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Mars On 2016
Mars On 2016
Effects of aerobic, resistance, and combined exercise training on insulin
resistance markers in overweight or obese children and adolescents: A
systematic review and meta-analysis
PII: S0091-7435(16)30342-5
DOI: doi: 10.1016/j.ypmed.2016.10.020
Reference: YPMED 4821
Please cite this article as: Marson Elisa Corrêa, Delevatti Rodrigo Sudatti, Prado Alexan-
dre Konig Garcia, Netto Nathalie, Kruel Luiz Fernando Martins, Effects of aerobic,
resistance, and combined exercise training on insulin resistance markers in overweight
or obese children and adolescents: A systematic review and meta-analysis, Preventive
Medicine (2016), doi: 10.1016/j.ypmed.2016.10.020
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Review Article
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resistance markers in overweight or obese children and adolescents: A
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systematic review and meta-analysis
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Elisa Corrêa Marson1
Rodrigo Sudatti Delevatti1,2
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Alexandre Konig Garcia Prado1,3
Nathalie Netto1
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Luiz Fernando Martins Kruel1
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Universidade Federal do Rio Grande do Sul. Exercise Research Laboratory.
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2
Faculdade Sogipa de Educação Física. Porto Alegre. RS, Brazil.
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Faculdade Cenecista de Osório. Osório. RS, Brazil
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Authors' Address:
Phone: 51 3308-5820.
E-mail addresses:
Abstract
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Objective: To assess the associations of aerobic, resistance, and combined
exercise with changes in insulin resistance, fasting glucose, and fasting insulin
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in children and adolescents who are overweight or obese.
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Data Searches: MEDLINE via Pubmed, Cochrane-CENTRAL, SPORTDiscus,
and LILACS.
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Study Selection: Randomized clinical trials of at least six weeks of duration
that evaluated the ability of exercise training to lower at least one of the
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following outcomes: insulin resistance-HOMA, fasting glucose, and fasting
insulin in children and/or adolescents classified as obese or overweight.
Data Extraction and analysis: Two independent reviewers extracted data and
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group minus control group) in the outcomes evaluated were analyzed using a
random effects model.
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analysis showed that physical training in general was not associated with a
reduction in fasting glucose levels compared to the control, but it was
associated with reductions in fasting insulin levels (-3.37Uu/ml; CI 95%,-
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5.16Uu/ml to -1.57Uu/ml; I², 54%, p = 0.003) and HOMA (-0.61; CI 95%, -1.19
to -0.02; I², 49%, p=0.040). In addition, each modality (aerobic, resistance, and
combined) was compared to the control group. Aerobic exercise was associated
with declines in fasting insulin levels (-4.52Uu/ml; CI 95%, -7.40 to -1.65; I²,
65%, p=0.002) and in HOMA (-1.33; 95% confidence interval, -2.47 to -0.18; I²,
73%, p=0.005).
Conclusions: Exercise training, especially aerobic training, is associated with
the reduction of fasting insulin levels and HOMA in children and adolescents
with obesity and overweight, and may prevent metabolic syndrome and type 2
diabetes.
