RESEARCH ARTICLE
Cardiorespiratory and metabolic responses
and reference equation validation to predict
peak oxygen uptake for the incremental
shuttle waking test in adolescent boys
Andreza L. Gomes1☯, Vanessa A. Mendonc¸a1☯, Tatiane dos Santos Silva1‡, Crislaine K.
V. Pires1‡, Liliana P. Lima1‡, Alcilene M. Silva1‡, Ana Cristina R. Camargos1,2‡, Camila D.
C. Neves1‡, Ana C. R. Lacerda1‡, He´rcules R. LeiteID1☯*
1 Programa de Po´s-Graduac¸ão em Reabilitac¸ão e Desempenho Funcional, Departamento de Fisioterapia,
Universidade Federal dos Vales do Jequitinhonha e Mucuri (UFVJM), Campus JK, Alto da Jacuba,
Diamantina, Minas Gerais, Brazil, 2 Escola de Educac¸ão Fı´sica, Fisioterapia e Terapia Ocupacional
(EEFFTO), Departamento de Fisioterapia, Universidade Federal de Minas Gerais (UFMG), Diamantina,
Minas Gerais, Brazil
☯ These authors contributed equally to this work.
‡ These authors also contributed equally to this work.
* hercules.leite@ufvjm.edu.br
Abstract
Background
Previous studies speculated that the Incremental Shuttle Walking Test (ISWT) is a maximal
test in children and adolescents, however comparison between ISWT with cardiopulmonary
exercise test has not yet performed. Furthermore, there is no regression equation available
in the current literature to predict oxygen peak consumption (VO2 peak) in this population.
This study aimed to assesses and correlate the cardiorespiratory responses of the ISWT
with the cardiopulmonary exercise (CEPT) and to develop and validate a regression equa-
tion to predict VO2 peak in healthy sedentary adolescent boys.
Methods
Forty-one participants were included in the study. In the first stage, the VO2 peak, respira-
tory exchange ratio (R peak), heart rate max (HR max) and percentage of predicted HR max
(% predicted HR max) were evaluated in CEPT and ISWT (n = 26). Second, an equation
was developed (n = 29) to predict VO2 peak. In both phases, the VO2 peak, respiratory
exchange ratio R and hearth rate (HR) were evaluated. In the third stage, the validation
equation was performed by another 12 participants.
Results
Similar results in VO2 peak (P>0.05), R peak (P>0.05) and predicted maximum HR
(P>0.05) were obtained between the ISWT and CEPT. Both tests showed moderate signifi-
cant correlations of VO2 peak (r = 0.44, P = 0.002) e R peak (r = -0.53, P < 0.01), as well as
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OPEN ACCESS
Citation: Gomes AL, Mendonc¸a VA, Santos Silva
Td, Pires CKV, P. Lima L, Silva AM, et al. (2018)
Cardiorespiratory and metabolic responses and
reference equation validation to predict peak
oxygen uptake for the incremental shuttle waking
test in adolescent boys. PLoS ONE 13(11):
e0206867. https://doi.org/10.1371/journal.
pone.0206867
Editor: Gustavo Batista Menezes, UFMG, BRAZIL
Received: August 17, 2018
Accepted: October 19, 2018
Published: November 1, 2018
Copyright: © 2018 Gomes et al. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Data Availability Statement: All relevant data are
within the manuscript and its supporting
information files.
Funding: The authors are grateful to Brazilian
agencies CNPq, CAPES and FAPEMIG for financial
support.
Competing interests: The authors have declared
that no competing interests exist.
the agreement of these measurements by Bland-Altman analysis (VO2 peak, bias = -0.13; R
peak, bias = 0.0). Distance walked was the variable that explained 42.5% (R2 = 0.425, p =
0.0001) of the variance in VO2 peak. The equation was VO2 peak (predicted) = 20.94 +
(0.02 x distance walked). The results obtained by the equation were not significantly differ-
ent compared to the values obtained by the gas analyzer and the Bland-Altman analysis
showed agreement (bias = 1.6).
Conclusion
The ISWT produced maximal cardiorespiratory responses comparable to the CEPT, and
the developed equation showed viability for the prediction of VO2 peak in healthy sedentary
adolescent boys.
