Reduced exercise capacity for muscle mass in adolescents living with
obesity
Juliano Colapelle1, Julie
St-Pierre2, Julius Erdstein3, Larry
C. Lands4
1McGill University Experimental Medicine - Montréal
(QC) (Canada)
2McGill University Health Centre, General Pediatrics,
Maison de Santé Prévention Clinique 180 - Montréal (QC) (Canada)
3McGill University Health Centre Adolescent Medicine -
Montréal (QC) (Canada)
4McGill University Health Centre Pediatric Respiratory
Medicine - Montréal (QC) (Canada)
Corresponding author: Larry C. Lands, email:
larry.lands@mcgill.ca
Abstract
Background
Adolescents living with obesity (AlwO) can have limited exercise
capacity. Exercise capacity can be predicted by a 2-factor model
comprising lung function and leg muscle function, but no study has
looked at cycling leg muscle function and its contribution to cycling
exercise capacity in AlwO.
Methods
22 nonobese adolescents and 22 AlwO (BMI>95 percentile)
were studied. Anthropometry, body composition (DEXA), spirometry, 30-sec
isokinetic work capacity, and maximal exercise (cycle ergometry) were
measured.
Results
AlwO had greater lean leg mass (LLM) (14.8±4.1 vs 21.0±4.3 kg, Con vs
AlwO p<0.001). Lung function did not differ, although
FEV1 trended higher in AlwO (101.0±13.1 vs 107.9±12.7
percent predicted, p=0.08). Leg 30-second work output did not differ in
absolute terms or per allometrically scaled LLM.
Peak oxygen consumption did not differ between the groups in absolute
terms or as percent predicted values (78.5±15.4 vs 82.1±16.5 percent
predicted), but was lower in AlwO when expressed per scaled kg of LLM.
Peak oxygen consumption related to both lung function and 30-second work
capacity, with no observed group effect. 30-second leg work capacity
related to the scaled muscle mass, with a small group effect. There was
some correlation between leg work capacity and time spent in moderate to
vigorous physical activity in AlwO (rs=0.39, p=0.07).
Conclusion
AlwO have larger LLM and preserved exercise capacity, when expressed as
percentage of predicted, but not per allometrically scaled LLM.
Increasing time spent in moderate to vigorous activity may benefit AlwO.
Shared abstract
Adolescents living with obesity have reduced exercise capacity when
scaled per LLM. They may benefit from increased time spent in moderate
to vigorous activity.
Adolescent obesity rates continue to rise worldwide (1, 2). Obesity
negatively impacts physical fitness (3), a predictor of current and
future health (4, 5). Further, physical fitness is best assessed using
maximal effort tests such as progressive exercise testing by cycle
ergometry with gas exchange to determine the peak oxygen consumption
(6).
Maximal exercise ability can be determined by a combination of lung
function and leg muscle function (7, 8). In turn, leg muscle function is
dependent mostly upon lean leg mass (LLM), and to a lesser extent, the
amount of time spent in moderate to vigorous activity (MVPA). Obesity
can adversely affect lung function through expiratory flow limitation
leading to dynamic hyperinflation, excessive ventilation, and dyspnea
(9). While many adolescents living with obesity (AlwO) have increased
LLM and force (10-14), they may also spend less time in MVPA or more
time in sedentary activity. This may decrease the quality of the muscle,
such as aerobic capacity.
The contribution of leg muscular function to exercise capacity has had
little study in AlwO. Long jump distance correlated with maximal cycling
exercise capacity (15). However, LLM was not assessed and this explosive
power manoeuvre is quite different than the activity done during
cycling. Isokinetic knee extensor strength was higher in obese male
adolescents compared to nonobese adolescents (16). Knee extensor is only
one muscle group that participates in the cycling motion. Further, knee
extensor strength was less when expressed per kg of thigh muscle mass.
Others (11) have found that force was maintained when expressed per kg
of muscle mass. Many of the differences between studies are likely due
to a scaling issue. Normalization should result in the normalized
outcome being unrelated to the normalization factor. When combining
groups with different anthropometry, normalization by total body mass or
even total muscle mass typically does not result in normalization (17,
18). Additionally, whole body mass may not accurately reflect LLM (17).
