported asthma control, suggesting the importance of incorporating measures of pulmonary function into the treatment of pediatric obesity-related asthma.
Keywords: Asthma Control, Oral Steroids, Body Mass Index, Health Disparities, Healthcare Utilization
Introduction
Asthma and obesity are two of the most common chronic pediatric conditions that substantially worsen each other 1,2. There is a complex interaction of mutual causality that exists between pediatric obesity and asthma. A large body of literature suggests that obesity may predispose people to asthma, with higher Body Mass Index (BMI) generally elevating the risk for asthma diagnosis in children 3–7. In a longitudinal study, researchers found that the adjusted risk for asthma in overweight and obese youth compared to asthma only youth was 1.17 and 1.26 respectively 8. Conversely, there is evidence that asthma may contribute to the development of obesity 9–11.
Children with obesity-related asthma have worse asthma outcomes than children with asthma alone. Obesity-related asthma in children is associated with greater asthma severity 12,13, worse asthma control 14, and more frequent asthma symptoms 15. Children with obesity-related asthma also use more quick relief medications 12,14, require more oral steroid bursts 12,14,16, have more asthma-related emergency room (ER) visits 12,15,16, and hospitalizations in intensive care than their asthma only counterparts 17. Children with obesity-related asthma are also less responsive to their controller medications including inhaled corticosteroids, as well as their quick relief medications 18,19. This higher asthma morbidity may partly be explained by worse pulmonary function in obese children as compared to children with asthma only.
Obese children with asthma have lower FEV1/FVC ratios as compared to children with asthma 20–24. In a longitudinal study, researchers found that children with asthma who became obese had significantly lower FEV1/FVC ratios as young adults compared to those who remained nonobese 25. However, few studies have examined the association between the percent predicted FEV1 and FEV1/FVC ratio with clinical outcomes and asthma symptoms specifically in children with obesity-related asthma compared to children with asthma.
The current study conducted secondary data analyses in an ethnically diverse sample of pediatric patients to examine associations between pulmonary function measures (percent predicted FEV1 and FEV1/FVC), clinical outcomes (e.g., asthma-related ER visits, hospitalizations, and oral steroid bursts) and asthma control, both as a composite measure and individual asthma symptom categories. We hypothesized that children with obesity-related asthma would have worse self-reported asthma control and report an increased number of asthma symptoms compared to children with asthma only. Additionally, we hypothesized that lower FEV1/FVC would be associated with worse clinical asthma outcomes and worse self-reported asthma control in the obesity-related asthma group than in the asthma only group, supporting FEV1/FVC as a more sensitive pulmonary function measure to examine in youth with obesity-related asthma.
Materials and Method
Procedure and Participants
Data was collected cross-sectionally during the baseline sessions of a study that examined obesity-related asthma 20 and a separate study on asthma symptom perception, medication adherence, and clinical asthma outcomes 26,27. Furthermore, data collected from these studies were approved by the affiliated Institutional Review Boards. Participants were 7–15 years old, Black and Latino children diagnosed with asthma (total N = 218). Participants were eligible if they had an asthma diagnosis from a physician and were prescribed a controller medication. Exclusion criteria for the study included any severe learning disabilities that were deemed to interfere with study participation. Questionnaires were administered to participants at the baseline session. Participants with a BMI greater than or equal to the 95th percentile were included in the obesity-related asthma group and all other children with a BMI less than the 85th percentile were included in the asthma only group. Informed consent and assent was gathered from participants who were recruited from asthma clinics, primary care clinics, or mailings from providers located in the Bronx, New York.
Clinical Asthma Outcomes
Asthma outcomes were also evaluated via parent self-report of their children’s ER visits, hospitalizations, and oral steroid bursts due to asthma in the past 12 months. ER visits, hospitalizations, and oral steroid bursts due to asthma were categorized as either none or 1 or more.
Asthma Control
Parents provided self-report of their child’s daytime and night-time symptoms, quick relief-medication use, and daily activity limitations due to asthma. Overall asthma control and the number of individual asthma symptoms was determined based on National Heart, Lung, and Blood Institute guidelines. 28 Overall asthma control was determined if asthma symptoms met criteria for either well-controlled, not well-controlled or very poorly controlled asthma. The number of individual asthma symptoms was assessed based on how many symptoms were reported that met criteria for either not well controlled or very poorly controlled asthma 28.
Additional Measures
Demographic information collected included age, sex, and race/ethnicity. BMI was calculated based on anthropometric measures of height, weight, age and sex. Pulmonary function was measured through spirometry testing following American Thoracic Society guidelines 29 and the National Health and Nutrition Examination Survey (NHANES III) was used for the spirometry reference equations in the present study 30. Percent predicted FEV1 and FEV1/FVC were retained in the analysis as measures of airflow obstruction. For these two pulmonary function variables (percent predicted FEV1 and FEV1/FVC), there were missing data for 14 participants across both groups (N = 218).
Statistical Analyses
Descriptive statistics were run (i.e., mean, standard deviation, frequency, percentage) to characterize the sample and bivariate associations between key demographic variables and clinical outcome measures. Differences between the obesity-related asthma group and the asthma only group were analyzed with χ2 tests for categorical variables (e.g., asthma control) using SPSS Statistics Version 27.
