Cardiorespiratory Fitness and Physical Activity in Pediatric Diabetes

Original Investigation | Pediatrics
Cardiorespiratory Fitness and Physical Activity in Pediatric Diabetes

A Systemic Review and Meta-Analysis
Hannah Steiman De Visser, BSc; Isaak Fast, BSc; Nicole Brunton, MSc, PhD(c); Edward Arevalo, BSc; Nicole Askin, MLIS; Rasheda Rabbani, PhD;
Ahmed M. Abou-Setta, MD, PhD; Jonathan McGavock, PhD
Abstract Key Points

Question Are cardiorespiratory fitness
IMPORTANCE It is unclear whether cardiorespiratory fitness (CRF) and physical activity are lower
(CRF) and physical activity lower among
among youths with type 1 diabetes (T1D) and type 2 diabetes (T2D) compared with youths without
youths with diabetes compared with
diabetes.
youths without diabetes?
OBJECTIVE To describe the magnitude, precision, and constancy of the differences in CRF and Findings In this systematic review and
physical activity among youths with and without diabetes. meta-analysis of 18 studies including
1988 youths with type 2 diabetes (T2D)
DATA SOURCES MEDLINE, Embase, CINAHL, and SPORTDiscus were searched from January 1, and 59 studies with 14 278 youths with
2000, to May 1, 2022, for eligible studies. type 1 diabetes (T1D), CRF was 44.5%
lower and physical activity 8.3% lower in
STUDY SELECTION Observational studies with measures of CRF and physical activity in children and youths with T2D compared with peers
adolescents aged 18 years or younger with T1D or T2D and a control group were included. without diabetes. Both CRF and physical
activity were 10% lower in youths with
DATA EXTRACTION AND SYNTHESIS Data extraction was completed by 2 independent reviewers. T1D compared with peers without
A random-effects meta-analysis model was used to estimate differences in main outcomes. The diabetes.
pooled effect estimate was measured as standardized mean differences (SMDs) with 95% CIs. The
Meaning These findings suggest that
Preferred Reporting Items for Systematic Review and Meta-Analyses guideline was followed.
deficits in CRF are larger and more
consistent in youths with T2D vs T1D,
MAIN OUTCOMES AND MEASURES The main outcomes were objectively measured CRF obtained
reinforcing calls for novel interventions
from a graded maximal exercise test and subjective or objective measures of physical activity.
to empower these youths to engage in
Subgroup analyses were performed for weight status and measurement type for outcome measures.
regular physical activity.
RESULTS Of 7857 unique citations retrieved, 9 studies (755 participants) with measures of CRF and
9 studies (1233 participants) with measures of physical activity for youths with T2D were included; + Supplemental content
for youths with T1D, 23 studies with measures of CRF (2082 participants) and 36 studies with Author affiliations and article information are
measures of PA (12 196 participants) were included. Random-effects models revealed that directly listed at the end of this article.
measured CRF was lower in youths with T2D (SMD, −1.06; 95% CI, −1.57 to −0.56; I2 = 84%; 9
studies; 755 participants) and in youths with T1D (SMD, −0.39; 95% CI, −0.70 to −0.09; I2 = 89%; 22
studies; 2082 participants) compared with controls. Random-effects models revealed that daily
physical activity was marginally lower in youths with T1D (SMD, −0.29; 95% CI, −0.46 to −0.11;
I2 = 89%; 31 studies; 12 196 participants) but not different among youths with T2D (SMD, −0.56; 95%
CI, −1.28 to 0.16; I2 = 91%; 9 studies; 1233 participants) compared with controls. When analyses were
restricted to studies with objective measures, physical activity was significantly lower in youths with
T2D (SMD, −0.71; 95% CI, −1.36 to −0.05; I2 = 23%; 3 studies; 332 participants) and T1D (SMD, −0.67;
95% CI, −1.17 to −0.17; I2 = 93%; 12 studies; 1357 participants) compared with controls.
CONCLUSIONS AND RELEVANCE These findings suggest that deficits in CRF may be larger and
more consistent in youths with T2D compared with youths with T1D, suggesting an increased risk for
(continued)
Open Access. This is an open access article distributed under the terms of the CC-BY License.
JAMA Network Open. 2024;7(2):e240235. doi:10.1001/jamanetworkopen.2024.0235 (Reprinted) February 23, 2024 1/15
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JAMA Network Open | Pediatrics Cardiorespiratory Fitness and Physical Activity in Pediatric Diabetes
Abstract (continued)
cardiovascular disease–related morbidity in adolescents with diabetes, particularly among those with
T2D. The findings reinforce calls for novel interventions to empower youths living with diabetes to
engage in regular physical activity and increase their CRF.
JAMA Network Open. 2024;7(2):e240235. doi:10.1001/jamanetworkopen.2024.0235
Introduction
Cardiorespiratory fitness (CRF)1,2 and physical activity3,4 in adolescence are important modifiable
determinants of pediatric cardiometabolic disease and long-term mortality.5 Adolescents with high
CRF6,7 and high daily physical activity3,4 are characterized as having lower blood pressure and lower
central and overall obesity and may be less likely to develop cardiovascular disease–related morbidity
in adulthood. Accordingly, engaging in regular physical activity8,9 and increasing CRF10 are consistent
recommendations for optimal growth and health for children and adolescents, including those living
with diabetes.11-15
Current clinical practice and expert guidelines argue that children and adolescents (referred to
herein as youths) with type 1 diabetes (T1D) and type 2 diabetes (T2D) may be less active and have
lower CRF than their peers without diabetes.11-15 Despite these claims, the evidence is mixed. Some
studies have documented large deficits in physical activity and CRF in youth with T2D,16 while others
have suggested that the differences are less profound.17 Among youths with T1D, some studies have
found lower levels of physical activity and CRF,18 while many have suggested no difference19 or, in
some cases, higher levels of physical activity.20 In the absence of a systematic review and meta-
analysis of observational studies, the consistency, magnitude, and precision of these differences
remain unclear. More accurate estimates of the differences in physical activity and CRF among youths
living with chronic diseases is a priority among researchers in this area,21 and understanding the
magnitude of these differences could help to tailor behavioral interventions to improve health
outcomes for youths living with diabetes. To address these knowledge gaps in clinical pediatric
diabetes, a systematic review and meta-analysis was done to determine whether (1) CRF and physical
activity are lower among youths with diabetes compared with youths without diabetes and (2) to
assess the overall quality of studies that describe differences in CRF and physical activity among
youths with diabetes and their peers without diabetes.
Methods
Data Sources and Search Strategy
This systematic review and meta-analysis was conducted according to the Methodological
Expectations of Cochrane Reviews22 and reported according to the Preferred Reporting Items for
Systematic Reviews and Meta-Analyses (PRISMA) guideline.23 Institutional ethics approval was not
required for this study as individual-level data were not used for the analysis.
We searched MEDLINE, Embase, CINAHL, and SPORTDiscus. Controlled vocabulary and free-
text terms were used. A search for cross-sectional and cohort studies published between January 1,
2000, and May 1, 2022, was conducted (eTable 1 in Supplement 1). The systematic review followed
a priori eligibility criteria, and the protocol was registered in the PROSPERO International Prospective
Register of Systematic Reviews (CRD42022329303).
Inclusion Criteria and Classification of Diabetes Type