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INTRODUCTION
Obesity in children and adolescents has been one of the major public
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health problems of the last century. Estimates show that about 170 million
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children worldwide are overweight and this prevalence is higher in low- and
middle-income countries (WHO, 2012). According to the World Health
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Organization (WHO), overweight and obesity are defined by an age-related BMI
greater than one and two standard deviations above the median of the WHO’s
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growth reference, respectively (WHO, 2016). Many cardiovascular risk factors
are associated with being overweight, such as higher blood pressure,
development of dyslipidemia, and insulin resistance. However, in obese
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One of the main factors related to obesity and being overweight, along
with insulin resistance, is a sedentary lifestyle in childhood and adolescence
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(Rennie et al., 2005). A study by Rey-López et al., (2008) highlighted the time
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that children spent watching television as a determining factor in weight gain, for
which physical exercise was the indicated therapeutic approach. Systematic
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reviews with meta-analyses showed the beneficial effects of exercise on lipid
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profile (Kelley and Kelley, 2007), blood pressure (Garcia-Hermoso et al., 2013),
glucose, and insulin levels (Garcia-Hermoso et al., 2014) for children and
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adolescents who are overweight or obese. However, evidence of the effect of
exercise on glucose metabolism (Garcia-Hermoso et al., 2014) focused only on
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aerobic exercise, although resistance training is also able to show different
benefits for children and adolescents (Faigenbaum and Myer, 2010) and higher
levels of muscular fitness are inversely associated with cardiometabolic
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adolescents (Artero et al., 2012). Besides that, only isolated insulinemic and
glycemic responses have been investigated, without consistent evidences of the
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METHODS
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search of the references from the studies found in the chosen databases was
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carried out. We only included articles that were already published in journals.
Theses and dissertations were excluded.
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There was no language restriction in the search criteria. Boolean
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operators ―OR‖ and ―AND‖ were used. In PubMed, the search was performed
using the MeSH terms and their synonyms. Related terms to MeSH were used
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in the other databases. The complete search strategy used for the PubMed
database is shown in the Electronic Supplementary Material (Table 1).
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Two independent reviewers (E.C.M and N.N) read the titles and abstracts
of all papers found, and independently read the full article if the paper met the
eligibility criteria. Disagreements were solved by consensus and discussion with
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Eligibility criteria
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Criteria for inclusion into the present study were: children and
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adolescents (until 19 years old) of both sexes, overweight or obese, and not
engaged in structured exercise for at least three months. Clinical trials should
have included at least six-week of intervention period. There were no
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Data extraction
Data extraction was performed by two independent reviewers (E.C.M and
N.N). Disagreements between the two reviewers about the conditions of the
studies were solved by a consensus meeting with the third reviewer (R.S.D).
For data extraction, a standardized form was used, composed of the following
items: author, population, intervention data, and outcomes. For each item, the
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and weekly duration, weekly frequency, intensity, number of set and repetitions,
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and rest interval between sets); Results (mean values and standard deviation of
the pre- and post-intervention, and the difference between the means).
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Study quality assessment (risk of bias)
Study quality assessment included adequate sequence generation,
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allocation concealment, blinding of outcomes assessors, use of intention-to-
treat analysis, and description of losses and exclusions. Studies without clear
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descriptions of an adequate sequence generation or how the allocation list was
concealed were considered not to have fulfilled these criteria. Quality
assessment was independently performed by two unblinded reviewers (E.C.M.
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(R.S.D).
The risk of bias was evaluated in the following form: high risk - when the
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reported or were not performed; low risk - when the methodological criteria were
performed appropriately; unclear risk - when there was no adequate description
of the criteria, making it difficult to evaluate it as high or low risk.
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Data analysis
For consideration in the statistical analysis, only studies which results
could be compared in three or more studies were included. Those results that
did not meet this standard were only described in the results. Some studies in
which the exercise group was associated with nutritional counseling, we
considered as control group the one that had nutritional counseling, because in
this cases, it provides a better control for physical exercise than that of the
group without any intervention.
The results were presented as mean difference weighted with confidence
intervals (CI) of 95%. Calculations were performed using a method of random
effects, adopting α = 0.05. Statistical heterogeneity of the intervention effects
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among the studies was assessed by using Cochran’s Q test and the
inconsistency by I2 test. Values above 25% and 50% were considered
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indicators of being moderate and high heterogeneity, respectively. All analysis
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were performed using Review Manager, version 5.3. A primary analysis was
performed with all studies (Exercise training (overview)) and sub-group
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analyses were carried out considering the training modalities (aerobic,
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resistance, and combined) used in the studies and average age of individuals
(≤12 and >12 years old).