Two-group (obesity-related asthma and asthma only) structural equation models (SEM) were used to address the study hypotheses for the following endogenous variables: asthma control, number of symptoms, steroid bursts, ER visits and hospitalizations. Separate models were run for each outcome variable. The chi-square difference test evaluated whether the models for the obesity-related asthma groups were significantly different from the models for the asthma only group. Each model included a variable Study Group for examination of whether findings differed by which study data were obtained from. The first set of SEM models included the following exogenous variables: age, sex, race/ethnicity, inhaled corticosteroid use, and FEV1/FVC. The analyses were repeated replacing FEV1/FVC with FEV1. Adjusted standard errors were examined and model fit indices computed using maximum likelihood estimation. Following conventions outlined by Kline 31,32, our criteria for assessing adequacy of fit were: χ2/df ratio of less than 2, comparative fit index (CFI) and Tucker-Lewis Index (TLI) at or above 0.90, a root mean square error approximation (RMSEA) at or below 0.05 and standardized root mean square residual (SRMR) <0.08. MPlus version 8.8 33 was used for the SEM analyses.
Missing Data
SEM allows for missing data on the endogenous variable using full maximum likelihood methods which assume that the data are missing at random. Multiple imputation was done when exogenous variables were missing.
Results
Participant descriptive characteristics are displayed in Table 1. The mean age of children was approximately 10 years across both the obesity-related asthma group and the asthma only group. The sample (N = 218) was comprised of 54.1% males, 47.7% Black, and 45.4% Hispanic children, with most participants reporting current use of a controller medication (ICS or LTRA or both) for asthma (62.4%). On average, 53% of participants reported using quick relief medications less than or equal to 2 days per week. Overall asthma control based on NHLBI categorization showed that half of the participants reported very poor asthma control (50.0%) (Table 2). In the past year, most participants reported an ER visit (67.9%), oral steroid use (64.2%) but no hospitalizations in the past year (82.1%).
Table 1.
Participant Demographics and Medication Use Descriptive Statistics
Total (N = 218) | Obesity-related Asthma Group (n =109) | Asthma only Group (n = 109) | p | |
---|---|---|---|---|
Age (M, SD) | 9.99 (1.94) | 9.91 (1.87) | 10.07 (2.01) | .530 |
Child Gender (n, %) | .057 | |||
Male | 118 (54.1) | 66 (60.6) | 52 (47.7) | |
Female | 100 (45.9) | 43 (39.4) | 57 (52.3) | |
Child Race (n, %) | .907 | |||
Black | 104 (47.7) | 53 (48.6) | 51 (46.8) | |
Hispanic | 99 (45.4) | 48 (44.0) | 51 (46.8) | |
Other | 15 (6.9) | 8 (7.3) | 7 (6.4) | |
BMI (M, SD) | 22.74 (6.97) | 28.30 (5.55) | 17.18 (2.15) | <.001 |
Quick Relief Use (n, %) b | .117 | |||
less than or equal to 2 days | 114 (53.0) | 63 (58.3) | 51 (47.7) | |
more than 2 days | 101 (47.0) | 45 (41.7) | 56 (52.3) | |
ICS Use (n, %) | .058 | |||
Yes | 110 (50.5) | 62 (56.9) | 48 (44.0) | |
No | 108 (49.5) | 47 (43.1) | 61 (56.0) | |
LTRA Use (n, %) | .404 | |||
Yes | 84 (38.5) | 45 (41.3) | 39 (35.8) | |
No | 134 (61.5) | 64 (58.7) | 70 (64.2) | |
Any Controller Use (n, %) | .162 | |||
Yes | 136 (62.4) | 73 (67.0) | 63 (57.8) | |
No | 82 (37.6) | 36 (33.0) | 46 (42.2) |
Abbreviations: ICS Use, Inhaled corticosteroids; LTRA Use, Leukotriene receptor antagonists.
Any Controller Use includes participants who were either taking an ICS, LTRA, or both.
Missing 3 participant data for quick relief use; obesity-related asthma group, n = 108 and healthy-weight asthma group, n =107
Table 2.
