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Waist-to-Height Ratio are Related to Exercise-Induced Bronchoconstriction in Adolescents.


Exercise-induced bronchospasm (EIB) is characterized as a transient obstruction in the lower airways after performing intense physical activities that last 6 to 8 min (21). It is more frequent in individuals with a history of asthma and/or allergic rhinitis (1). In addition, the association of asthma and obesity has shown greater intensity in the drop in lung function and longer recovery time after exercise when compared to non-obese (11,12). Therefore, in the management of EIB, this combination is a concern since both diseases show an increase in prevalence and simultaneously in several individuals (13).

Changes in the population's lifestyle, such as longer screen time and increased consumption of processed foods are environmental factors implicated in the genesis of asthma and obesity (14). Added to this is the use of new technologies and smartphones that increase sedentary behavior among pediatric population (6). Singly or collectively, they are factors that lead to changes in body composition and increased abdominal adiposity, which is related to the mechanical concerns that restrict diaphragmatic expansion and the appearance of asthma attacks. In addition, the significant reduction in central obesity may favor the improvement of thoracic mechanics, increase in vital capacity and the volume of expiratory reserve (18).

During intense exercise, there is an increase in catecholamine concentrations due to the stimulation of the sympathetic system, which is a factor that promotes physiological bronchodilation during exercise. Thus, in general, the EIB occurs between the 5th and 10th-min after exercise and reverses spontaneously, restoring lung function to pre-exercise levels between 30 and 60 min (19). Laboratory diagnosis of EIB is performed by spirometry before and after standardized physical exercise, based on the drop in forced expiratory volume in the first second (FE[V.sub.1]) in relation to pre-exercise (4,15).

However, changes in values in waist circumference, waist-to-height ratio, and fat mass have not been evaluated as risk factors for the triggering of EIB, as well as their impact on intensity and the decrease in lung function. Therefore, the purpose of this study was to verify the frequency of EIB in asthmatic and non-asthmatic adolescents, as well as to identify the anthropometric and body composition variables associated with EIB.



Cross-sectional study with 100 adolescents of both sexes, aged between 10 and 17 yrs, obese and non-obese, asthmatic, and non-asthmatic, divided according to the presence (EIB+) or absence (EIB-) of EIB. All subjects signed the consent form, and the parents or the guardians signed the consent form that was approved by the Ethics Committee of the Federal University of Parana (protocol 2460.067/2011 -03).


Body mass was assessed on a digital scale with a maximum capacity of 150 kg and a resolution of 100 grams. Height was assessed on a stadiometer with a resolution of 0.1 cm (8). The body mass index (BMI) was calculated and the BMI z score (BMI-z) was calculated using the WHO AnthroPlus[R] program. Subjects were divided into three groups according to BMI-z in: (a) eutrophic (>-2 and <+1); (b) overweight (>+1 and <+2); and (c) obese (>+2).

Waist circumference (WC) was measured with a flexible and inextensible tape with an accuracy of 0.1 cm. The waist-to-height ratio (WHtR) was obtained by the ratio between WC (cm) and height (cm).

Body composition was assessed by the bioelectrical impedance method (BIA) using the tetrapolar Maltron[R] device model BF906 (Essex, UK). The procedure was performed in the fasting state of 10 to 12 hrs in the morning period in the supine position. Resistance values were obtained and fat free mass (FFM) and fat mass (FM) were calculated using the equation validated in obese adolescents by Lopes et al. (9).

The presence or absence of a clinical history of bronchial asthma was performed by medical interview and by the subjects' clinical history in accordance with the International Study of Asthma and Allergies Childhood questionnaire (22).

Cardiorespiratory fitness was assessed on a treadmill, using the ramp protocol, with progressive load intensity according to the age group. Maximum heart rate (HR max) was measured using a HR monitor (Polar[R]). The Medgraphics VO2000[R] gas analyzer was used to assess the peak oxygen consumption (V[O.sub.2peak]). The respiratory exchange ratio (RER) was calculated directly every 15 sec of data collection. The test was considered maximum when two of the following three criteria were met: (a) exhaustion or inability to maintain the required speed; (b) RER [greater than or equal to]1.0; and (c) reached the HR max predicted by the formula: 208 - 07 * (age).

Pulmonary function was measured by the Microlab 2000[R] spirometer in a sitting position and using a nose clip. The variables measured were forced vital capacity (FVC) and forced expiratory volume in the first second (FE[V.sub.1]), in liters. Three spirometric maneuvers were performed and the one with the highest FE[V.sub.1] and FVC values was selected. The percentages of the predicted FE[V.sub.1], FVC, and the FE[V.sub.1]/FVC ratio values for age and sex were calculated according to Polgar and Promadhat (16).