We included cross-sectional and cohort studies that compared measures of CRF or physical activity
between youths with T1D or T2D and controls without diabetes. The inclusion criteria for data
extraction and meta-analyses were studies of youths up to age 18 years, cases of youths with T1D or

T2D, a comparison group without diabetes, and published estimates of differences and variance for
physical activity or CRF between youths with diabetes and controls without diabetes. We excluded
experimental studies and studies that included data from adults (aged >18 years), compared youths
with T1D and T2D directly without a comparison group without diabetes, or were published in
languages other than English. We applied definitions established by Diabetes Canada24,25 and the
American Diabetes Association26,27 to define T2D (hyperglycemia in the absence of markers of
autoimmune disease) and T1D (autoimmunity and requirements for exogenous insulin) in youth.
Study Selection
Abstracts and titles of relevant citations were independently screened by 3 reviewers (H.S.D., I.F.,
and E.A.) to determine eligibility. Prior to the full screen, a preliminary screen of 30 titles and
abstracts was conducted to determine a preliminary agreement rating. As the preliminary agreement
rate was adequate (28 of 30 abstracts were in agreement), the same reviewers independently
screened all remaining titles and abstracts. Two reviewers (H.S.D. and I.F.) independently assessed
the eligibility of full-text articles using a standardized prepiloted form outlining the inclusion and
exclusion criteria. Disagreements were resolved by consensus or with the involvement of a third
reviewer (J.M.).
Data Extraction
Data were extracted independently by 2 reviewers (H.S.D. and I.F.), with disagreements resolved by
consensus or with the involvement of a third reviewer (J.M.). Two authors (H.S.D. and I.F.) extracted
data for study population demographics (age, sex, weight status, race and ethnicity [Black, Hispanic,
Indigenous, White, and other], duration of diabetes, socioeconomic status) and outcome measures.
We examined data on race and ethnicity because rates of T2D are disproportionally higher in
racialized youths. We also created binary variables for the methods used to collect physical activity
(objective vs subjective) and CRF (field vs laboratory) and within the measure of CRF, whether the
tests were maximal or submaximal. Objective methods included pedometer- or accelerometer-based
quantification of daily physical activity, while subjective methods included a range of self-reported
tools. Laboratory-based methods to quantify CRF included graded maximal tests to exhaustion and
submaximal tests with measured rates of oxygen consumption. Field tests of CRF included graded
maximal tests to exhaustion (ie, shuttle run tests) that reported estimated rates of peak oxygen
consumption (V̇o2peak) or time to exhaustion.
Outcomes of Interest and Subgroup Analyses

Cardiorespiratory fitness was reported as the rate of maximal rate of oxygen consumption relative to
body weight (milliliters per kilogram per minute) or mass of fat-free mass (milliliters per kilogram
fat-free mass per min) or time to exhaustion at the end of a graded maximal exercise test. Physical
activity was reported as minutes of physical activity per day, minutes of moderate to vigorous
physical activity per day, metabolic equivalent tasks (METs), and MET-minutes and MET-hours per
week. As there was substantial heterogeneity for the methods and reporting of both CRF and
physical activity, we used the J-correction factor for an unbiased estimate of the standard mean
difference (SMD) between youths with and without diabetes.28
Risk-of-Bias Assessment
We evaluated the internal validity of included studies using a modified version of a risk-of-bias tool
used in a previous meta-analysis of cross-sectional studies of physical activity for youths living with
chronic diseases.19 This risk-of-bias tool consists of several domains specific to measurements of
physical activity and CRF, including type of measurement (objective vs subjective), time of year for
data collection, data reduction, criteria used to define a valid measurement, and reporting of
confounding. Each domain was judged as yes or no and given a score of 1 or 0 for the presence or