Asthma Clinical Outcomes and Pulmonary Function Variables Descriptive Statistics
Total (N = 218) | Obesity-related Asthma Group (n =109) | Asthma only Group (n = 109) | p | |
---|---|---|---|---|
Asthma Control (n, %) | .095 | |||
Well Controlled | 38 (17.4) | 21 (19.3) | 17 (15.6) | |
Not Well Controlled | 71 (32.6) | 28 (25.7) | 43 (39.4) | |
Very Poor | 109 (50.0) | 60 (55.0) | 49 (45.0) | |
Number of Asthma Symptoms (n,%) | ||||
Zero | 68 (31.2) | 36 (33.0) | 32 (29.4) | |
One | 38 (17.4) | 19 (17.4) | 19 (17.4) | .647 |
Two | 49 (22.5) | 20 (18.3) | 29 (26.6) | |
Three | 28 (12.8) | 16 (14.7) | 12 (11.0) | |
Four | 35 (16.1) | 18 (16.5) | 17 (15.6) | |
ER Visits past year (n, %) | .772 | |||
1 or more | 148 (67.9) | 73 (67.0) | 75 (68.8) | |
None | 70 (32.1) | 36 (33.0) | 34 (31.2) | |
Hospitalizations past year (n, %) | .596 | |||
1 or more | 39 (17.9) | 21 (19.3) | 18 (16.5) | |
None | 179 (82.1) | 88 (80.7) | 91 (83.5) | |
Oral Steroid Use past year (n, %) a | .434 | |||
1 or more | 140 (64.2) | 75 (70.1) | 65 (65.0) | |
None | 67 (30.7) | 32 (29.9) | 35 (35.0) | |
Pulmonary Function b | ||||
% Predicted FEV1 (M, SD) | 89.79 (14.97) | 90.38 (15.20) | 89.22 (14.77) | .584 |
FEV1/FVC (M, SD) | 84.22 (7.70) | 82.26 (7.68) | 86.15 (7.25) | <.001 |
Missing 11 participant’s data; obesity-related asthma group, n =107 and asthma only group, n =100.
Missing 14 participant’s data; obesity-related asthma group, n = 101 and asthma only group, n = 103.
Of the total sample, there were 109 participants in the obesity-related asthma group and 109 participants in the asthma only group. Table 2 shows that FEV1/FVC was significantly lower in the obesity-related asthma group (M = 82.26, SD = 7.68) than the asthma only group (M = 86.15, SD = 7.25) t(202) = −3.73, p < .001). Overall asthma control was not different between the obesity-related asthma group and the asthma only group. Furthermore, the number of asthma symptoms that met criteria for very poor asthma control did not differ between groups.
Clinical Asthma Outcome Measures and Pulmonary Function
In the obesity-related asthma group, lower percent predicted FEV1 was significantly associated with an oral steroid burst in the past 12 months (β = −0.29, p = .03) but not in the asthma only group (β = −0.20, p = .12) (Table 3). The overall model accounted for a higher proportion of variance of oral steroid bursts in the obesity-related asthma group (25%) than in the asthma only group (15%) and the chi-square difference test revealed that the models were significantly different (χ2 diff = 4.467; p =.03). In the obesity-related asthma group, participants with lower percent predicted FEV1 had more hospitalizations in the past 12 months (β = −0.33, p = .03). FEV1 was not associated with hospitalizations in the asthma only group (β = 0.02, p = .92). The overall models for hospitalizations did not differ between the obesity–related and asthma only groups (χ2 diff = 0.419, p =.52). Additionally, FEV1 was not associated with ER visits in either group.
Table 3.
Asthma Outcomes and % predicted FEV1
Variable | ER Visits (Y/N) | Hospitalizations (Y/N) | Steroid Bursts (Y/N) | |||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
Obesity-related asthma group | Asthma only group | Obesity-related asthma group | Asthma only group | Obesity-related asthma group | Asthma only group | |||||||
Model R2 | .14 | .10 | .19 | .21 | .25 | .15 | ||||||
Χ2
Difference Test |
Χ2 diff=0.765; p=.38 | Χ2 diff=0.419; p=.52 | Χ2 diff=4.467; p=.03 | |||||||||
β (SE) | p-Value | β (SE) | p-Value | β (SE) | p-Value | β (SE) | p-Value | β (SE) | p-Value | β (SE) | p-Value | |
Study Group | −.30 (.12) | .01 | −0.21 (.14) | .15 | −0.13 (.17) | .43 | −0.004 (.16) | .98 | −0.10 (.15) | .51 | −0.03 (.16) | .85 |
Age | −0.05 (.14) | .72 | −0.10 (.14) | .46 | 0.13 (.17) | .46 | −0.29 (.18) | .12 | 0.36 (.15) | .02 | 0.28 (.12) | .02 |
Sex | 0.05 (.13) | .70 | −0.17 (.13) | .17 | 0.08 (.15) | .57 | −0.31 (.17) | .07 | −0.05 (.14) | .71 | −0.08 (.13) | .54 |
Race | 0.14 (.15) | .34 | −0.05 (.11) | .63 | 0.002 (.15) | .99 | 0.20 (.15) | .19 | 0.01 (.14) | .94 | 0.02 (.13) | .86 |
ICS Use | 0.18 (.12) | .14 | 0.23 (.12) | .06 | 0.28 (.16) | .08 | 0.16 (.15) | .28 | 0.24 (.14) | .08 | −0.006 (.14) | .96 |
%FEV1 | −0.04 (.13) | .76 | 0.001 (.12) | 1.00 | −0.33 (.16) | .03 | 0.02 (.21) | .92 | −0.29 (.14) | .03 | −0.20 (.13) | .12 |
Abbreviations: ICS Use, Inhaled corticosteroids
Lower FEV1/FVC was also associated with more oral steroid bursts in the past 12 months in the obesity-related asthma group (β = −0.36, p = .008) but not in the asthma only group (β = −0.20, p = .12; Table 4). The model accounted for a greater percentage of variance of oral steroids in the obesity-related asthma group (29%) than in the asthma only group (14%) and these differences were significant (χ2 diff = 4.986; p =.03). Lower FEV1/FVC in the obesity-related asthma group was associated with more hospitalizations in the past 12 months (β = −0.28, p = .02), but not in the asthma only group (β = −0.004, p = .98). The overall models for hospitalizations were not different between the two groups (χ2diff = 1.048, p =.31). Pulmonary function, both percent predicted FEV1 and FEV1/FVC, was not associated with ER visits in either group.