The exercise test for EIB assessment was performed on an ergometric treadmill using the protocol that consists of walking/running for 8 min at intensity greater than 85% of HR max, which was obtained in a previous maximal exercise test. The incline of the treadmill was 10% and the speed was estimated by the equation proposed by Eggleston and Guerrant and described by Sano et al. (17). After the bronchial provocation test, FE[V.sub.1] was measured at 5, 10, and 15 min post-exercise. The FE[V.sub.1] percentage in relation to the pre-exercise value was calculated using the equation: % FE[V.sub.1] = [(FE[V.sub.1] pre-exercise - FE[V.sub.1] post-exercise)/FE[V.sub.1] pre-exercise] * 100. The EIB was considered positive for a reduction in FE[V.sub.1] [greater than or equal to]10% to the pre-exercise value. The EIB intensity was calculated by the maximum percentage fall in FE[V.sub.1] ([MFFEV.sub.1]) using the calculation of the percentage decrease in FE[V.sub.1] post-exercise in relation to the pre-exercise value, considering the biggest drop and the Area Above the Curve (AAC) was calculated using the trapezoidal method.

Statistical Analyses

The Kolmogorov Smirnov test was used to analyze normality distribution. For the comparison between groups, the independent Student's t test and the Mann-Whitney U test were used. The Chi-Square test was used to assess the proportions between groups. Spearman's correlation coefficient was used to verify the correlation between variables, with regards to: (a) 0.10 to 0.39 as weak; (b) 0.40 to 0.69 as moderate; and (c) 0.70 to 1.00 as strong. The level of statistical significance adopted was P[less than or equal to]0.05 and the SPSS statistical package (version 24.0) was used to perform the tests.


The study included 100 adolescents (56 girls and 44 boys) 10 to 17 yrs of age. They were divided into two groups according to the presence or absence of EIB. Table 1 shows the variables of anthropometric and body composition. The EIB+ Group had a lower mean age (P<0.01) and higher means of WHtR (P=0.05) than the EIB- Group.

The cardiorespiratory fitness and pulmonary function at rest and after the exercise challenge test are shown in Table 2. The EIB+ Group showed lower values for the FE[V.sub.1] variables, both in liters (P<0.01), in the percentage predicted for height (P<0.01), and in the FE[V.sub.1]/FVC ratio (P=0.04) when compared with the EIB- Group. The variables of FVC were similar between the Groups. In addition, FE[V.sub.1] values at 5, 10, and 15 min, as well as the area above the curve (AA[C.sub.0-15]) obtained higher fall values in the EIB+ Group when compared with the EIB-Group (P<0.01).

Asthma was diagnosed in 19% of the sample and EIB in 18%, with a higher proportion in asthmatics (57.9%; P<0.00) than non-asthmatics (8.6%). Eighteen adolescents (8 boys and 10 girls) were classified as EIB+ and 82 presented EIB- (36 boys and 46 girls). There was no significant difference in the proportion of sex ([chi square]=0.002; P=0.97) between the EIB Groups. In addition, there were no differences in the frequency of asthma and EIB according to the degree of adiposity ([chi square]=5.168; P=0.07; [chi square]=0.818; P=0.66, respectively) (Figure 1).
Figure 1. Frequency of Asthma and EIB According to the Degree of
Adiposity. EIB+ = Presence of Exercise-Induced Bronchoconscriction;
EIB- = Absence of EIB

                 Eutrophic   Overweight   Obese

Asthmatic        10.5        52.6         36.8
Non-asthmatics   27.2        27.2         45.7
EIB+             16.7        38.9         44.4
EIB-             25.6        30.5         43.9

Note: Table made from bar graph.

Table 3 shows the correlations between anthropometric body composition, cardiorespiratory fitness, and pulmonary function at rest and after the exercise challenge test. Moderate and direct correlations were found between FFM and FE[V.sub.1] (rho=0.523, P<0.001) and FVC (rho=0.630, P<0.001) and weak and inverse correlations with FEWFVC (rho=-0.374, P<0.001). In the anthropometric variables, weak and inverse correlations were found between WC and FE[V.sub.1]/FVC (rho=-0.226, P=0.024), FE[V.sub.1]10min (rho=-0.231, P=0.023), FE[V.sub.1]15min (rho=-0.322, P=0.001) and direct with AA[C.sub.0-15] (rho=0.232, P=0.020). In addition, weak and inverse correlations between the WHtR and FE[V.sub.1]10min (rho=-0.245, P=0.015), FE[V.sub.1]15min (rho=-0.338, P=0.001), [QMVEF.sub.1] (r=-0.208, P=0.038) and direct with AA[C.sub.0-15] (rho= 0.243, P=0.015). In addition, moderate and direct correlations were found between V[O.sub.2peak] and FE[V.sub.1] (rho=0.458, P<0.01), FVC (rho=0.503, P<0.001) and weak and inverse with FE[V.sub.1]/FVC (rho=-0.269, P=0.007).