absence of each potential source of bias. The overall risk-of-bias score was based on the responses to
individual domains.
Statistical Analysis
The primary outcomes for the meta-analyses were SMDs in physical activity and CRF. When at least
2 studies of similar populations, methods, and outcomes were available, inverse variance–weighted
random-effects meta-analyses were performed to calculate SMDs with 95% CIs between youths
with and without diabetes. We initially calculated SMDs with 95% CIs for all studies that met the
inclusion criteria. Absolute mean differences with 95% CIs were calculated for differences in the main
outcomes for subgroup analyses of studies that used identical tools to quantify outcome measures
between youths with and without diabetes. The range of differences and the inconsistency index (I2)
were both used to quantify heterogeneity among studies.28,29 Subgroup analyses were performed
to determine if differences in outcomes were influenced by (1) the methods used to assess the main
outcomes of interest (direct vs indirect measures for CRF and subjective vs objective measures for
physical activity) and (2) the type of control population studied (healthy weight vs weight matched).
We also performed sensitivity analyses by removing extreme outliers. Funnel plots were used to
investigate publication bias using the Egger test and visual inspection to assess plot asymmetry for
all 4 meta-analyses. The meta-analyses were conducted using the general meta and metafor
packages30 in RStudio, version 2022.07.2 + 576 and R, version 4.2.2 (R Project for Statistical
Computing).
Results
The search results yielded 7857 unique individual citations, which were included in the preliminary
screen. At the end of the title and abstract screen, 7400 articles were excluded, 52 were included,
and 405 were in conflict across the 3 reviewers. There was a 94.8% agreement rate among the
reviewers for the title and abstract screen. The 405 articles with conflicting scores were resolved by
the 3 reviewers and 1 author (J.M.) to determine consensus for eligibility for full-article screening and
data extraction. After all the conflicts were resolved, 130 articles were included for the full-article
screen, and 54 studies were included for data extraction (eFigure 1 in Supplement 1).16-18,20,31-80
Details for each individual study are presented in eTables 2 to 5 in Supplement 1. For all 4 meta-
analyses, cases and controls were similar in age and sex (Table 1), with limited data available for race
and ethnicity across all studies (eTables 6 and 7 in Supplement 1).
Table 1. Studies Included in the Systematic Review and Meta-Analysis
T2D and CRFa T1D and CRFb T2D and PAc T1D and PAd
Cases Controls Cases Controls Cases Controls Cases Controls
No. of participants 286 469 1018 1064 442 791 3209 8993
Age, median (range), y 15.1 15.1 14.1 13.5 15.2 14.8 14.0 13.6
(12.9-16.4) (12.5-16.2) (10.5-16.2) (10.1-16.0) (12.9-16.4) (12.5-16.0) (7.4-16.0) (7.3-16.3)
BMI, median (range) 34.3 26.6 21.3 21.43 31.9 24.9 20.78 20.32
(25.3-42.5) (20.3-35) (18.0-31.1) (17-32.9) (25.3-35.0) (21.0-32.3) (16.6-24.6) (17.0-32.9)
Sex, No. (%)
Girls 161 (56.2) 277 (59.1) 465 (45.7) 529 (49.7) 301 (68) 464 (59) 1653 (51.6) 4559 (50.7)
Boys 125 (43.8) 192 (40.9) 553 (54.3) 535 (50.3) 141 (32) 327 (41) 1550 (48.4) 4434 (49.3)
V̇o2peak, mean (SD), mL/kg/min 20.6 (3.5) 25.1 (5.4) 36.9 (5.3) 40.2 (5.9) NA NA NA NA
MVPA, median (range), min/d NA NA NA NA 30.4e 53.4e 54.6 73.7
(42.4-82.9) (53.4-114.0)
b
Abbreviations: BMI, body mass index (weight in kilograms divided by height in meters Twenty-two studies.18, 34, 38-40, 44-46, 48, 50, 51, 53, 56, 58, 65, 67, 69, 72, 73, 75, 77, 78
squared); CRF, cardiorespiratory fitness; MVPA, moderate to vigorous physical activity; c
Nine studies.16,17,35,44,55,61,66,71,76
NA, not applicable; PA, physical activity; T1D, type 1 diabetes; T2D, type 2 diabetes; d
Thirty-one studies.18, 33, 34, 36, 37, 39-44, 47, 48, 52, 54, 55, 57-60, 64-66, 70, 73-75, 78
V̇o2peak, peak oxygen consumption.
e
a MVPA reported in minutes per day in only 1 study.44
Nine studies.16,17,35,44,46,49,61,72,79

Among the 55 studies included in data extraction, 9 studies (755 participants, including 286
cases [median (range) age, 15.1 (12.9-16.4) years; 161 girls (56.2%); 125 boys (43.8%)] and 469
controls [median (range) age, 15.1 (12.5-16.2) years; 277 girls (59.1%); 192 boys (40.9%)]) met the
eligibility criteria for the outcome of CRF for youths with T2D,16,17,35,44,46,49,61,72,79 and 22 studies (38
unique comparisons; 2082 participants; 1018 cases [median (range) age, 14.1 (10.5-16.2) years; 465
girls (45.7%); 553 boys (54.3%)] and 1064 controls [median (range) age, 13.5 (10.1-16.0) years; 529
girls (49.7%); 535 boys (50.3%)]) met the eligibility criteria for the outcome of CRF for youths with
T1D18, 34, 38-40, 44-46, 48, 50, 51, 53, 56, 58, 65, 67, 69, 72, 73, 75, 77, 78 (Table 1). Mean (SD) V̇o2peak values from
laboratory-based studies were 20.7 (3.5) mL/kg/min for youths with T2D (44.6% lower than controls
with healthy weight and without diabetes and 17.4% for weight-matched controls) and 36.9 (5.3)
mL/kg/min for youths with T1D (8.3% lower than controls without diabetes) (Figure 1). The random-
effects meta-analysis revealed that youths with T2D displayed significantly lower CRF compared with
controls without diabetes (SMD, −1.06; 95% CI, −1.57 to −0.56; I2 = 84%; 9
studies16,17,35,44,46,49,61,72,79; 755 participants; 286 cases) (Figure 2A). When data were restricted to
studies with laboratory-based measures of V̇o2peak, youths with T2D displayed significantly lower
CRF compared with controls without diabetes (mean difference, −8.76 mL/kg/min; 95% CI, −12.7 to
−4.9 mL/kg/min; I2 = 82%; 8 studies16,17,35,44,46,49,72,79; 575 participants).
The random-effects meta-analysis revealed that CRF was also lower in youths with T1D
compared with controls without diabetes (SMD, −0.39; 95% CI, −0.70 to −0.09; I2 = 89%; 22
studies18, 34, 38-40, 44-46, 48, 50, 51, 53, 56, 58, 65, 67, 69, 72, 73, 75, 77, 78; 2082 participants; 1018 cases)
(Figure 2B). Restricting the analysis to laboratory-based measures of CRF did not change the
estimate of the difference between youths with T1D and controls without diabetes (mean difference,
−3.9 mL/kg/min; 95% CI, −6.3 to −1.6 mL/kg/min; I2 = 68%; 13 studies18,34,40,45,50,53,56,65,67,73,75,77,78;
917 participants). Subgroup analyses of studies of youths with T2D revealed that the differences in
CRF were lower for controls without diabetes who had obesity (SMD, −0.75; 95% CI, −1.15 to −0.35;
I2 = 77%; 8 studies17,35,44,46,49,61,72,79; 593 participants) compared with studies with controls who
had a healthy weight (SMD, −2.10; 95% CI, −2.74 to −1.47; I2 = 77%; 7 studies16,17,35,46,49,72,79; 328
participants). Subgroup analyses restricted to youths with T1D with a healthy weight revealed that
CRF was lower compared with controls with a healthy weight and without diabetes (SMD, −0.75;
95% CI, −1.09 to −0.41; I2 = 86%; 15 studies18, 34, 39, 48, 50, 51, 53, 56, 58, 65, 72, 73, 75, 77, 78; 1295 participants).
Only 2 studies46,72 performed in youths with T1D who had obesity showed no differences in CRF
compared with controls without diabetes.
Figure 1. Differences in Peak Oxygen Consumption (V̇o2peak) Between