Direct measurement of leg muscle function during a full cycling motion
can better represent the contribution of leg muscle function to exercise
capacity. This can be done using short term isokinetic cycling, where
the cycling speed is fixed and work output directly measured. Total work
achieved over a 30-second bout of isokinetic cycling directly relates to
maximal cycle ergometry exercise capacity (7, 8). When 30-second
isokinetic work output is combined with lung function
(FEV1), maximal oxygen consumption can be reasonably
predicted.
The present study aimed to look at the factors contributing to exercise
limitation in AlwO, including anthropometric measures, time spent in
MVPA and sedentary activity, lung function, isokinetic leg muscle
function, and maximal exercise capacity by cycle ergometry. We
hypothesized that exercise capacity in the AlwO would be mildly reduced
due to decreased time spent in MVPA and/or more time spent being
sedentary.
Methods
Ethics statement: The study was approved by the Pediatric Research
Ethics Committee of the MUHC (Study no. 2022-8098).
Participants: AlwO (males and females, 12-18 years of age)
(BMI>95 percentile) (19) were recruited from the Montreal
Children’s Hospital-McGill University Health Centre (MUHC) Adolescent
Obesity Clinic and La Maison de Santé Prévention Adolescent Obesity
Clinic. Non-obese, otherwise healthy, adolescents were also recruited
from both clinics, as well as by friends and family of the AlwO.
Procedures
In advance of the study visit, participants were asked to not eat or
exercise two hours prior to the visit (20). Participants were also told
to limit their consumption of alcohol and caffeine 12 hours prior to the
visit to ensure a state of normal hydration. Moreover, it was ensured
that participants did not consume calcium pills 24 hours prior to
testing, nor did they have any nuclear or barium scans 7 days prior to
testing.
Anthropometry and Body Composition: Weight was measured on an electronic
balance, height by stadiometry, and Body Mass Index (BMI) was
calculated. Waist and hip circumferences were measured according to the
protocol provided by the World Health Organisation (WHO), using a body
measuring tape (21). Sexual maturation was assessed by self-reported
Tanner scores using pictograms (22). Body composition was then measured
using a dual-energy X-ray absorptiometry (DEXA) scanner. DEXA scans were
taken using the Lunar iDXA by GE Healthcare powered by
enCORETM software (Version 15), while the participant
was lying down within the confines of the scan. From the scan, total
body mass, lean body mass, total fat mass, and LLM were extracted. As
done by others (23), chest mass and fat mass, and abdominal mass and fat
mass, were also derived.
Questionnaires: Habitual physical activity level was assessed using the
IPAQ-A (International Physical Activity Questionnaire for Adolescents).
The IPAQ-A measured overall total physical activity and was scored in
MET-minutes (metabolic equivalent of task) per week, according to MET
values provided by the IPAQ Research Committee (24). Sedentary time was
assessed using the ASAQ (Adolescent Sedentary Activity Questionnaire)
(25). Participants were asked to think about a normal week, during
school term, and to report how long they usually spent engaged in
several different sedentary behaviours before and after school on each
day of the week, as well as on each day of the weekend. Time spent in
each category of sedentary behaviour and total time being sedentary were
calculated for weekdays, weekend days and all days.
Spirometry was performed as per ATS/ERS standards (26) using
multi-ethnic Global Lung Initiative predictive values (27).
Isokinetic cycling: Participants underwent a 30-sec isokinetic cycle
test (Excalibur Sport Ergometer PFM 06 Version 10.14.0, Lode). This test
fixed the pedalling speed and calculated force, total 30-second work,
and fatiguability (peak force-end force)/(peak force) expressed as a
percentage. Initially subjects were tested at a pedalling speed of 60
RPM. For ease of cycling, most were tested at a 90 RPM. Peak force and
fatiguability differ when tested at 60 and 90 RPM, but 30-second work
does not differ (28), so for analysis, the 30-second work (watts) was
used. No predicted values are available for the isokinetic cycle used.