The purpose of this study was to verify the frequency of EIB in asthmatic and non-asthmatic overweight adolescents as well as to identify associated factors since EIB restricts diaphragmatic expansion due to increased abdominal adiposity that also limits exercise. The diagnosis of asthma (1) and obesity (11,12) are risk factors for its onset. Therefore, in the management of EIB, this combination is of concern due to the increased prevalence of these diseases (13).

The pulmonary function variables showed lower values in the EIB+ Group compared to the EIB- Group, except for FVC, which was similar between the two Groups. Results that are divergent from those found in studies with obese and asthmatic adolescents did not find significant differences in FE[V.sub.1] (11,12). Regarding the results of the physical exercise test to assess the EIB, the individuals in the EIB+ Group showed greater falls in FE[V.sub.1] in the 5, 10, and 15 min, in the maximum fall in FE[V.sub.1], as well as in the area above the curve that reinforced the expected differences between Groups.

In addition, some studies have shown that individuals with EIB+ participate less in physical activities (2,3) and, consequently, have lower values of V[O.sub.2peak]. In this study, the EIB+ Group did not present lower values of cardiorespiratory fitness, suggesting that there may be no differences in the level of physical activity of those evaluated. Asthmatic individuals who control the disease well tend not to have the same exercise limitations as their non-asthmatic peers, which suggests that those with EIB + do the proper management with warm-up prior to physical exercise, as well as the use of beta-2 agonists that inhibit EIB (20). However, a recent systematic review suggests there is insufficient evidence that physical training contributes to a reduction in the frequency and/or severity of EIB in young asthmatics (10).

In the present study, the EIB+ Group had a higher proportion of history of asthma (57.9%; P<0.00) when compared to the EIB- Group, which is in agreement with the results by Lopes et al. (12) who found the proportion of 50% of EIB in obese asthmatic individuals in Brazil. A justification for the relationship between EIB and asthma is indicated in the increase of the production of inflammatory mediators, given the decrease in the production of protective lipid mediators and the infiltration of the airways with eosinophils and mast cells that are the main factors established for EIB (7).

Regarding overweight, no statistically significant differences were found in the proportion between the EIB+ Group and the EIB- Group with the BMI categories diverging from what was expected that the greater proportion of individuals overweight would be diagnosed with positive EIB. In addition, the individuals characterized as EIB+ had a lower mean age (yrs) when compared to the EIB- Group, which is corroborates the findings by Vilozni et al. (23) who reported that younger individuals trigger EIB due mainly to their smaller airway caliber.

No differences were found between WC values and height between the Groups. Two variables related to EIB, since the increase in abdominal adiposity is related to the restriction of diaphragmatic expansion (5) and the height with the lung size of the individual. However, when the relationship between WC and height was performed, the mean of this variable was higher in the EIB+ Group. In addition, weak and inverse correlations were found between the WHtR and FE[V.sub.1] variables at 10 and 15 min, at the maximum drop in FE[V.sub.1] and in the area above the curve (AA[C.sub.0-15]). As well as, there were weak and inverse correlations between the WC and FE[V.sub.1] variables at 10 and 15 min and in the area above the curve (AA[C.sub.0-15]).


The findings indicate that WHtR was shown to be the best anthropometric indicator in the evaluation of EIB, since greater abdominal adiposity is a mechanical and inflammatory factor that can cause impairment of pulmonary function after intense physical exercise in adolescents. Also, the data demonstrate that anthropometry can be an important tool for the physical education teacher, given that it is simple and easy to apply. It can provide important information to propose effective interventions to combat obesity and associated risk factors.


The authors are grateful to the Brazilian funding agencies CAPES and CNPq for scholarships. The authors give thanks for the financial support from the Brazilian funding agency Fundagao Araucaria (Edital 05/2011) and PR/SESA-PR/CNPq/MS-Decit (Edital CP 01/2016). JM was supported by the following grants: FCT: SFRH/BSAB/142983/2018 and UID/DTP/00617/2019 as well as Santander University Program (2018).