Youths Without Diabetes and Youths With Type 1 Diabetes (T1D)
and Type 2 Diabetes (T2D)
50
40
Vo2peak, mL/kg/min
30
20
10
0
T2D Control Control with T1D Control
with obesity healthy weight
Group
The bars indicate the means; whiskers indicate SDs.

Of the 55 studies that met eligibility for data extraction, 9 studies (10 unique comparisons; 1233
participants, including 442 cases [median (range) age, 15.2 (12.9-16.4) years; 301 girls (68%); 141 boys
(32%)] and 791 controls [median (range) age, 14.8 (12.5-16.0) years; 464 girls (59%); 327 boys
(41%)]) met eligibility for the outcome of physical activity for youths with T2D,16,17,35,44,55,61,66,71,76
and 31 studies (12 196 participants, including 3203 cases [median (range) age, 14.0 (7.4-16.0) years;
1653 girls (51.6%); 1550 boys (48.4%)] and 8993 controls [median (range) age, 13.6 (7.3-16.3) years;
4559 girls (50.7%); 4434 boys (49.3%)]) met eligibility for the outcome of physical activity for
youths with T1D18-20, 33, 34, 36, 37, 39-44, 47, 48, 52, 54, 55, 57-60, 62, 64-66, 70, 73-75, 78 (Table 1). Random-effects
Figure 2. Differences in Cardiorespiratory Fitness Between Youths With Diabetes and Controls
A Type 2 diabetes
Experimental Control
Mean (SD) Mean (SD) Standard mean
Source difference Total difference Total difference (95% Cl) Weight, %
Yardley et al,79 2015 24.30 (6.30) 23 29.13 (8.22) 38 –0.63 (–1.16 to –0.10) 12.0
Bjornstad et al,35 2016 20.40 (4.20) 37 27.81 (7.90) 74 –1.07 (–1 .49 to –0.65) 12.9
Hodges et al,49 2018 15.70 (6.40) 12 25.88 (7.19) 32 –1.43 (–2.16 to –0.70) 10.3
Miranda-Lora et al,61 2021 72.30 (24.70) 97 74.10 (23.70) 83 –0.07 (–0.37 to 0.22) 13.8
Wittmeier et al,17 2012 38.90 (7.90) 27 44.56 (6.55) 110 –0.82 (–1.26 to –0.39) 12.8
Tommerdahl et al,72 2021 21.90 (4.20) 59 33.51 (10.23) 90 –1.38 (–1.74 to –1.01) 13.4
Gusso et al,46 2008 20.30 (2.00) 8 31.50 (7.03) 20 –1.78 (–2.74 to –0.82) 8.4
Faulkner et al,44 2014 20.20 (3.50) 9 23.20 (4.00) 10 –0.76 (–1.70 to 0.18) 8.6
Nadeau et al,16 2009 21.80 (4.20) 14 40.40 (9.90) 12 –2.44 (–3.49 to –1.39) 7.7
Total (95% CI) 286 469 –1.06 (–1.57 to –0.56] 100
Heterogeneity: τ2 = 0.3150; χ28 = 51.30; P <.01; I2 = 84%
–4 –2 0 2 4
Standard mean difference (95% Cl)
B Type 1 diabetes
Experimental Control
Mean (SD) Mean (SD) Standard mean
Source difference Total difference Total difference (95% Cl) Weight, %
Trigona et al,73 2010 45.50 (1.27) 32 48.70 (0.99) 42 –2.83 (–3.49 to –2.17) 4.5
Jahn et al,50 2022 37.90 (2.00) 16 40.20 (1.80) 14 –1.17 (–1.96 to –0.39) 4.1
Komatsu et al,53 2005 41.57 (7.68) 72 51.12 (9.94) 46 –1.10 (–1.50 to –0.70) 5.1
Wu et al,78 2021 35.48 (8.72) 48 44.43 (8.29) 19 –1.03 (–1.59 to –0.47) 4.7
Nadeau et al,65 2010 31.50 (7.60) 12 40.40 (9.90) 12 –0.97 (–1.83 to –0.12) 3.9
Jegdic et al,51 2013 601.30 (86.10) 100 672.10 (60.60) 100 –0.95 (–1.24 to –0.65) 5.4
Heyman et al,48 2005 2.28 (0.09) 17 2.37 (0.13) 18 –0.78 (–1.47 to –0.09) 4.4
Nguyen et al,18 2015 38.50 (5.80) 8 42.70 (4.30) 8 –0.78 (–1.80 to 0.25) 3.4
Riddell et al,67 2000 41.75 (2.91) 16 44.26 (3.76) 14 –0.73 (–1.48 to 0.01) 4.2
Abreu de Lima et al,40 2017 38.38 (7.54) 45 42.44 (4.65) 119 –0.72 (–1.08 to –0.37) 5.2
Bjornstad et al,34 2015 31.50 (6.30) 69 36.20 (7.90) 13 –0.71 (–1.31 to –0.11) 4.6
Tommerdahl et al,72 2021 28.07 (7.13) 270 33.51 (10.20) 270 –0.62 (–0.79 to –0.44) 5.5
Lukács et al,56 2012 40.13 (6.42) 106 43.28 (7.28) 130 –0.45 (–0.71 to –0.19) 5.4
Cuenca-García et al,39 2012 90.70 (34.30) 60 99.50 (45.90) 37 –0.22 (–0.63 to 0.19) 5.1
Gusso et al,46 2008 31.60 (2.00) 12 31.50 (7.03) 20 0.02 (–0.70 to 0.73) 4.3
Maggio et al,58 2010 195.00 (6.90) 48 193.70 (8.90) 85 0.16 (–0.20 to 0.51) 5.2
Woo et al,77 2010 41.01 (8.27) 10 39.17 (5.35) 10 0.25 (–0.63 to 1.13) 3.8
Galassetti et al,45 2006 39.00 (10.46) 12 36.00 (7.14) 12 0.32 (–0.48 to 1.13) 4.0
Van Ryckeghem et al,75 2021 43.80 (9.90) 19 40.50 (8.70) 19 0.35 (–0.29 to 0.99) 4.5
Correa de Jesus et al,38 2019 2.09 (0.54) 10 1.87 (0.50) 12 0.41 (–0.44 to 1.26) 3.9
Faulkner et al,44 2014 33.00 (7.60) 20 23.20 (4.00) 10 1.43 (0.58 to 2.28) 3.9
Rosa et al,69 2009 40.50 (2.50) 16 33.43 (3.72) 54 2.00 (1.35 to 2.66) 4.5
Total (95% CI) 1018 1064 –0.39 (–0.70 to –0.09) 100
Heterogeneity: τ2 = 0.4307; χ 2 = 189.48; P <.01; I2 = 89%
21
–4 –2 0 2 4
The boxes and whiskers indicate standardized mean differences and 95% CIs.