Introduction
Assessment of functional capacity or cardiorespiratory fitness (CRF) is defined as the ability to
perform a moderate to high intensity exercise involving large muscle groups over a period of
time [1,2]. It is an important component of health related physical fitness, which reflects the
functional capacities of the respiratory, cardiovascular and musculoskeletal systems [1]. The
CRF assessment has been widely used in clinical practice and research aiming to provide
parameters for physical activity prescription and to evaluate reduced exercise tolerance in sev-
eral health conditions [3–5].
The performance of a cardiopulmonary exercise testing (CEPT) followed by the measure-
ment of peak oxygen consumption (VO2 peak) through the direct analysis of exhaled gases is
the most commonly reported procedure in the literature for the evaluation of CRF [6]. How-
ever, this measurement is often infeasible because its require high-cost equipment, specialized
laboratory and trained professionals [7]. Thus, field test and prediction equation to indirect
estimate VO2 peak in clinical practice has been widely implemented [2]. Among the field test,
we highlight the Incremental Shuttle Walking Test (ISWT) developed by Sing et al., [8] which
comprises as a simple incremental walk test with pace dictated by external stimulus which
asses CRF based on distance walked. Despite being developed initially for individuals with
chronic obstructive pulmonary disease [8], it has been used recently in different health condi-
tions and age groups [5,9,10].
Some studies have used ISWT to asses CRF in children and adolescents with asthma [11],
scoliosis [5] and very low premature newborn [10]. However, the application and intensity of
this test in a healthy population is scarce. Lanza et al., [9] developed an equation to predict dis-
tance walked and also showed that the ISWT is a maximal test in a children and adolescent
population determined indirectly by means of the maximum heart rate (HR max) achieved at
the end of the test. On the other hand, Coelho et al. [12] demonstrated that a healthy control
group of children and adolescents showed submaximal values of HR max in the ISWT. How-
ever, these authors fail to confirm the cardiorespiratory responses with the completion and
comparison with the CEPT.
Taken together, there is a gap in the current literature regarding the ISWT intensity valida-
tion, as well as an equation to predict VO2 peak in the adolescent population. Thus, the present
study aims to evaluate and correlate the cardiorespiratory outcomes during the ISWT and a
CEPT, in order to classify the intensity of ISWT, and to develop and validate an equation to
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predict VO2 peak in healthy adolescent boys. We postulate that the ISWT would promote
maximal cardiorespiratory responses in agreement with the CEPT, and the regression equa-
tion would be feasible for predicting VO2 peak in healthy adolescent boys.
Materials and methods
This was a cross-sectional study that included 41 healthy adolescent boys. They were recruited
by convenience from private and public schools. The protocol began in July 2016 and ended in
November 2017. All measurements were obtained in the physiology of exercise laboratory
(UFVJM) by trained investigators. The parents were asked to report the health history of the
subject (i.e., prematurity birth and current physical activity engagement and comorbidities).
Thus, the inclusion criteria were as follows: male boys, ages 12–18 years old, absence of chronic
or acute diseases, physical activity engagement less than three times a week, preterm birth and
parents sign the consent form. The volunteers were excluded if they were unable to understand
the test. To meet the objectives, this study was divided into three stages. The first stage aimed
to evaluate the intensity of the ISWT; the second stage aimed to develop a regression for the
prediction of VO2 peak; and the third stage to validate the prediction equation. This study fol-
lowed the declaration of Helsinki. The Ethics and Research Committee of Universidade Fed-
eral dos Vales do Jequitinhonha e Mucuri (UFVJM), Brazil, approved this study (Protocol:
52980816.4.0000.5108). The following protocol description reproduces information already
reported elsewhere [2].
First stage procedures
In the first stage, 26 volunteers went to the laboratory on three consecutive days at the same
time period each day. On the first day, the body composition was assessed (weight, height,
BMI) and familiarization was performed. The weight and height were measured on an anthro-
pometric mechanical scale, the BMI was calculated as the weight divided by height squared
[3]. Familiarization consisted of testing that would be performed on consecutive days to
reduce the effect of learning. On the second and third days, the ISWT and CEPT were applied.