Address for correspondence: Maiara C Tadiotto, MD, Department of Physical Education, Federal University of Parana, Rua Cel. Francisco H. dos Santos, 100. CEP 81531-980, Jardim das Americas, Curitiba, Parana, Brazil, Email:


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Maiara C. Tadiotto (1), Wendell A. Lopes (2), Cassio L. M. Consentino (1), Larissa R. Silva (3), Patricia R. P. Corrazza (1), Francisco J. Menezes-Junior (1), Nelson A. Rosario-Filho (1), Rosana B. Radominski (1), Jorge Mota (4), Neiva Leite (1,4)

(1) Federal University of Parana, Curitiba, Brazil, (2) University of Maringa, Maringa, Brazil, (3) University of Western Parana, Marechal Candido Rondon, Brazil, University of Porto, Porto, Portugal

Tadiotto MC, Lopes WA, Consentino CLM, Silva LR, Corazza PRP, Menezes-Junior FJ, Rosario-Filho NA, Radominski RB, Mota J, Leite N. Waist-to-Height Ratio are Related to Exercise-Induced Bronchoconstriction in Adolescents. JEPonline 2020;23(4): 38-48.
Table 1. Anthropometric and Body Composition Variables in EIB+ and EIB-

Variables                 EIB+                 EIB-
                          (n=18)               (n=82)

Age (yrs)                 13.7 [+ or -] 1.7    15.0 [+ or -] 1.2
Height (m)                 1.71 [+ or -] 0.2    1.78 [+ or -] 0.2
BM (kg)                   71.9 [+ or -] 15.2   74.3 [+ or -] 14.6
BMI (kg*[m.sup.-2]) (*)   27.4 [+ or -] 5.7    26.7 [+ or -] 4.6
BMI-z (z score)            2.4 [+ or -] 1.8     1.8 [+ or -] 1.2
WC (cm)                   88.8 [+ or -] 14.8   83.4 [+ or -] 11.6
WtHR                       0.5 [+ or -] 0.1     0.5 [+ or -] 0.1
FM (%)                    35.0 [+ or -] 9.3    35.1 [+ or -] 10.2
FFM (%)                   65.0 [+ or -] 9.3    64.9 [+ or -] 10.2
FM (kg)                   25.9 [+ or -] 10.9   26.6 [+ or -] 10.7
FFM (kg)                  44.2 [+ or -] 7.6    44.8 [+ or -] 8.0

Variables                 t or U    P-value

Age (yrs)                 423.0     0.00
Height (m)                622.5     0.23
BM (kg)                   637.0     0.36
BMI (kg*[m.sup.-2]) (*)     0.524   0.60
BMI-z (z score)           615.5     0.27
WC (cm)                   585.5     0.17
WtHR                      523.0     0.05
FM (%)                    732.0     0.95
FFM (%)                   732.0     0.95
FM (kg)                    -0.262   0.79
FFM (kg)                  710.0     0.80

EIB+ = Presence of Exercise-Induced Bronchoconstriction, EIB- = Absence
of Exercise-Induced Bronchoconstriction, BMI = Body Mass Index, BMI-z =
Body Mass Index z-score, WC = Waist Circumference; WtHR =
Waist-to-Height Ratio, FM = Fat Mass, FFM = Fat Free Mass, (*) test t
student for independent samples

Table 2. Cardiorespiratory Fitness, Pulmonary Function at Rest and
After Exercise Challenge Test in EIB+ and EIB- Groups.


V[O.sub.2peak] (L*[min.sup.-1])     2.62 [+ or -] 0.53
V[O.sub.2peak]                     37.23 [+ or -] 8.36
FE[V.sub.1] ([L.sup.-1])            2.88 [+ or -] 0.68
FE[V.sub.1] (%predict) (*)         95.10 [+ or -] 13.95
FVC ([L.sup.-1])                    3.53 [+ or -] 0.61
FVC (%predict) (*)                101.97 [+ or -] 14.41
FE[V.sub.1]/FVC (%) (*)             0.84 [+ or -] 0.05
FE[V.sub.1] 5min (%)              -14.42 [+ or -] 12.89
FE[V.sub.1] 10min (%)             -12.82 [+ or -] 10.46
FE[V.sub.1] 15min (%)              -9.34 [+ or -] 11.95
[MFFEV.sub.1] (%)                 -16.51 [+ or -] 11.94
[AAC.sub.0-15] (%.min)            229.58 [+ or -] 220.79