Table 4.
Asthma Outcomes and FEV1/FVC
Variable | ER Visits (Y/N) | Hospitalizations (Y/N) | Steroid Bursts (Y/N) | |||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
Obesity-related asthma group | Asthma only group | Obesity-related asthma group | Asthma only group | Obesity-related asthma group | Asthma only group | |||||||
Model R2 | .15 | .10 | .18 | .21 | .29 | .14 | ||||||
Χ2
Difference Test |
Χ2 diff=1.247; p=.26 | Χ2 diff=1.048; p=.31 | Χ2 diff=4.986; p=.03 | |||||||||
β (SE) | p-Value | β (SE) | p-Value | β (SE) | p-Value | β (SE) | p-Value | β (SE) | p-Value | β (SE) | p-Value | |
Study Group | −.30 (.12) | .01 | −0.20 (.14) | .15 | −0.18 (.16) | .27 | −0.005 (.16) | .97 | −0.11 (.15) | .43 | −0.005 (.16) | .97 |
Age | −0.06 (.14) | .68 | −0.11 (.14) | .43 | 0.07 (.17) | .70 | −0.29 (.18) | .11 | 0.30 (.14) | .03 | 0.27 (.12) | .03 |
Sex | 0.06 (.13) | .61 | −0.16 (.13) | .20 | 0.12 (.15) | .43 | −0.30 (.18) | .09 | 0.006 (.13) | .96 | −0.04 (.14) | .78 |
Race | 0.15 (.15) | .33 | −0.05 (.11) | .64 | 0.07 (.16) | .68 | 0.20 (.14) | .17 | 0.07 (.14) | .63 | 0.05 (.13) | .73 |
ICS Use | 0.17 (.13) | .17 | 0.22 (.12) | .07 | 0.24 (.16) | .14 | 0.16 (.16) | .31 | 0.18 (.14) | .18 | −0.03 (.14) | .86 |
FEV1/FVC | −0.09 (.16) | .56 | −0.05 (.14) | .72 | −0.28 (.12) | .02 | −0.004 (.18) | .98 | −0.36 (.14) | .008 | −0.20 (.13) | .12 |
Abbreviations: ICS Use, Inhaled corticosteroids
Asthma Control with Pulmonary Function
Percent predicted FEV1 was not associated with asthma control in the obesity-related group (β = −0.02, p = .89) or in the asthma only group (β = 0.16, p = .17; Table 5). Although, the model for asthma control accounted for more variance in the asthma only group (19%) than in the obesity-related asthma group (5%) and the differences were significantly different (χ2 diff = 11.78, p <.001). Similarly, percent predicted FEV1 was not associated with the number of asthma symptoms in the obesity-related group (β = −0.07, p = .46) or in the asthma only group (β = −0.03, p = .77). The model for number of asthma symptoms accounted for more variance in the asthma only group (11%) than the obesity – related asthma group (4%) and the differences were significantly different (χ2diff = 7.81, p =.005).
Table 5.
Asthma Control and % predicted FEV1
Variable | Asthma Control | # Symptoms | ||||||
---|---|---|---|---|---|---|---|---|
Obesity-related asthma group | Asthma only group | Obesity-related asthma group | Asthma only group | |||||
Model R2 | .05 | .19 | .04 | .11 | ||||
Χ2 Difference Test | Χ2 diff=11.783; p=<.0001 | Χ2 diff=7.81; p=.005 | ||||||
β (SE) | p-Value | β (SE) | p-Value | β (SE) | p-Value | β (SE) | p-Value | |
Study Group | 0.14 (.12) | .25 | 0.10 (.11) | .36 | −0.02 (.11) | .84 | −0.10 (.10) | .32 |
Age | 0.20 (.12) | .11 | −0.11 (.13) | .39 | 0.00 (.11) | 1.00 | 0.14 (.10) | .16 |
Sex | −0.03 (.12) | .79 | −0.03 (.1) | .81 | −0.06 (.10) | .57 | −0.03 (.09) | .74 |
Race | −0.007 (.13) | .95 | 0.31 (.10) | .003 | 0.06 (.10) | .55 | −0.15 (.09) | .11 |
ICS Use | −0.06 (.13) | .65 | −0.24 (.11) | .02 | 0.17 (.10) | .08 | 0.26 (.09) | .004 |
%FEV1 | −0.02 (.13) | .89 | 0.16 (.12) | .17 | −0.07 (.10) | .46 | −0.03 (.09) | .77 |
Abbreviations: ICS Use, Inhaled corticosteroids
FEV1/FVC was not associated with asthma control in the obesity-related asthma group (β = −0.03, p = .77) or in the asthma only group (β = 0.20, p = .08; Table 6). The model for asthma control accounted for more variance in the asthma only group (20%) than in the obesity-related group (5%) and the differences were significantly different (χ2 diff =11.432, p =.0007; Table 6). Lower FEV1/FVC was associated with the number of asthma symptoms endorsed in the asthma only group (β = −0.29, p = .002) but not in the obesity-related asthma group (β = −0.07, p = .48). The model accounted for more variance in the number of asthma symptoms in the asthma only group (18%) than in the obesity-related asthma group (4%) and differences were significant (χ2 diff = 16.662; p < .0001).