models revealed that daily physical activity was not different among youths with T2D (SMD, −0.56;
95% CI, –1.28 to 0.16; I2 = 91%; 9 studies16,17,35,44,55,61,66,71,76; 1233 participants; 442 cases)
(Figure 3A) compared with controls without diabetes but was marginally lower among youths with
T1D (SMD, −0.29; 95% CI, –0.46 to −0.11; I2 = 89%; 31 studies18-20, 33, 34, 36, 37, 39-44, 47, 48, 52, 54, 55, 57-60,
62, 64-66, 70, 73-75, 78
; 12 196 participants; 3203 cases) (Figure 3B) compared with controls without
diabetes. Analyses restricted to studies with objective measures found that physical activity was
lower in youths with T2D (SMD, −0.71; 95% CI, −1.36 to −0.05; I2 = 23%; 3 studies17,44,66; 332
participants) and T1D (SMD, −0.67; 95% CI, −1.17 to −0.17; I2 = 93%; 13
studies18,20,39,42,44,58,59,65,66,70,73,78 [Elmesmari et al42 used 2 different measures for the same
study]; 1357 participants) compared with controls without diabetes (eFigures 2 and 3 in
Supplement 1).
To determine the overall quality of the studies in this area, we summarized the distribution of
bias for studies of CRF and physical activity among youths with T2D and T1D (Table 2). For all studies
combined, 78% to 89% of studies provided information on the recruitment process for the
comparison population. Only 22% to 36% of studies described the timing of the measurements of
physical activity, 22% to 39% of all studies described methods to address potential sources of bias,
14% to 44% adjusted for confounding, and 0% to 22% presented sex-disaggregated data. For
studies of youths with T2D, the majority (8 of 9 studies17,35,44,46,49,61,72,79) relied on laboratory-based
measures of CRF. For studies of physical activity among youths with T2D, only 3 of 9 studies17,44,66
used objective measures, and none of the studies provided definitions for a valid assessment of
physical activity or described the season during which data were collected. For studies of CRF among
youths with T1D, the majority relied on laboratory-based maximal tests to exhaustion (21 of 23
studies18, 34, 38-40, 44-46, 48, 50, 53, 58, 65, 67-69, 72, 73, 77, 78), but only some reported criteria for achieving
maximal exertion.18, 34, 39, 40, 44, 45, 48, 53, 58, 68, 72, 73, 77, 78 For studies of physical activity among youths
with T1D, 13 of 31 used objective measures18,20,39,42,44,58,59,65,66,70,73,78 (Elmesmari et al42 used 2
different measures for the same study) and 11 of 13 studies provided definitions for a valid assessment
of physical activity.18,20,39,42,44,58,59,65,70,73 Funnel plots revealed no publication bias for the 4 meta-
analyses presented above (eFigures 4-7 in Supplement 1).
Discussion
The main finding from this systematic review and meta-analysis was that youths with T2D had very
low CRF, with values 17% to 45% lower than in age-matched controls without diabetes, and modestly
lower daily physical activity. The mean V̇o2peak for youths with T2D (20.7 mL/kg/min) was well below
normative values for adolescents and established thresholds for optimal cardiometabolic risk
profiles.2,81-83 Among youths with T1D, both CRF and physical activity were modestly lower
compared with age-matched controls without diabetes. The differences in physical activity between
adolescents with diabetes and controls were more evident when objective measures were used to
quantify physical activity. Finally, most studies were poorly designed and did not follow current
reporting guidelines, which may explain the high heterogeneity of effect sizes across studies.
Low CRF was associated with increased cardiometabolic risk factor clustering in adolescence
and cardiovascular disease–related morbidity in adulthood.2,10,84,85 The mean V̇o2peak derived from
direct laboratory-based measures for youths with T2D was 20.7 mL/kg/min, a value approximately
45% lower than in controls with a healthy weight and without diabetes. This deficit was largely
mediated by excess body weight, as differences with weight-matched controls were approximately
17%. In contrast, adolescents with T1D had a mean V̇o2peak of 36.9 mL/kg/min, a value approximately
10% lower than controls without diabetes. These levels of CRF for youth with T2D are well below
mean values for representative samples of adolescents in the US,81 Canada,82 and Europe83 and
below the minimum threshold at which the odds of cardiometabolic risk factor clustering increase 2-
to 4-fold (<41.6 mL/kg/min for boys; <34.6 mL/kg/min for girls).2 These deficits in CRF in youths living
with diabetes may therefore contribute partially to the cardiovascular disease risk factor clustering