RESULTS
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Studies description
The initial search resulted in 1853 studies, 78 of which were excluded as
duplicates, and 1721 articles of which the title and abstract were read. Of the 54
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articles analyzed in full, 18 studies met the eligibility criteria. The research and
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Tables 2 and 3.
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to 0.10mg/dl; I² = 81%, p for heterogeneity< 0.001) as compared with the
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control. However, physical training (Figure 4) was associated with a reduction in
fasting insulin of-3.37Uu/ml (CI 95%: -5.16Uu/ml to -1.57Uu/ml; I² = 54%, p for
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heterogeneity = 0.003) and in HOMA of -0.61 (CI 95%: -1.19to -0.02; I² = 49%,
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p for heterogeneity = 0.040) as compared with the control. The association
between physical training and changes in insulin resistance (HOMA) is
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summarized in Figure 5. MA
Aerobic exercise training
Aerobic exercise training (Figure 3) was not associated with
improvements in fasting plasma glucose (MD:-0.99mg/dl; CI 95%: -2.00mg/dl to
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compared with the control, but was associated with a reduction in fasting insulin
(Figure 4) levels of-4.52Uu/ml (CI 95%: -7.40Uu/ml to -1.69Uu/ml; I² = 65%, p
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for heterogeneity = 0.002; 10 studies, 244 individuals) and in HOMA of -1.33 (CI
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plasma glucose (Figure 3) (MD:0.33mg/dl; CI 95%: -0.98 mg/dl to 0.31 mg/dl; I²
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= 93%, p for heterogeneity < 0.001; 3 studies, 58 individuals) compared to
control. Regarding to fasting insulin, the combined exercise training was not
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associated with a reduction in fasting insulin (Figure4) (-2.48Uu/ml; CI 95%: -
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5.50Uu/ml to 0.54Uu/ml; I² = 52%, p for heterogeneity = 0.10; 4 studies, 75
individuals). As with the assessment of resistance training, the restricted
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number of studies with combined training and HOMA assessment made
statistical analysis for this outcome unfeasible.
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―Insert figure 3, 4, and 5‖
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years old) comparing to the effects in adolescents (>12 years old). In children,
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only a maintenance in fasting glucose was found (MD: 0.12 mg/dl; CI 95%: -
1.40 mg/dlto1.64 mg/dl; I² = 71%, p for heterogeneity = 0.03; 3studies,
47individuals). In fasting insulin, a reduction was found (MD: -4.73 Uu/ml; CI
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Other studies
Three studies were described only (Foschini et al., 2010; Inoue et al.,
2014; Tsang et al., 2009) and where subsequently considered inadequate for
statistical analysis as they present single characteristics of interventions, not
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found elsewhere in the study for this review. Two of these (Foschini et al., 2010;
Inoue et al., 2014) showed a reduction in insulinemic levels and insulin
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resistance. The study by Foschini et al., (2010) found a positive result in a
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combined training group periodization of wave form during 14 weeks, which did
not happened with a linear periodization. Inoue et al., (2014) showed reduction
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in insulinemic levels, glucose, and insulin resistance in two combined training
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models of one year duration (wave periodization and linear), which did not occur
with aerobic training alone. Tsang et al., (2009) did not find any changes in the
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outcomes after 27 weeks of Kung Fu or Taichi.
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DISCUSSION
The characteristics of the exercise training interventions were different
between studies. In terms of an aerobic training modality, the majority of the
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studies used a treadmill, cycle ergometer and elliptical trainer, with others
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studies using sports (Wong et al., 2008; Tsang et al., 2009), dancing games
(Murphy et al., 2009) and jump rope (Lee et al., 2010a). In these studies, the
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heart rate, maximal uptake oxygen, and by first ventilatory threshold. In terms of
resistance training, the majority of the studies used weight machines, with one
study using elastic bands and own body weight (Farpour et al., 2009). In these
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fasting insulin levels below the normal cut point of 15–20μU/ml (SBC, 2005). In
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children and adolescents, these high insulin levels are still able to maintain the
glycemia at suitable levels. This may explain the lack of association between
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physical training and glycemic reduction. For this reason, a focus on glycemic
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outcomes does not seem to be advisable in this population, which shows
increases in insulin levels preceded by increases in glycemic levels. Despite
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this important discussion about the sensibility of the outcomes and metabolic
status of the children and adolescents, the primary aim of this study was to
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analyze how the investigated outcomes were affected by exercise training
(overview) and by different training modalities.