The testing order was randomized and balanced. The subjects were instructed to avoid physi-
cal activity and any intake of caffeine in the 24 hours prior to testing, to get at least 8 hours of
sleep the night before, to eat a light meal and to ingest 500 ml of water in two hours before the
tests. On the days of testing subjects were asked about their compliance with the recommenda-
tions above and about possible complications or changes in their daily routines [2].
To perform the ISWT, the participants were instructed to walk a distance of 10 meters
around a marking between two cones, placed 0.5m from each endpoint [8]. The walking speed
at which the participant should walk (or run) was dictated by a sound played from a CD that
was originally generated by a microcomputer. Each minute the walking speed increased by
0.17m/s. The test was finished when the volunteer was not able to maintain the required speed
(more than 0.5m from the cone), at the request of the volunteer, or for some other reported
symptom (dyspnea, dizziness, vertigo, angina). The original protocol consisted of 12 levels
(1020m); however, as suggested by the literature, we used a protocol of 15 levels (1500m) to
evaluate healthy participants, in order to prevent the ceiling effect [13]. Additionally, during
the testing, the laps were recorded to calculate the distance and gait speed reached at the last
full level. The ISWT were performed twice with at least 30 min of rest between them. The best
test (i.e., the longest distance walked) was considered for analysis. The maximum difference
between the tests should be 40 m [14]. A third test was performed when the difference was
greater than this. A trained professional conducted the tests. Before and after the test, heart
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rate (HR, measured by a heart rate monitor) and blood pressure (measured by a mercury
sphygmomanometer cuff and a stethoscope) were measured.
The CEPT was performed on a treadmill using a protocol based on the progression of the
ISWT. This protocol consisted of 1-minute stages, with speed increasing every minute without
increasing the incline of the treadmill. The initial speed was 0.5 m/s, and it increased by 0.17
m/s at each stage. Before, during and after the test, heart rate and blood pressure were mea-
sured as described above. The criteria for stopping the test was as follows systolic blood
pressure (SBP) greater than 210 mmHg; diastolic blood pressure greater than 120 mmHg; sus-
tained decrease in SBP, angina dyspnea, cyanosis; nausea, dizziness or by the request of the
volunteer [15].
Second stage procedures
In the second stage 29 volunteers went to the laboratory at two different days. On the first day,
the body composition measurements were obtained as described in the first stage. On the sec-
ond day, the participants went to the laboratory for two ISWT with an interval of 30 minutes
between them. Completion of two ISWTs with this interval had been suggested to reduce
the effects of the learning test [13,16]. For the data analysis, the results of the test in which the
volunteer obtained the greatest distance covered were used. As with the first stage, the entire
procedure took place during a single day shift: the subjects were instructed to follow all the rec-
ommendations for the practice of physical tests, and prior to completion of the tests.
Cardiorespiratory and metabolic responses
During the tests of the two stages of this study, the exhaled gases were collected using a gas
analyzer via the portable telemetry system (k4b2, Cosmed, Rome, Italy). Among other vari-
ables, oxygen uptake (VO2), respiratory quotient (R) and HR breath-by-breath were moni-
tored. The absolute VO2 peak rate (mL/min) was expressed as relative rate defined as VO2
peak (mL/kg/min) and R peak the highest value of these measures at peak effort [17] and maxi-
mum heart rate (HRmax) as the highest HR value recorded during the test [2]. The maximum
predicted HR was calculated as 208 (0.7  age) [18].
Validation of the reference equation
To validate the equation, a different group of healthy males, composed of 12 individuals, was
selected according to the same inclusion criteria of the study. This group completed the ISWT
as described in the preceding stages. Likewise, the VO2 peak was predicted by the reference
equation.
Statistical analysis
The statistical analysis was performed using the statistical packages SPSS 22.0 (Inc., USA) and
GraphPad Prism 4 (Inc., USA). In the first stage, the normality of data was checked by the Sha-
piro–Wilk test and the differences among measured variables were determined by paired-t-
test for variables with normal distribution or the Wilcoxon test for variables with non-normal
distribution. Pearson’s coefficient of correlation was performed to study the correlation
between variables and the agreement between tests was assessed by Bland-Altman analysis.