Figure 3. Differences in Daily Physical Activity Between Youths With Diabetes and Controls
A Type 2 diabetes
Experimental Control Standard mean

Source Mean (SD) difference Total Mean (SD) difference Total difference (95% Cl) Weight, %
Shaibi et al,71 2008 0.60 (0.20) 13 1.40 (0.30) 13 –3.04 (–4.22 to –1.86) 8.1
Lobelo et al,55 2010 4.82 (0.63) 90 5.45 (0.53) 173 –1.11 (–1.38 to –0.84) 12.2
Wittmeier et al,17 2012 4475.00 (2382.00) 27 7269.46 (2916.92) 110 –0.98 (–1.42 to –0.55) 11.7
O’Neill et al,66 2012 4959.00 (3474.00) 49 6870.00 (3521.00) 127 –0.54 (–0.88 to –0.21) 12.0
Faulkner et al,44 2014 9.10 (7.80) 9 17.10 (18.20) 10 –0.53 (–1.46 to 0.39) 9.4
West et al,76 2009 4.80 (6.30) 106 5.60 (6.30) 189 –0.13(–0.36 to 0.11) 12.3
Nadeau et al,16 2009 64.00 (18.80) 14 64.00 (11.20) 12 0.00 (–0.77 to 0.77) 10.2
Bjornstad et al,35 2016 64.10 (16.70) 37 61.09 (10.19) 74 0.24 (–0.16 to 0.63) 11.8
Miranda-Lora et al,61 2021 4.20 (5.20) 97 2.60 (4.60) 83 0.32 (0.03 to 0.62) 12.2
Total (95% CI) 442 791 –0.56 (–1.28 to 0.16) 100
Heterogeneity: τ2 = 0.6662; χ28 = 91.92; P <.01; I2 = 91%
–5 –4 –3 –2 –1 0 1 2 3 4
B Type 1 diabetes
Experimental Control Standard mean
Source Mean (SD) difference Total Mean (SD) difference Total difference (95% Cl) Weight, %
Maggio et al,58 2010 497.00 (54.00) 48 668.00 (35.00) 85 –3.97 (–4.57 to –3.37) 2.7
Elmesmari et al,19 2017 8201.00 (3231.00) 20 10 959.00 (2024.00) 20 –1.00 (–1.66 to –0.34) 2.6
Elmesmari et al,19 2017 1.70 (0.70) 20 2.20 (0.40) 20 –0.86 (–1.51 to –0.21) 2.6
Abreu de Lima et al,40 2017 68.78 (34.11) 45 118.85 (68.69) 119 –0.81 (–1.17 to –0.46) 3.5
Heyman et al,48 2005 0.70 (1.00) 19 1.40 (1.00) 19 –0.69 (–1.34 to –0.03) 2.6
Wu et al,78 2021 2.09 (0.41) 48 2.41 (0.60) 19 –0.67 (–1.22 to –0.13) 2.9
Lobelo et al,55 2010 5.20 (0.30) 384 5.45 (0.53) 173 –0.65 (–0.83 to –0.46) 3.9
Faulkner et al,44 2014 8.90 (10.00) 20 17.10 (18.20) 10 –0.60 (–1.38 to 0.17) 2.3
Marshall et al,59 2021 82.90 (37.20) 23 114.00 (72.10) 17 –0.56 (–1.20 to 0.08) 2.6
Särnblad et al,70 2005 505.00 (145.00) 13 572.00 (125.00) 22 –0.49 (–1.19 to 0.20) 2.5
Trigona et al,73 2010 567.10 (313.15) 32 694.90 (291.96) 42 –0.42 (–0.88 to 0.05) 3.2
Hensel et al,47 2016 1.70 (0.80) 40 2.00 (0.70) 44 –0.40 (–0.83 to 0.04) 3.3
Valerio et al,74 2007 2.80 (2.50) 138 3.60 (1.90) 269 –0.38 (–0.58 to –0.17) 3.9
Nguyen et al,18 2015 45.90 (16.30) 8 53.80 (28.10) 8 –0.33 (–1.31 to 0.66) 1.8
Kummer et al,54 2014 5.50 (4.80) 629 7.00 (7.10) 6813 –0.22 (–0.30 to –0.13) 4.0
Joseph et al,52 2020 2.20 (0.50) 62 2.30 (0.50) 61 –0.20 (–0.55 to 0.16) 3.5
Mutlu et al,31 2017 20.92 (6.44) 41 22.17 (6.50) 38 –0.19 (–0.63 to 0.25) 3.2
Czenczek-Lewandowska 254.80 (158.70) 215 268.30 (83.70) 115 –0.10 (–0.32 to 0.13) 3.8
et al,20 2019
Mohammed et al,62 2014 3.40 (1.66) 66 3.50 (1.87) 54 –0.06 (–0.42 to 0.30) 3.5
Mutlu et al,64 2015 2.65 (0.90) 47 2.68 (0.68) 55 –0.04 (–0.43 to 0.35) 3.4
Lukács et al,57 2016 2.56 (1.49) 106 2.60 (1.29) 130 –0.03 (–0.29 to 0.23) 3.7
Cohen et al,37 2021 3.55 (3.86) 40 3.60 (4.90) 18 –0.01 (–0.57 to 0.54) 2.9
Nadeau et al,65 2010 64.00 (7.00) 12 64.00 (11.00) 12 0.00 (–0.80 to 0.80) 2.2
Cuenca-García et al,39 2012 26 995.10 (11 668.60) 60 26 477.10 (10 157.60) 37 0.05 (–0.36 to 0.46) 3.3
Bishop et al,33 2014 5.00 (1.80) 300 4.90 (1.70) 100 0.06 (–0.17 to 0.28) 3.8
O’Neill et al,66 2012 7413.00 (3415.00) 304 6870.00 (3521.00) 127 0.16(–0.05 to 0.36) 3.9
Fainardi et al,43 2011 7.01 (6.52) 129 5.92 (5.31) 214 0.19 (–0.03 to 0.41) 3.8
Van Ryckeghem et al,75 2021 2.64 (0.65) 19 2.47 (0.45) 19 0.30 (–0.34 to 0.94) 2.6
Massin et al,60 2005 41.83 (22.89) 127 34.64 (16.27) 200 0.38 (0.15 to 0.60) 3.8
Heyman et al,48 2005 2.10 (0.30) 17 2.00 (0.20) 18 0.39 (–0.28 to 1.06) 2.5
Bjornstad et al,34 2015 64.00 (13.00) 69 58.00 (10.00) 13 0.47 (–0.13 to 1.07) 2.8
Francisco dos Santos 17.61 (10.27) 32 12.00 (9.00) 30 0.57 (0.06 to 1.08) 3.0
Haber et al,41 2022
Caferoğlu et al,36 2016 70 72 0.0
Total (95% CI) 3203 8993 –0.29 (–0.46 to –0.11) 100
Heterogeneity: τ2 = 0.1938; χ 2 = 286.76; P <.01; I2 = 89%
31
–5 –4 –3 –2 –1 0 1 2 3 4
Heyman et al48 had 2 control groups and was entered twice in the meta-analysis. Elmesmari et al42 used 2 different measures for the same study. The boxes and whiskers indicate
standardized mean differences and 95% CIs.