Our findings related to fasting plasma glucose differ from the results of
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Hermoso et al., (2014) did not consider nutritional intervention or children and
adolescents who are overweight in their analysis, and therefore has less
heterogeneity when compared to the present study.
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reduction in fasting insulin levels, including duration of the sessions and great
energy expenditure. It is more usual to design an aerobic training regime with a
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focus on metabolic changes compared to resistance training, usually focused
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on musculoskeletal aspects, in children and adolescents. This is probably why
there are relatively few studies using resistance training in the assessment of
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fasting insulin levels; this is evidenced by the present study, which found only
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four studies, with a total of 58 individuals. In addition to this methodological
characteristic, lower insulin production results from lower resistance to this
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hormone, as a consequence, among other factors, of the anti-inflammatory
effect of exercise, which is very evident with aerobic training (Hayashino et al.,
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2014; Delevatti et al., 2015). These benefits might be obtained even without a
reduction in body fat (Goran et al., 2003), suggesting that these metabolic
improvements are not totally dependent on morphological changes.
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However, there are not enough data to perform a comparative analysis between
resistance and combined training. It is interesting to highlight that one of the
selected articles using resistance training (Davis et al., 2009b) did not find
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Faced by this worrying scene, our findings are promising, because the
prescription of aerobic training seems to be an effective alternative, reducing
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insulin levels to maintain glycemic homeostasis. Aiming to prevent problems in
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adulthood and to reduce health care costs, the practice of exercise training,
especially aerobic training, should be encouraged in schools and in other
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locations for children and adolescents.
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As physiological alterations associated with puberty may influence
glycemic metabolism, a sub-analysis for age was also performed. The findings
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were similar in the two analyses, the fasting insulin being reduced by means of
exercise training in children (≤12 years old) and adolescents (> 12 years old),
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without alterations in fasting glucose in both analyses. We were not able to
analyze HOMA results due to the small number of studies that analyzed only
children or adolescents.
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error in at least one of the analyzed items, which may have contributed to the
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CONCLUSIONS
In general, exercise training interventions for at least eight weeks are
associated with reductions in fasting insulin and HOMA levels. More specifically,
aerobic exercise training is associated with reductions in fasting insulin and
HOMA levels, whereas combined exercise training and resistance exercise
training are not associated with the evaluated metabolic outcomes. Exercise
training interventions are not associated with fasting glucose. Based on these
results, it seems likely that physical training could play an important role in
preventing or delaying metabolic syndrome and type 2 diabetes. We emphasize
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the need for future intervention studies investigating the effects of resistance
and combined training on insulin resistance markers in overweight or obese
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children and adolescents. It is important that future intervention studies have
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higher methodological quality, with adequate random sequence generation,
allocation concealment, and blinding of outcomes assessment, aiming to
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increase the internal validity and thus diminish the between-studies
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heterogeneity of future meta-analyses.
CONFLICT OF INTEREST STATEMENT
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The authors declare no conflict of interest associated with this manuscript.
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Eletronic Search
(n=1853)
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Records after
duplicates removes
(n=78)
Records excluded
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(n= 1721)
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- No variable of interest: n= 11
Studies included in
review
(n=18)
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Figure 3. Absolute changes in fasting glucose levels of individual studies of
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exercise training (all modalities, aerobic, resistance and combined exercise vs.
no intervention.