                                 EIB-                   t or U   P-value

V[O.sub.2peak] (L*[min.sup.-1])    2.69 [+ or -] 0.62   702.5    0.75
V[O.sub.2peak]                    36.67 [+ or -] 7.21   732.0    0.95
FE[V.sub.1] ([L.sup.-1])           3.45 [+ or -] 0.65   434.5    0.00
FE[V.sub.1] (%predict) (*)       106.79 [+ or -] 13.10   -3.390  0.00
FVC ([L.sup.-1])                   4.02 [+ or -] 0.81   604.0    0.22
FVC (%predict) (*)               107.07 [+ or -] 14.35   -1.363  0.17
FE[V.sub.1]/FVC (%) (*)            0.88 [+ or -] 0.07    -2.072  0.04
FE[V.sub.1] 5min (%)               0.17 [+ or -] 4.49    66.0    0.00
FE[V.sub.1] 10min (%)              1.06 [+ or -] 4.52    25.0    0.00
FE[V.sub.1] 15min (%)              1.47 [+ or -] 4.78   153.5    0.00
[MFFEV.sub.1] (%)                 -0.92 [+ or -] 4.42     3.5    0.00
[AAC.sub.0-15] (%.min)           -22.93 [+ or -] 85.24   20.0    0.00

EIB+ = Presence of Exercise-Induced Bronchoconscriction; EIB- = Absence
of Exercise-Induced Bronchoconscriction; V[O.sub.2peak] = Peak Oxygen
Uptake; FE[V.sub.1] = Forced Expiratory Volume in the First Second; FVC
= Forced Vital Capacity; [MFFEV.sub.1] = Maximum Fall in FE[V.sub.1];
[AAC.sub.0-15] = Area Above the Curve between 0 to 15 min after
Exercise Challenge Test; (*) Student t test for independent samples

Table 3. Correlation of Anthropometric and Body Composition with
Pulmonary Function at Rest and After Exercise Challenge Test.

Variables                       FE[V.sub.1]   FVC        FE[V.sub.1]/FVC

BMI (kg*[m.sup.-2])              0.071         0.064     -0.150
BMI-z (z score)                  0.016         0.014     -0.192
WC (cm)                          0.069         0.122     -0.226*
WtHR                            -0.139        -0.106     -0.126
FM (%)                          -0.181        -0.254*     0.063
FFM (%)                          0.181         0.254*    -0.063
FM (kg)                          0.097         0.060     -0.111
FFM (kg)                         0.523**       0.630**   -0.374**
V[O.sub.2peak]                   0.458**       0.503**   -0.269**
V[O.sub.2peak]                   0.190         0.186     -0.023

Variables                       FE[V.sub.1]5min   FE[V.sub.1]10min

BMI (kg*[m.sup.-2])              0.001            -0.143
BMI-z (z score)                 -0.073            -0.207*
WC (cm)                         -0.125            -0.231*
WtHR                            -0.131            -0.245*
FM (%)                           0.088            -0.020
FFM (%)                         -0.088             0.020
FM (kg)                          0.068            -0.054
FFM (kg)                        -0.143            -0.169
V[O.sub.2peak]                  -0.108            -0.133
V[O.sub.2peak]                  -0.063            -0.024

Variables                      FE[V.sub.1]15min  [MFFEV.sub.1]   AAC0-15

BMI (kg*[m.sup.-2])            -0.210*           -0.055           0.115
BMI-z (z score)                -0.277*           -0.128           0.178
WC (cm)                        -0.322**          -0.180           0.232*
WtHR                           -0.338**          -0.208*          0.243*
FM (%)                         -0.125             0.001           0.012
FFM (%)                         0.125            -0.001          -0.012
FM (kg)                        -0.153             0.003           0.055
FFM (kg)                        0.163            -0.108           0.179
V[O.sub.2peak]                 -0.133            -0.066           0.122
V[O.sub.2peak]                  0.016            -0.020          0.000

BMI = Body Mass Index, BMI-z = Body Mass Index z-score, WC = Waist
Circumference; WtHR = Waist-to-Height Ratio, FM = Fat Mass, FFM = Fat
Free Mass, V[O.sub.2peak] = Peak Oxygen Uptake, FE[V.sub.1] = Forced
Expiratory Volume in the First Second, FVC = Forced Vital Capacity,
[MFFEV.sub.1] = Maximum Fall in FE[V.sub.1], AA[C.sub.0-15] = Area
above the Curve between 0 to 15 min after Exercise Challenge Test.
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Author:Tadiotto, Maiara C.; Lopes, Wendell A.; Consentino, Cassio L. M.; Silva, Larissa R.; Corrazza, Patri
Publication:Journal of Exercise Physiology Online
Geographic Code:3BRAZ
Date:Aug 1, 2020
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