reported in adolescence31 and excessive cardiovascular disease–related morbidity observed in young

adulthood.86,87 These data also support clinical practice guidelines and expert opinions that CRF is
impaired in youths with both T1D and T2D.11-15
Engaging in daily physical activity is a cornerstone in the management of pediatric diabetes.11-15
Despite the widely recognized benefits of physical activity, very few systematic reviews with meta-
analyses have been published describing daily physical activity levels in youths living with diabetes.
One meta-analysis of cross-sectional studies of adolescents with chronic diseases found no
difference in moderate to vigorous physical activity among youths with T1D compared with a control
population.17 With an additional 5 studies,20,42,47,66,78 we found a very small difference in daily
physical activity among youths with T1D compared with peers without diabetes. Fewer studies have
documented levels of daily physical activity among youths with T2D; however, they consistently
revealed very low levels of daily physical activity compared with expert recommendations
(approximately 7000 steps per day and approximately 35 minutes of moderate to vigorous physical
activity daily).17,88-90 Compared with youths without diabetes, the differences in daily physical
activity were greater for youths with T2D compared to youths with T1D. The large deficits in daily
physical activity among youths with T2D may contribute to the lower CRF reported here, reinforcing
the need for novel approaches to support physical activity behaviors for adolescents with T2D.
Limitations
This systematic review is, to our knowledge, the largest and most comprehensive description of CRF
and physical activity levels among youths living with diabetes to date. Although we applied strict
criteria for study inclusion and published the methods a priori, there are several limitations to
consider. First, the quality of a meta-analysis depends on the quality of studies included. One of the
main objectives of this systematic review was to determine the quality of studies in this area. As the
majority of studies did not report key methodological considerations for valid measures of physical
activity and CRF, consistently describe strategies to address bias (including weight status), or present
sex-specific results, the risk of bias was high in most studies. Therefore, the point estimates provided
here should be interpreted with caution. Second, the external validity or transferability of the results
is also limited by several factors, including failure to report race and ethnicity; socioeconomic status;
Table 2. Summary of Risk Scores Across Different Populations and Outcomes
No. of studies (%)

T1D T2D
Variable PA (n = 31) CRF (n = 22) PA (n = 9) CRF (n = 9)
Objective/direct 14 (45.2) 20 (90.9) 4 (44.4) 8 (88.9)
Sample recruitment 27 (87.1) 18 (81.8) 8 (88.9) 7 (77.8)
Time of year 11 (35.5) 1 (4.5) 2 (22.2) 0
Place of recruitment 27 (87.1) 16 (72.7) 7 (77.8) 7 (77.8)
Sample description, mean (maximum score = 3) 2.84 2.77 2.89 2.90
Attrition, mean (maximum score = 2) 1.41 1.41 1.44 1.5
Data collection and reduction, mean (maximum 2.63 3.72 1.44 3.20
score = 5)
PA intensity/maximum criteria definition 19 (61.2) 16 (72.7) 3 (33.3) 5 (55.6)
Results (No. actually analyzed) 31 (100) 22 (100) 8 (88.9) 9 (100)
Control recruitment described 23 (74.1) 15 (68.2) 8 (88.9) 7 (77.8)
Eligibility criteria described 20 (64.5) 19 (86.4) 5 (55.6) 8 (88.9)
Address bias 11 (35.5) 8 (36.4) 3 (33.3) 2 (22.2)
Report confounding 19 (61.2) 17 (77.2) 8 (88.9) 8 (88.9)
Adjust for confounding 4 (12.9) 4 (18.2) 3 (33.3) 4 (44.4)
Sex-disaggregated data 5 (16.1) 5 (22.7) 0 1 (11.1)
Ethnicity data, mean (maximum score = 3) 0.41 0.18 1.33 0.70 Abbreviations: CRF, cardiorespiratory fitness; PA,
physical activity; T1D, type 1 diabetes; T2D,
Total score, mean (maximum score = 25) 13.75 15.40 13.67 15.20
type 2 diabetes.