The sample size was calculated based on the study by Neves et al [2] and was identified at least
10 participants. In the second stage, the normality of data was checked by Kolmogorov-Smir-
nov test and for compiling the reference equation, the linear multiple regression analysis was
performed to identify the predictors of the dependent variable. Multicollinearity was measured
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by variance inflation factors (VIF). In this stage, the sample size was estimated on GPower
Software version 3.1 and based on the relationship between the numbers of variables to be
included in the multiple regression analysis and the minimum number of observations
required, indicating at least 29 participants in order to develop a linear model containing up to
three variables. At the end of the regression analysis, the paired t-test was utilized to compare
the means of the results obtained by the reference equation with the measured values of VO2
peak obtained using the gas analyzer. Moreover, the validation of the reference equation was
evaluated in an additional group of 12 volunteers: the values of VO2 peak obtained by the ref-
erence equation were compared with the measured values of VO2 peak obtained by the gas
analyzer using the paired t-test. The level of statistical significance was P<0.05.
Results
A total of 336 subjects were screened, but 186 did not return the baseline questionnaire. From
the 150 eligible participants, 28 reported any chronic, acute illness or reported premature
birth, 49 decline and 32 subjects were excluded for other reasons. The final sample was 41
male adolescents.
First stage
The general characteristics of the participants of first and second stage and their performance
on ISWT are showed in Table 1. The cardiorespiratory responses obtained at the end of the
ISWT and CEPT are presented in Table 2. Similar results in VO2 peak, R peak, and predicted
HRmax were found. Moderate and significant correlations in VO2 peak (r = 0.44, P = 0.02)
and R peak (r = -0.53, P<0.01) were found between the tests. The Bland-Altman analysis also
showed agreement between the results for VO2 peak (bias = -0.13) and R peak (bias = 0.00) on
the ISWT and CEPT (Fig 1A and 1B).
Table 2. Comparison between the results of cardiorespiratory variables at the end of the test, obtained in ISWT
and CEPT.
Outcome
Tests
Comparison between tests
ISWT (n = 26)
CEPT (n = 26)
P-value
VO2 peak (mL/kg/min)
44.02 (8.2)
44.2 (6.2)
0.93a
R peak
1.1 (0.2)
1.1 (0.1)
0.28b
HR max (% predicted)
98.8 (6.3)
96.6 (3.5)
0.63b
The data is presented as mean (SD). ISWT = incremental shuttle walking test; CEPT = cardiopulmonary exercise
testing; VO2 = oxygen uptake; R = respiratory exchange ratio; HR = heart rate.
aPaired-t test,
bWilcoxon test.
https://doi.org/10.1371/journal.pone.0206867.t002
Table 1. Characteristics of participants of the first, second and third stage.
Characteristics of the participants
(n = 41)
First phase
(n = 26)
Second phase
(n = 29)
Third phase
(n = 12)
Age (yr)
14.2 (1.8)
14.3 (1.8)
14.3 (1.9)
BMI (kg/m2)
19.5 (2.4)
19.5 (2.4)
20.5 (2.8)
Gait speed (m/s)
2.2 (0.3)
2.2 (0.3)
2.2 (0.4)
Distance walked (m)
923.9 (249.4)
938.0 (250.2)
915 (309.5)
The data is presented as mean (SD). BMI = body mass index.
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Fig 1. Agreement between VO2 (mL/kg/min) peak and R peak obtained in the ISWT and CEPT. (A) Bland-Altman plot of the
difference between the VO2 peak of the ISWT and CEPT plotted against the mean VO2 peak of the ISWT and CEPT; (B) Difference R
peak of the ISWT and CEPT plotted against the mean R peak of the ISWT and CEPT. ISWT = Incremental Shuttle Walking Test;
CEPT = cardiopulmonary exercise testing; VO2 = oxygen uptake; R = respiratory exchange ratio.