Progressive exercise testing: Following a rest period after performing
isokinetic cycling, progressive exercise testing was performed by cycle
ergometry with gas exchange while wearing a facemask
(VyntusTM CPX powered by
SentrySuiteTM Software Solution (V2.19.96)). A
standard modified Godfrey protocol (1-minute incremental protocol)
progressive exercise test, with workload increments increasing by 10, 15
or 20 W/min was employed. According to the participant’s predicted
maximal exercise capacity (29), the workload was selected to have the
test completed in 8 – 12 minutes. The test was stopped when the
participant could no longer maintain the 60 RPM cycling cadence. Maximal
workload (29) and peak oxygen consumption (30) were recorded.
Data Analysis: With the control group having a mean value for maximal
exercise capacity of 100% predicted and a SD of 20, and the group of
AlwO having a mean value of 80% predicted, 22 subjects in each group
would enable detection of this difference with a power of 0.90. For
purposes of exercise and muscle function, we expressed data (presented
as mean ± SD for normally distributed variables, median ± interquartile
range) in terms of absolute values, percent predicted values and
allometrically scaled values. Normality was assessed by Shapiro-Wilk
test, equality of variances was assessed by Levene’s test, and effect
size was assessed by Cohen’s d, which allowed for parametric testing to
be used. When normality was demonstrated, groups were compared using
Student t-test, and modeling of exercise capacity was done using Pearson
correlation and forward stepwise regression. Nonparametric relations
were assessed by Spearman rank correlation. When variables were not
normally distributed, groups were compared by Mann Whitney U test. A
p-value <0.05 was considered as significant. Statistical
analysis was performed using statistical software (JASP Version 0.17
Intel, University of Amsterdam, Netherlands).
Scaling: The relation between size and function is best assessed using
allometric scaling (31). This uses a power function (eg, peak oxygen
consumption=aXbexp(c.group), where a
is the proportionality coefficient, X is the mass to be scaled to, and b
is the allometric scaling factor). Typically maximal exercise capacity
is compared between groups by expressing maximal exercise capacity as
per kg of body mass (implying a scaling factor b=1). However, employment
of a scaling factor of 1 leaves large residual effects, even when using
LLM in the evaluation of cycling performance (17, 18, 32). In the
current study, allometric scaling was conducted to derive a scaling
factor such that work per kg of LLM to the power of b did not correlate
with LLM to the power of b.
Results
23 nonobese adolescents and 24 AlwO were recruited. As not all tests
were completed for each participant, results of the 22 participants in
each group (9 male/13 female nonobese, 12 male/10 female AlwO) with
complete data are reported.
Anthropometric and lung function results are reported in Table 1. The
groups did not differ with respect to sex distribution, age, height or
level of sexual maturation. As expected, the AlwO group weighed more,
had a greater BMI, waist and hip circumferences, and waist-to-hip ratio.
Correspondingly, DEXA scanning demonstrated that the AlwO group had
greater body mass, lean and fat mass, percent body fat, LLM, chest mass
and chest fat mass, and abdominal mass and abdominal fat mass (Table 2).
The AlwO group was less physically activity (total activity and MVPA)
but did not spend more time being sedentary (Table 3).
The AlwO group tended to have greater lung function for their height
(Table 4).
An allometric scaling factor (0.85, 95% confidence interval: 0.622,
1.085) for LLM was derived according to the method of Batterham and
colleagues (31) using regression analysis of Peak Oxygen Consumption to
LLM for the combined groups. The validity of this factor was confirmed
as there was no significant correlation between maximal exercise
capacity (Wmax or VO2 Peak/(kg
LLM)0.85) and the scaled LLM.
The groups did not differ in 30-second isokinetic work capacity in
absolute terms (9.42 ± 4.252 w vs 11.46 ± 4.657 w, control vs AlwO) or
per scaled LLM (0.93 ± 0.260 vs 0.85 ± 0.249
w/(LLM)0.85, control vs AlwO).