Table 6.
Asthma Control and FEV1/FVC
Variable | Asthma Control | # Symptoms | ||||||
---|---|---|---|---|---|---|---|---|
Obesity-related asthma group | Asthma only group | Obesity-related asthma group | Asthma only group | |||||
Model R2 | .05 | .20 | .04 | .18 | ||||
Χ2
Difference Test |
Χ2 diff=11.432; p=.0007 | Χ2 diff=16.662; p=<.0001 | ||||||
β (SE) | p-Value | β (SE) | p-Value | β (SE) | p-Value | β (SE) | p-Value | |
Study Group | 0.14 (.12) | .26 | 0.08 (.11) | .47 | −0.03 (.10) | .80 | −0.08 (.10) | .39 |
Age | 0.19 (.12) | .12 | −0.10 (.13) | .44 | −0.01 (.11) | .91 | 0.10 (.10) | .29 |
Sex | −0.03 (.12) | .82 | −0.06 (.12) | .59 | −0.05 (.10) | .64 | 0.04 (.09) | .67 |
Race | −0.003 (.13) | .98 | 0.28 (.10) | .006 | 0.07 (.10) | .48 | −0.14 (.09) | .12 |
ICS Use | −0.06 (.12) | .63 | −0.23 (.11) | .03 | 0.16 (.10) | .10 | 0.22 (.09) | .02 |
FEV1/FVC | −0.03 (.11) | .77 | 0.20 (.11) | .08 | −0.07 (.10) | .48 | −0.29 (.09) | .002 |
Abbreviations: ICS Use, Inhaled corticosteroids
Discussion
The current study extends the existing literature on children with obesity-related asthma to examine the relationship between pulmonary function, asthma control, and clinical outcomes. FEV1/FVC was lower in the obesity-related asthma group than in the asthma only group. However, FEV1/FVC was not associated with asthma control or number of asthma symptoms amongst the obesity-related asthma group. Asthma control and number of asthma symptom in the present study were based on self-report and suggest subjective interpretation of disease control. In addition, worse pulmonary function (percent predicted FEV1 and FEV1/FVC) was associated with more oral steroid bursts and hospitalizations in the obesity-related asthma group, but not in the asthma only group. Conversely, lower FEV1/FVC was associated with more asthma symptoms in asthma only group but not in the obesity-related asthma group. These results suggest that there is a discordance between symptom reporting and objective measures of disease control including oral steroid bursts among children with obesity-related asthma. Further, the results highlight the usefulness of measuring pulmonary function in children with obesity-related asthma given its associations with oral steroids and hospitalizations .
The FEV1/FVC ratio is particularly pertinent in the context of obesity-related asthma, since obesity affects both FVC and FEV1 and the mechanisms that affect these parameters in obese children are distinct from those associated with airway hyper-responsiveness in children with asthma only. One such proposed mechanism is the mechanical effect of abdominal fat displacing the diaphragm into the abdomen 34 and contributing to a loss of expiratory reserve volume 35,36. Another potential explanation is airway dysanapsis, which is the discrepancy between lung size and airway caliber 37. Airway dysanapsis leads to a normal or slightly elevated FEV1 and FVC, with a larger effect on FVC, which in turn contributes to a lower FEV1/FVC ratio, as observed in children with obesity-related asthma 24,37.
Airway dysanapsis may play a key role in connecting worse clinical asthma outcomes to worse pulmonary function in children with obesity-related asthma. Forno et al. (2017) found that airway dysanapsis was linked to severe asthma exacerbations (e.g., ER visits, hospitalizations) and the use of oral steroids. Airway dysanapsis and mechanical changes that occur in the lungs of children with obesity-related asthma may not create the same asthma symptoms that occur in children with asthma only. Obese children with early-onset asthma have a different pattern of asthma symptoms from their asthma only counterparts with more shortness of breath and less reported cough 38. It has been hypothesized that obesity and dysanapsis in asthma patients may contribute to asthma morbidity through increased anatomical or developmental airway obstruction, rather than bronchospasm or airway inflammation more routinely observed in children with asthma only 37. However, the mechanisms underlying dysanaptic growth of lungs in children still remain to be uncovered 37.