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Figure 5. Absolute changes in HOMA of individual studies of exercise training
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(all modalities) and aerobic exercise vs. no intervention
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of study gender Cointervention
participants
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1. Ackel et al. (2014) 72 16.4 ± 1.5 (F/M) Yes NR
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2. Davis et al. (2009a) 21 15.2± 1.1 (F) Yes 9
3. Davis et al. (2009b) 38 15.5 ± 1.0 (F/M) Yes 12
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4. Davis et al. (2011) 26 15.8 ± 1.1 (F) No 6
5. Farpour et al. (2009) 44 8.9 ± 1.5 (F/M) No 8
6. Foshini et al.(2010) 32 16.5 ± 1.7 (F/M) Yes N
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7. Inoue et al. (2014) 45 16.2 ± 1.3 (F/M) Yes 35
8. Karacabey (2009) 40 11.5 ±0,65 (M) No N
9. Kelly et al. (2004) 20 10.9 ± 0.4 (F/M) No 5
10. Lee et al. (2010a) 18 16.7 ± 0.6 (F) No N
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11. Lee et al. (2012) 42 14.8± 1.6 (M) Yes 3
12. Lee et al. (2013) 36 14.8±2.0 (F) Yes 6
13. Leite et al. (2013) 59 12.7 ± 1.7 (F) Yes 26
14. Meyer et al. (2006) 67 13.9 ± 2.2 (F/M) No 19
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(2006)
17. Tsang et al (2009) 19 13.1 ± 2.1 (F/M) No 1
18. Wong et al. (2008) 24 14±1.3 (M) No N
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duration number of
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study
participants
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1. Ackel et 27 weeks Aerobic (24) Aerobic: 3x/wk.60 min in VT1
al. (2014) Combined (24) Combined: 3x/wk. AERO: 60
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Leisure (24) min in VT1; RESISTANCE:
progressive training: 20–
15RM, 12–10RM, 6–8RM
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Leisure: Leisure activities
2. Davis et 16 weeks Resistance (9) Resistance: 2x/wk.60 min
al. (2009a) Combined (15) (intensity not related)
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Control (7) Combined: 2x/wk. AERO: 30
min; RESISTANCE: 30 min
(intensity not related)
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periodization modified its volume and
(12) intensity differently; however,
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their final values were
equivalent
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8. 12 weeks Aerobic (20) Aerobic: 3x/wk. 60 min, 50–
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Karacabey Control (20) 65%HRreserve
(2009)
9. Kelly et al. 8 weeks Aerobic (10) Aerobic: 4x/wk. 30–50 min,
(2004) Control (10) 50–90% VO2peak
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10. Lee et al. 12 weeks Aerobic (11) Aerobic: 4x/wk. 30–40 min,
(2010a) Control (7) 40–80% HRmax
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11. Lee et al. 12 weeks Aerobic (15) Aerobic: 3x/wk. 40-60 min
(2012) Resistance (16) (main part), 50–75% VO2peak
Control (11) Resistance: 3x/sem. First 4
weeks (1 or 2 sets of 8-12
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Participants could choose
between these activities and
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regular gym participation
17. Tsang et 27 weeks Kung Fu (11) Kung Fu: The group was
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al. (2009) Control: Tai Chi guided by a professional Kung
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(8) Fu teacher; classes 3x/wk, 40
min.
Control Tai Chi: The group
was guided by a professional
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in Tai Chi; classes 3x/wk, 40
min.
MA
18. Wong et 12 weeks Combined (12) Combined: 2x/wk. 45–62
al. (2008) Control (12) min, 50–85% HRmax
x/wk: times a week; VT1: first ventilatory threshold; AERO: aerobic; HRmax:
Maximum heart rate; RM: Maximum repetitions, VO2peak: Peak of oxygen
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uptake.
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HIGHLIGHTS
T
Childhood obesity is associated with high fasting insulin levels;
IP
Aerobic training is associated with reduction in insulin resistance;
R
Aerobic training is associated with reduction in fasting insulin.
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MA
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