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Second stage
The characteristics of the participants of the second stage are showed in Table 1. Considering
the best ISWT, age, BMI and distance walked were the demographic, anthropometric and
physical performance variables selected for the preparation of the reference equation, respec-
tively. The univariate analysis showed that the VO2 peak correlated significantly with age
(r = 0.38, p = 0.04), and distance (r = 0.67, p = 0.0001). There was no significant correlation
with BMI (r = -0.24, p = 0.22). A model of stepwise linear multiple regressions showed that dis-
tance walked explained 42.5% (R2 adjusted = 0.425, p = 0.0001) of the variance in VO2 peak.
The 95% Confidence Interval for unstandardized coefficients were the constants (11.12 to
30.77) and distance (0.01 to 0.03). The reference equation for the VO2 peak in the ISWT was:
VO2 peakðpredictedÞ ¼ 20:94 þ ð0:02 x distance walkedÞ
Validation of the reference equation
The characteristics of the volunteers who attended in the equation validation stage were pres-
ent in Table 1. The results obtained by the equation of VO2 peak with the values obtained by
the gas analyzer, showed no significant difference between them (VO2 peak [predicted] =
39.24 ± 6.1 mL/kg/min; VO2 peak [gas analyzer] = 40.87 ± 5.4 mL/kg/min, P = 0.1776). It was
possible to verify the agreement between these measures by the Bland-Altman method, in
which a bias of 1.6 was showed, representing a difference of 4.4% in the VO2 peak (Fig 2). Fur-
thermore, there was no statistically significant difference between the participants of equation
elaboration and validation for age (p = 0.7978), weight (p = 0.5498), height (p = 0.0650), BMI
(p = 0.2480), distance walked (p = 0.9213) and walking speed (p = 0.0.6212).
Discussion
The present study describes the comparison of CRF between the ISWT with CEPT in healthy
sedentary adolescent boys. In the ISWT, the adolescent boys reached values of HRmax > 90%
and R peak > 1.1, thus classifying the ISWT as a maximal effort test [19,20]. Furthermore,
results showed a moderate and significant correlations as well as agreement between VO2 peak
and R peak by both tests. Our results are corroborated by the results of Lanza et al. [9]. These
authors showed that ISWT is a maximal test in children and adolescent by registering higher
Fig 2. Bland-Altman agreement of VO2 peak in the validation of the reference equation.
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HR values (>90%) at end of the test. Our research group also showed previously in healthy
men [2] and women (data not published) that cardiorespiratory outcomes (VO2 peak and R
peak) collected during ISWT are comparable to CEPT test, as well as both tests showed agree-
ment and high correlations between VO2 and R peak between ISTW and CEPT [2]. In the
other hand, previous studies showed lower HR max in healthy control children at end of
the test compared to our data, such as 69% [11] and 55% [10]. However, it’s important to high-
light that our participants were allowed to run which can explain the higher HRmax found. To
the best of our knowledge there are no studies evaluating CRF between ISWT and CEPT in
healthy sedentary adolescent boys. Taken together, our data support that ISWT can be consid-
ered as a valid measure to assess CRF in this population as a maximal effort test.
Additionally, our study is the first one to develop an equation to predict VO2 peak in the
ISWT in this population. Despite of have including anthropometric variables in the multivari-
ate analysis, only distance walked explained the variance of VO2 (43%) peak in our population.
Distance walked as one of the major determinant of VO2 peak was also observed in previous
studies that developed reference equations for the prediction of VO2 peak during the applica-
tion of the ISWT in healthy adults [21,22] and during the six-minute walking test in obese ado-
lescents [23].
Although the age was significantly correlated to VO2 in the linear analysis, this correlation
was not strong the sufficient for explained the variance of VO2 peak. Similar result was
observed by Tsiaras et al. (2010), which shown that the addiction of age did not further
improve the prediction accuracy of the equation for prediction of VO2 peak from a maximal
treadmill test in 12–18 year-old active male adolescents [24]. This absence of influence of age
seems to be related to the stabilization of aerobic performance in youth when compared to
childhood. In fact, previous studies showed that the performance of adolescents improved lin-
early with increase of age, it increased up to 12–13 years, and after (aged 14–19 years) tended
to achieve a plateau [25,26]. As with age, BMI did not influence the prediction of VO2 peak.
