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Original Contribution |

Exercise Dose and Diabetes Risk in Overweight and Obese Children:  A Randomized Controlled Trial FREE

Catherine L. Davis, PhD; Norman K. Pollock, PhD; Jennifer L. Waller, PhD; Jerry D. Allison, PhD; B. Adam Dennis, MD; Reda Bassali, MD; Agustín Meléndez, PhD; Colleen A. Boyle, PhD; Barbara A. Gower, PhD
[+] Author Affiliations

Author Affiliations: Departments of Pediatrics (Drs Davis, Pollock, Bassali, and Boyle), Biostatistics (Dr Waller), Radiology (Dr Allison), and Medicine (Dr Dennis), Medical College of Georgia, Augusta; School of Physical Activity and Sports Sciences (National Institute of Physical Education), Polytechnic University of Madrid, Madrid, Spain (Dr Meléndez); and Department of Nutrition Sciences, University of Alabama, Birmingham (Dr Gower).


JAMA. 2012;308(11):1103-1112. doi:10.1001/2012.jama.10762.
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Published online

Context Pediatric studies have shown that aerobic exercise reduces metabolic risk, but dose-response information is not available.

Objectives To test the effect of different doses of aerobic training on insulin resistance, fatness, visceral fat, and fitness in overweight, sedentary children and to test moderation by sex and race.

Design, Setting, and Participants Randomized controlled efficacy trial conducted from 2003 through 2007 in which 222 overweight or obese sedentary children (mean age, 9.4 years; 42% male; 58% black) were recruited from 15 public schools in the Augusta, Georgia, area.

Intervention Children were randomly assigned to low-dose (20 min/d; n = 71) or high-dose (40 min/d; n = 73) aerobic training (5 d/wk; mean duration, 13 [SD, 1.6] weeks) or a control condition (usual physical activity; n = 78).

Main Outcome Measures The prespecified primary outcomes were postintervention type 2 diabetes risk assessed by insulin area under the curve (AUC) from an oral glucose tolerance test, aerobic fitness (peak oxygen consumption [V. O2]), percent body fat via dual-energy x-ray absorptiometry, and visceral fat via magnetic resonance, analyzed by intention to treat.

Results The study had 94% retention (n = 209). Most children (85%) were obese. At baseline, mean body mass index was 26 (SD, 4.4). Reductions in insulin AUC were larger in the high-dose group (adjusted mean difference, −3.56 [95% CI, −6.26 to −0.85] × 103 μU/mL; P = .01) and the low-dose group (adjusted mean difference, −2.96 [95% CI, −5.69 to −0.22] × 103 μU/mL; P = .03) than the control group. Dose-response trends were also observed for body fat (adjusted mean difference, −1.4% [95% CI, −2.2% to −0.7%]; P < .001 and −0.8% [95% CI, −1.6% to −0.07%]; P = .03) and visceral fat (adjusted mean difference, −3.9 cm3 [95% CI, −6.0 to −1.7 cm3]; P < .001 and −2.8 cm3 [95% CI, −4.9 to −0.6 cm3]; P = .01) in the high- and low-dose vs control groups, respectively. Effects in the high- and low-dose groups vs control were similar for fitness (adjusted mean difference in peak V. O2, 2.4 [95% CI, 0.4-4.5] mL/kg/min; P = .02 and 2.4 [95% CI, 0.3-4.5] mL/kg/min; P = .03, respectively). High- vs low-dose group effects were similar for these outcomes. There was no moderation by sex or race.

Conclusion In this trial, after 13 weeks, 20 or 40 min/d of aerobic training improved fitness and demonstrated dose-response benefits for insulin resistance and general and visceral adiposity in sedentary overweight or obese children, regardless of sex or race.