and, in most cases, sex-specific differences in CRF and physical activity within each population.
Structural factors that influence access, safety, and participation in physical activity are important
when studying differences in physical activity for youths of various racial and ethnic identities, who
are new immigrants, and who identify as female or nonbinary. Type 2 diabetes is more common
among American Indian, Black, and Hispanic youths91 and those living in low-income households92;
however, despite calls for reporting sex- and race and ethnicity–specific outcomes, these data are
largely absent from studies published to date. Finally, we did not include non-English publications or
studies within the gray literature in order to increase the feasibility of this review, and this may have
introduced selective reporting bias (eg, publication bias).
Conclusions
The findings of this systematic review and meta-analysis suggest that youths with T2D have
profoundly lower CRF and modestly lower objectively measured physical activity compared with
peers without diabetes. Deficits in CRF and objectively measured physical activity are also evident,
but less pronounced, among youths with T1D. These findings reinforce calls for novel interventions to
empower youths living with diabetes to engage in regular physical activity and increase their CRF.
ARTICLE INFORMATION
Accepted for Publication: December 22, 2023.
Published: February 23, 2024. doi:10.1001/jamanetworkopen.2024.0235
Open Access: This is an open access article distributed under the terms of the CC-BY License. © 2024 Steiman De
Visser H et al. JAMA Network Open.
Corresponding Author: Jonathan McGavock, PhD, Department of Pediatrics and Child Health, Faculty of Health
Sciences, University of Manitoba, 511 JBRC, Children’s Hospital Research Institute of Manitoba, 715 McDermot Ave,
Winnipeg, MB R3E 3P4, Canada (jmcgavock@chrim.ca).
Author Affiliations: Children’s Hospital Research Institute of Manitoba, Winnipeg, Manitoba, Canada (Steiman De
Visser, Fast, Brunton, Arevalo, McGavock); Neil John MacLean Library, Rady Faculty of Health Sciences, University
of Manitoba, Winnipeg, Manitoba, Canada (Askin); George & Fay Yee Centre for Healthcare Innovation, University
of Manitoba, Winnipeg, Manitoba, Canada (Rabbani, Abou-Setta); Department of Pediatrics and Child Health,
University of Manitoba, Winnipeg, Manitoba, Canada (McGavock); Diabetes Research Envisioned and
Accomplished in Manitoba (DREAM) Research Theme, Winnipeg, Manitoba, Canada (McGavock); Diabetes Action
Canada, Toronto, Ontario, Canada (McGavock).
Author Contributions: Dr McGavock had full access to all of the data in the study and takes responsibility for the
integrity of the data and the accuracy of the data analysis. Ms Steiman De Visser and Mr Fast contributed equally as
co–first authors.
Concept and design: Askin, McGavock.
Acquisition, analysis, or interpretation of data: All authors.
Drafting of the manuscript: McGavock.
Critical review of the manuscript for important intellectual content: All authors.
Statistical analysis: Steiman De Visser, Arevalo, Rabbani, Abou-Setta.
Obtained funding: McGavock.
Administrative, technical, or material support: Brunton, Abou-Setta, McGavock.
Supervision: Abou-Setta, McGavock.
Conflict of Interest Disclosures: None reported.
Funding/Support: This project was supported by Applied Public Health Chair and Obesity grant CPP-137910 from
the Canadian Institutes of Health Research and the DREAM Theme at the Children’s Hospital Research Institute of
Manitoba.

Role of the Funder/Sponsor: The funders had no role in the design and conduct of the study; collection,
management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and
decision to submit the manuscript for publication.
Data Sharing Statement: See Supplement 2.
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SUPPLEMENT 1.
eTable 1. Search Strategies and Results
eTable 2. Baseline Characteristics of Included Studies for Youth With Type 1 Diabetes and Cardiorespiratory Fitness
eTable 3. Baseline Characteristics of Included Studies for Youth With Type 1 Diabetes and Physical Activity
eTable 4. Baseline Characteristics of Included Studies for Youth With Type 2 Diabetes and Physical Activity
eTable 5. Baseline Characteristics of Included Studies for Youth With Type 2 Diabetes and Cardiorespiratory
Fitness
eTable 6. Ethnicity of Participants in Each Study of Youth With Type 2 Diabetes Within Studies That Reported It
eTable 7. Ethnicity of Participants in Each Study of Youth With Type 1 Diabetes
eFigure 1. Flow Chart Describing Search and Screening Results for Studies That Were Included in the Meta-Analysis
eFigure 2. Differences in Objectively Measured Physical Activity Between Youth With Type 2 Diabetes and
Controls
eFigure 3. Differences in Objectively Measured Physical Activity Between Youth With Type 1 Diabetes and Controls
eFigure 4. Funnel Plot Demonstrating No Publication Bias in Studies Examining Differences in Cardiorespiratory
Fitness Between Youth With Type 2 Diabetes and Controls
eFigure 5. Funnel Plot Demonstrating No Publication Bias in Studies Examining Differences in Cardiorespiratory
Fitness Between Youth With Type 1 Diabetes and Controls
eFigure 6. Funnel Plot Demonstrating No Publication Bias in Studies Examining Differences in Physical Activity
Between Youth With Type 2 Diabetes and Controls
eFigure 7. Funnel Plot Demonstrating No Publication Bias in Studies Examining Differences in Physical Activity
Between Youth With Type 1 Diabetes and Controls
SUPPLEMENT 2.
Data Sharing Statement

Cardiorespiratory Fitness and Physical Activity in Pediatric Diabetes - A Systematic Review and Meta Analysis

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Original Investigation | Pediatrics

Abstract Key Points

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JAMA Network Open. 2024;7(2):e240235. doi:10.1001/jamanetworkopen.2024.0235

Inclusion Criteria and Classification of Diabetes Type

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Outcomes of Interest and Subgroup Analyses

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Table 1. Studies Included in the Systematic Review and Meta-Analysis

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Figure 1. Differences in Peak Oxygen Consumption (V̇o2peak) Between

The bars indicate the means; whiskers indicate SDs.

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Experimental Control Standard mean

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reported in adolescence31 and excessive cardiovascular disease–related morbidity observed in young

Table 2. Summary of Risk Scores Across Different Populations and Outcomes

No. of studies (%)

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