The probable reason for this seems to be related to homogeneity of sample of present study. It
is noted that participants of present study showed normal BMI. Thus, given that the CRF is
lower in adolescents who are overweight than in those of normal weight, the normal body
composition did not was correlated to VO2 peak [25,27]. Finally, it’s important to highlight
that distance walked is a feasible variable in clinical practice and have to take into account
when developing a regression equation [28].
Although the prediction equation proposed in the present study might be explained by
moderate variance, the VO2 peak data collected by the gas analyzer and the developed equation
showed agreement. Moreover, the reference values from the current literature that classify
CRF (i.e. very week to excellent) vary approximately 7mL/kg/min among the age ranges. Thus,
the variation found in the present study (4%) is less likely to change the individuals CRF classi-
fication [17]. Finally, the VO2 peak mean reached by the male adolescents in our study (~ 44.0
mL/kg/min) was smaller than previous study reporting VO2 reference for trained men with
age ranging from 15 to 24 (53.3 mL/kg/min) [17] or 10–14 years old ( 52.3 mL/kg/min) [6],
which classifies our population as sedentary [17].
The results pointed here raise important advancing scientific knowledge regarding the level
of ISW in healthy sedentary adolescent boys. The results found in this study contribute to the
process of measurement of peak VO2 becomes more accessible to clinical practice so that the
prescription and elaboration of exercise programs happen in a more informed and assertive
way, as well as ISWT can be used as a maximal effort test in replacement of submaximal
field test available (e.g. six minute walking test) [29]. Moreover, clinicians should considerer
ISWT instead of other field test (e.g. 9-minute walk / run test, 1-mile walk / run test and
the 20 m Shuttle Run Test) [30–32] because these tests are influenced by external factors
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(e.g. motivation and self-paced) which can lead to great variability and compromising the
application in randomized controlled trials. Lastly, our prediction equation could be used in
clinical studies aiming to investigate CRF in disable adolescent boys population avoiding to
use control groups for comparing theirs results [5,9,10]. However, due to restrictions of fund-
ing and time, no further experiments such as assessing girls and children with age under 12
years old were conducted. Further studies are necessary to address this population.
Conclusion
In a conclusive way, the VO2 peak values found in our study allow us to affirm that the ISWT
was in fact a maximum intensity test in healthy sedentary adolescent boys assessed by direct
gas analyzer. Furthermore, the regression equation was feasible and might be useful for clini-
cians for predicting VO2 peak in this population.
Author Contributions
Conceptualization: Andreza L. Gomes, Vanessa A. Mendonc¸a, Alcilene M. Silva, Ana Cristina
R. Camargos, Camila D. C. Neves, Ana C. R. Lacerda, He´rcules R. Leite.
Data curation: Tatiane dos Santos Silva, Crislaine K. V. Pires, Ana Cristina R. Camargos.
Formal analysis: Andreza L. Gomes, Vanessa A. Mendonc¸a, Ana Cristina R. Camargos, He´r-
cules R. Leite.
Funding acquisition: Vanessa A. Mendonc¸a, He´rcules R. Leite.
Investigation: Vanessa A. Mendonc¸a, Crislaine K. V. Pires, Liliana P. Lima, He´rcules R. Leite.
Methodology: Andreza L. Gomes, Tatiane dos Santos Silva, Ana Cristina R. Camargos, He´rcu-
les R. Leite.
Project administration: Ana C. R. Lacerda, He´rcules R. Leite.
Resources: He´rcules R. Leite.
Supervision: Ana C. R. Lacerda, He´rcules R. Leite.
Validation: He´rcules R. Leite.
Writing – original draft: He´rcules R. Leite.
Writing – review & editing: Vanessa A. Mendonc¸a, Liliana P. Lima, Camila D. C. Neves, He´r-
cules R. Leite.
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Cardiorespiratory and metabolic responses and reference equation validation to predict peak oxygen uptake for the incremental shuttle waking test in adolescent boys.
Gomes, Andreza L,Mendonça, Vanessa A,Dos Santos Silva, Tatiane,Pires, Crislaine K V,Lima, Liliana P,Gomes, Alcilene M,Camargos, Ana Cristina R,Neves, Camila D C,Lacerda, Ana C R,Leite, Hércules R