The study’s findings on pulmonary function and asthma symptom reports indicate some incongruity between these measures in children with obesity-related asthma. Our study showed that children with obesity-related asthma with lower FEV1/FVC was associated with increased likelihood of oral steroid bursts and hospitalizations in the past 12 months than compared to children with asthma-only. However, pulmonary function in the obesity-related group was not associated with asthma control or number of asthma symptoms. The difference between asthma symptom reporting in children with obesity-related asthma has been reported in the literature. There are studies that have indicated worse asthma control, greater shortness of breath, and wheezing in children with obesity-related asthma than children with asthma only 14,15,38. On the other hand, some studies have reported no relationship between asthma control or asthma symptoms and obesity in children 21,39–41. In comparison, greater concordance between symptoms and pulmonary function existed in the asthma only group as evidenced by associations between lower FEV1/FVC and the number of asthma symptoms that met criteria for poor asthma control. As noted, asthma symptoms were reported by caregivers in this study. Previous studies have demonstrated that caregivers generally underestimate their child’s asthma severity and overestimate asthma control 42. In addition, patients’ self-assessment of asthma control often does not match with the true level of asthma control 43. Researchers suggest that physicians and patients work together to assess the individual components of asthma control, which may remedy this inaccuracy and ultimately improve asthma outcomes 43.
The results of this study suggest the importance of incorporating pulmonary function in the clinical care of children with obesity-related asthma. In a study of 894 children, 36% had greater asthma severity determined by spirometry than clinical criteria alone 44. Other studies have also found higher asthma severity when lung function data are included in the assessment45. Underestimation of asthma severity can be problematic and lead to undertreatment with less prescriptions of controller medication in children with asthma 46. Given that spirometry is generally underused by physicians 47,48 and may not be feasible in the clinical setting due to lack of a spirometer, home peak flow monitoring by children with obesity-related asthma might help connect asthma symptoms with reductions in pulmonary function and may be useful in reducing the increased number of steroid bursts, as observed in our study, in children with obesity-related asthma. Children who guess their peak flow and then see how close their guess is to their actual peak flow show improvements in perceptual accuracy of airflow obstruction as well as adherence to controller medications 26.
This study has a number of limitations. First, only Black and Latino children were enrolled from hospitals in the Bronx, New York. Therefore, the study population is representative of an ethnically diverse inner-city population, which limits the generalizability of our results. Second, we included BMI and did not measure other secondary variables like percent body fat or waist circumference. BMI, while easily calculated, does not accurately reflect body fat distribution or abdominal obesity, which are critical measures in obesity-related asthma 49. Third, some of the outcome variables (e.g., healthcare utilization) were assessed through caregiver report which may be subject to recall bias. In addition, prescribed medication, asthma control and pulmonary function clinician were included as proxies for asthma severity, however clinician rated asthma severity was not collected and is a noted limitation. Furthermore, we investigated percent predicted FEV1 and FEV1/FVC as two measures of airflow obstruction, the latter being included specifically in light of the data on the effect of obesity on FVC. However, we did not examine FVC individually. Finally, the cross-sectional nature of our analyses is a major limitation as the single measurement of pulmonary function and clinical outcomes may be better assessed in a longitudinal fashion with multiple time points. Future studies should include longitudinal analyses to examine if pulmonary function predicts prospective clinical outcomes across time in children with obesity-related asthma. In addition, future analyses should be expanded to include home peak expiratory flow, which would allow daily measurement.
Conclusion
This study builds on existing evidence that multiple components of spirometry to physician assessment should be used to determine asthma control and guide clinical care in patients with obesity-related asthma. The association between low percent predicted FEV1 and low FEV1/FVC with more steroid bursts and hospitalizations shows the importance of monitoring pulmonary function to direct treatment plans in children with obesity-related asthma. This association may partially explain previous reports of increased asthma morbidity in children with obesity-related asthma. Children with obesity-related asthma and low percent predicted FEV1 and FEV1/FVC may represent an at-risk group that requires careful monitoring of lung function.
Supplementary Material
Funding/Support:
This study was funded by the American Lung Association (SB-20474-N;PI: J Feldman), the National Institute of Child and Human Development (R03HD053355; PI: J Feldman), National Heart, Blood, and Lung Institute (HL141849; PI: D Rastogi) and (HL144534; PI: D Rastogi)
Footnotes
Declaration of Interest
Disclosure Statement: The authors report no conflict of interest. No funders had any role in the design and conduct of the study.
References
- 1.Black LI BV (2018). Tables of Summary Health Statistics for U.S. Children: 2017 National Interview Survey https://www.cdc.gov/nchs/nhis/SHS/tables.htm.