Maximal exercise capacity and Peak Oxygen Consumption did not differ
between the groups in absolute terms and when expressed as a percent of
predicted. However, when expressed per scaled LLM, both maximal exercise
capacity and Peak Oxygen Consumption were reduced in the AlwO group
(Table 5). Peak oxygen pulse did not differ between the groups (11.23 ±
3.89 vs 12.52 ± 2.90 mL/beat, control vs AlwO)
Maximal exercise, whether in watts or peak ml of oxygen consumed
(VO2 peak) correlated with both FEV1 and
30-sec isokinetic work capacity, alone (Figure 1a-d) and combined (Wmax
r=0.87, p<0.001; VO2 Peak: r=0.85,
p<0.001), with no group effect. 30-second leg work capacity
correlated with scaled LLM, with a difference between the groups (Figure
2). There was some correlation between leg work capacity and time spent
in MVPA (rs=0.39, p=0.07) in AlwO, but not the control
group. There was no significant correlation between exercise capacity
(Wmax, VO2 Peak, 30-sec isokinetic work capacity) and
the amount of time spent in MVPA. Time spent in MVPA also did not
contribute significantly to the correlation of maximal exercise capacity
(Wmax, VO2 Peak) when FEV1 and 30-sec
isokinetic work capacity were factored in.
Discussion
When scaled to the amount of LLM (the active mass during cycling
exercise), AlwO had reduced exercise capacity. Isokinetic leg work
capacity correlated with LLM, but there was a steeper relation in AlwO.
AlwO also spent less time in MVPA, although not more time in sedentary
activities.
Lung function tended to be greater in AlwO. In a younger cohort of
children, obesity did not affect spirometric values (23). Of note, the
current population had a lower BMI percentile compared to the study of
younger children (mean 98.55 vs 122.6), but a non-significant greater
z-score (mean 2.33 vs 2.18). In addition, the average chest mass and
abdominal mass, as a % of total mass, was lower in the current
population. It is possible that the greater BMI percentile and relative
chest and abdominal masses in the younger group counterbalanced any
potential increase respiratory muscle strength induced by the work of
breathing against the additional mass.
The amount of habitual MVPA was lower in AlwO. The IPAQ scale correlates
with movement activities as assessed by accelerometry, even in obese
youth (33-35). Standard Metabolic Equivalent(s) of Task (METS)
calculations do not account for the extra energy expenditure associated
with movement of the larger mass in obesity. It has been suggested that
this should be scaled to lean tissue mass (36). However, the AlwO group
still had reduced MVPA even when scaling to LLM (Table 3). As reported
in a systematic review, sedentary time was not increased in AlwO (37).
Maximal exercise capacity between the nonobese adolescents and AlwO
differed when using allometric scaling using LLM, but not in absolute or
as a percent predicted values. Scaling is meant to correct for body size
and remove its influence (32). This is particularly important in
children. Our scaling factor of 0.85 (95% confidence interval: 0.622,
1.085) is higher than that (0.51 males, 0.45 females, confidence
intervals not reported) previously found in a study of adults aged 20-80
years using cycle ergometry (38). These authors found that
VO2 peak per scaled LLM negatively correlated with age.
Others have found scaling factors of 0.55-0.64 in children but scaling
was to treadmill oxygen consumption and not cycle ergometry (17, 39).
Thus, our scaling factor is in the range of those found by others. In
the future, with larger sample sizes, sex specific scaling factors
should be determined.
It is unclear why scaled exercise capacity was reduced in AlwO. Exercise
capacity correlated with lung function and leg muscle function
individually and combined, with no group differences. There was a group
difference for leg work capacity compared to LLM, whether in absolute or
when scaled. This is largely due to a lower leg work capacity in AlwO
with smaller LLM (Figure 1e). None of the AlwO met criteria for the
Metabolic Syndrome. However, the AlwO were less physically active, and
for the AlwO, but not for the nonobese group, there was some correlation
between leg work capacity and time spent in MVPA (r=0.44,
p<0.05, rs=0.39, p=0.07). Thus, it is possible
that the amount of time spent in MVPA impacted our results. A larger
sample size and measures that accurately capture the energy expenditure
of AlwO and LLM would help clarify this. However, this does suggest that
AlwO would benefit from programs aimed at increasing the habitual time
spent in MVPA (40).
In conclusion, AlwO have larger LLM and often preserved exercise
capacity, when looked on as percentage of predicted. Leg muscle
performance in AlwO appears influenced by the amount of time habitually
spent in MVPA. Increasing time spent in MVPA may benefit AlwO.
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