- 2.Hales CM, Carroll MD, Fryar CD & Ogden CL Prevalence of Obesity Among Adults and Youth: United States, 2015–2016. NCHS Data Brief, 1–8 (2017). [PubMed] [Google Scholar]
- 3.Peters U, Dixon AE & Forno E Obesity and asthma. J Allergy Clin Immunol 141, 1169–1179 (2018). 10.1016/j.jaci.2018.02.004 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Sybilski AJ et al. Obesity--a risk factor for asthma, but not for atopic dermatitis, allergic rhinitis and sensitization. Public Health Nutr 18, 530–536 (2015). 10.1017/s1368980014000676 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Azizpour Y, Delpisheh A, Montazeri Z, Sayehmiri K & Darabi B Effect of childhood BMI on asthma: a systematic review and meta-analysis of case-control studies. BMC Pediatr 18, 143 (2018). 10.1186/s12887-018-1093-z [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Lang JE et al. Effects of age, sex, race/ethnicity, and allergy status in obesity-related pediatric asthma. Pediatr Pulmonol 54, 1684–1693 (2019). 10.1002/ppul.24470 [DOI] [PubMed] [Google Scholar]
- 7.Malden S et al. Obesity in young children and its relationship with diagnosis of asthma, vitamin D deficiency, iron deficiency, specific allergies and flat-footedness: A systematic review and meta-analysis. Obes Rev 22, e13129 (2021). 10.1111/obr.13129 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Lang JE et al. Being Overweight or Obese and the Development of Asthma. Pediatrics 142 (2018). 10.1542/peds.2018-2119 [DOI] [PubMed] [Google Scholar]
- 9.Contreras ZA et al. Does early onset asthma increase childhood obesity risk? A pooled analysis of 16 European cohorts. Eur Respir J 52 (2018). 10.1183/13993003.00504-2018 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Chen Z et al. Effects of Childhood Asthma on the Development of Obesity among School-aged Children. American Journal of Respiratory and Critical Care Medicine 195, 1181–1188 (2017). 10.1164/rccm.201608-1691OC [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Zhang Y et al. The Dynamic Relationship Between Asthma and Obesity in Schoolchildren. Am J Epidemiol 189, 583–591 (2020). 10.1093/aje/kwz257 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Black MH, Zhou H, Takayanagi M, Jacobsen SJ & Koebnick C Increased asthma risk and asthma-related health care complications associated with childhood obesity. Am J Epidemiol 178, 1120–1128 (2013). 10.1093/aje/kwt093 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Luder E, Melnik TA & DiMaio M Association of being overweight with greater asthma symptoms in inner city black and Hispanic children. J Pediatr 132, 699–703 (1998). 10.1016/s0022-3476(98)70363-4 [DOI] [PubMed] [Google Scholar]
- 14.Quinto KB et al. The association of obesity and asthma severity and control in children. J Allergy Clin Immunol 128, 964–969 (2011). 10.1016/j.jaci.2011.06.031 [DOI] [PubMed] [Google Scholar]
- 15.Belamarich PF et al. Do obese inner-city children with asthma have more symptoms than nonobese children with asthma? Pediatrics 106, 1436–1441 (2000). 10.1542/peds.106.6.1436 [DOI] [PubMed] [Google Scholar]
- 16.Black MH, Smith N, Porter AH, Jacobsen SJ & Koebnick C Higher prevalence of obesity among children with asthma. Obesity (Silver Spring) 20, 1041–1047 (2012). 10.1038/oby.2012.5 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Gross E, Lee DS, Hotz A, Ngo KC & Rastogi D Impact of obesity on asthma morbidity during a hospitalization. Hospital pediatrics 8, 538–546 (2018). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Forno E et al. Decreased response to inhaled steroids in overweight and obese asthmatic children. J Allergy Clin Immunol 127, 741–749 (2011). 10.1016/j.jaci.2010.12.010 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.McGarry ME et al. Obesity and bronchodilator response in black and Hispanic children and adolescents with asthma. Chest 147, 1591–1598 (2015). 10.1378/chest.14-2689 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Rastogi D et al. Obesity-associated asthma in children: a distinct entity. Chest 141, 895–905 (2012). 10.1378/chest.11-0930 [DOI] [PubMed] [Google Scholar]
- 21.Tantisira KG, Litonjua AA, Weiss ST, Fuhlbrigge AL & Childhood Asthma Management Program Research, G. Association of body mass with pulmonary function in the Childhood Asthma Management Program (CAMP). Thorax 58, 1036–1041 (2003). 10.1136/thorax.58.12.1036 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Huang F et al. Adipokines, asymmetrical dimethylarginine, and pulmonary function in adolescents with asthma and obesity. J Asthma 54, 153–161 (2017). 10.1080/02770903.2016.1200611 [DOI] [PubMed] [Google Scholar]
- 23.Forno E, Han YY, Mullen J & Celedon JC Overweight, Obesity, and Lung Function in Children and Adults-A Meta-analysis. J Allergy Clin Immunol Pract 6, 570–581 e510 (2018). 10.1016/j.jaip.2017.07.010 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Jones MH et al. Asthma and Obesity in Children Are Independently Associated with Airway Dysanapsis. Front Pediatr 5, 270 (2017). 10.3389/fped.2017.00270 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Strunk RC et al. Airway Obstruction Worsens in Young Adults with Asthma Who Become Obese. J Allergy Clin Immunol Pract 3, 765–771 e762 (2015). 10.1016/j.jaip.2015.05.009 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Feldman JM et al. Prediction of peak flow values followed by feedback improves perception of lung function and adherence to inhaled corticosteroids in children with asthma. Thorax 67, 1040 (2012). 10.1136/thoraxjnl-2012-201789 [DOI] [PubMed] [Google Scholar]
- 27.Feldman JM et al. Perception of pulmonary function and asthma control: the differential role of child versus caregiver anxiety and depression. J Pediatr Psychol 38, 1091–1100 (2013). 10.1093/jpepsy/jst052 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.NHLBI. Expert Panel Report 3: Guidelines for the Diagnosis and Management of Asthma. (National Heart, Lung, Blood Institute, 2007). [Google Scholar]
- 29.ATS. Standardization of Spirometry, 1994 Update. . Am J Respir Crit Care Med 152, 1107–1136 (1995). 10.1164/ajrccm.152.3.7663792 [DOI] [PubMed] [Google Scholar]
- 30.Hankinson JL, Odencrantz JR & Fedan KB Spirometric reference values from a sample of the general U.S. population. Am J Respir Crit Care Med 159, 179–187 (1999). 10.1164/ajrccm.159.1.9712108 [DOI] [PubMed] [Google Scholar]
- 31.Kline RB Principles and practice of structural equation modeling Third edn, (Guilford Press, 2011). [Google Scholar]
- 32.Kline RB Principles and practice of structural equation modeling (Guilford Publications, 2015). [Google Scholar]
- 33.Muthen LKM a. B. O. MPLUS User’s Guide (Muthen & Muthen, 1998–2017; ). [Google Scholar]
- 34.Koenig SM Pulmonary complications of obesity. Am J Med Sci 321, 249–279 (2001). 10.1097/00000441-200104000-00006 [DOI] [PubMed] [Google Scholar]
- 35.Rastogi D, Bhalani K, Hall CB & Isasi CR Association of pulmonary function with adiposity and metabolic abnormalities in urban minority adolescents. Ann Am Thorac Soc 11, 744–752 (2014). 10.1513/AnnalsATS.201311-403OC [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36.Rastogi D et al. Inflammation, metabolic dysregulation, and pulmonary function among obese urban adolescents with asthma. Am J Respir Crit Care Med 191, 149–160 (2015). 10.1164/rccm.201409-1587OC [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Forno E et al. Obesity and Airway Dysanapsis in Children with and without Asthma. Am J Respir Crit Care Med 195, 314–323 (2017). 10.1164/rccm.201605-1039OC [DOI] [PMC free article] [PubMed] [Google Scholar]
- 38.Lang JE, Hossain MJ & Lima JJ Overweight children report qualitatively distinct asthma symptoms: Analysis of validated symptom measures. Journal of Allergy and Clinical Immunology 135, 886–893.e883 (2015). 10.1016/j.jaci.2014.08.029 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 39.Sah PK et al. Poor asthma control in obese children may be overestimated because of enhanced perception of dyspnea. J Allergy Clin Immunol Pract 1, 39–45 (2013). 10.1016/j.jaip.2012.10.006 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40.Evans EW, Koinis-Mitchell D, Kopel SJ & Jelalian E Lung Function, Dietary Intake, and Weight Status in Children with Persistent Asthma from Low-Income, Urban Communities. Nutrients 11 (2019). 10.3390/nu11122943 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 41.Ahmadizar F et al. Childhood obesity in relation to poor asthma control and exacerbation: a meta-analysis. Eur Respir J 48, 1063–1073 (2016). 10.1183/13993003.00766-2016 [DOI] [PubMed] [Google Scholar]
- 42.Silva CM & Barros L Asthma knowledge, subjective assessment of severity and symptom perception in parents of children with asthma. Journal of Asthma 50, 1002–1009 (2013). [DOI] [PubMed] [Google Scholar]
- 43.Fuhlbrigge A et al. Physician–patient concordance in the assessment of asthma control. The Journal of Allergy and Clinical Immunology: In Practice (2021). 10.1016/j.jaip.2021.03.056 [DOI] [PubMed] [Google Scholar]
- 44.Schifano ED, Hollenbach JP & Cloutier MM Mismatch between asthma symptoms and spirometry: implications for managing asthma in children. The Journal of pediatrics 165, 997–1002 (2014). [DOI] [PubMed] [Google Scholar]
- 45.Peer K et al. Developing and evaluating a pediatric asthma severity computable phenotype derived from electronic health records. J Allergy Clin Immunol (2020). 10.1016/j.jaci.2020.11.045 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 46.Halterman JS et al. Providers Underestimate Symptom Severity Among Urban Children With Asthma. Archives of Pediatrics & Adolescent Medicine 156, 141–146 (2002). 10.1001/archpedi.156.2.141 [DOI] [PubMed] [Google Scholar]
- 47.Dombkowski KJ, Hassan F, Wasilevich EA & Clark SJ Spirometry Use Among Pediatric Primary Care Physicians. Pediatrics 126, 682 (2010). 10.1542/peds.2010-0362 [DOI] [PubMed] [Google Scholar]
- 48.O’Dowd LC, Fife D, Tenhave T & Panettieri RA Attitudes of physicians toward objective measures of airway function in asthma. The American Journal of Medicine 114, 391–396 (2003). 10.1016/S0002-9343(03)00007-X [DOI] [PubMed] [Google Scholar]
- 49.Barnes PJ, Szefler SJ, Reddel HK & Chipps BE Symptoms and perception of airway obstruction in asthmatic patients: Clinical implications for use of reliever medications. Journal of Allergy and Clinical Immunology 144, 1180–1186 (2019). 10.1016/j.jaci.2019.06.040 [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.