Trial Registration clinicaltrials.gov Identifier: NCT00108901

Figures in this Article

Child obesity and overweight are epidemic in US children.1 A third of elementary school–aged children are overweight or obese.2 Childhood obesity is associated with a number of adverse conditions formerly thought to occur only in adults, including type 2 diabetes and atherosclerosis.37 Overweight, minority race/ethnicity, and family history of diabetes are risk factors for type 2 diabetes in youth.8

The Diabetes Prevention Program demonstrated reduction in diabetes risk among adults with prediabetes through diet and exercise.9 Some dose-response relationships between exercise and metabolic risk have been demonstrated in adults.10 Previous studies in children have shown reduction in metabolic risk factors through exercise,1113 but dose-response information needed to formulate evidence-based public health recommendations for children is not available.1416

The purpose of the current study was to test the dose-response effect of an aerobic training program on insulin resistance, overall and visceral adiposity, and aerobic fitness in overweight children. A secondary aim was to test moderation by race and sex.

Participants

Children were recruited from schools during 2003-2006 for a trial of aerobic exercise on health. The study was advertised via presentations and flyers distributed at 15 elementary schools in Richmond and Columbia counties in Georgia and Aiken county in South Carolina. Inclusion criteria were white or black race, aged 7 to 11 years, overweight or obese (≥85th percentile body mass index [BMI]; calculated as weight in kilograms divided by height in meters squared),17 sedentary (no regular physical activity program >1 hour per week), no medical condition or medications that would affect study results or limit physical activity, and ability to provide a fasting blood sample at baseline. Informed consent and assent were obtained orally and in writing from parents or guardians and from children. The study was approved by the Human Assurance Committee of the Medical College of Georgia. Testing and intervention occurred at the Medical College of Georgia.

Procedure

Six cohorts of 30 to 40 children participated over 4 years. Randomization to a low-dose exercise treatment (20 min/d of aerobic exercise), a high-dose exercise treatment (40 min/d of aerobic exercise), or a no-treatment control condition was performed by the statistician (J.L.W.), stratified by race and sex. As each cohort was enrolled, each participant was assigned a uniform (0, 1) random number using SAS software, versions 8.2 and 9.1 (SAS Institute Inc), within their respective race and sex group. If the number was between 0 and 0.33, the child was randomized to the low-dose group; between 0.34 and 0.67, to the high-dose group; and above 0.67, to the control group. Assignments were concealed until baseline testing was completed, then communicated to the study coordinator, who informed participants and monitored adverse events reported by participants. Children assigned to the control condition were asked to continue their usual activities. All families enrolled in the study were offered monthly lifestyle education classes that addressed topics such as healthy diet, physical activity, and stress management.

Exercise Interventions

The aerobic exercise program was offered each day after school for 10 to 15 weeks during a school semester. Children were bused to a gymnasium at the Georgia Prevention Institute and offered healthy snacks prior to exercise. The low- and high-dose exercise conditions were equivalent in intensity and differed only in duration and, therefore, volume (ie, energy expenditure) of daily exercise. Children assigned to the high-dose exercise condition were offered two 20-minute exercise bouts each school day. Children assigned to the low-dose exercise condition were included in the first 20-minute bout in the gymnasium and then went to another room for a 20-minute sedentary period.

The emphasis was on intensity, enjoyment, and safety, not competition or skill enhancement. Activities were selected based on ease of comprehension, fun, and eliciting intermittent vigorous movement and included running games, jump rope, and modified basketball and soccer (eg, Howe et al18). Points were awarded daily for an average heart rate higher than 150 beats/min in the program (S610i, Polar Electro; 30-second epoch) and redeemed for weekly prizes. The program handbook is available from the authors on request.

Outcomes

The prespecified primary outcomes of the study included insulin resistance (ie, insulin area under the curve [AUC]), fatness, visceral fat, and aerobic fitness; fasting glucose level was a secondary outcome. A secondary aim of the study tested moderation of group effects by race and sex to determine generalizability of results. Exploratory outcomes included fasting insulin level, Matsuda index, disposition indexes, subcutaneous abdominal fat, and BMI z score.

Measurements

Measurements were conducted at baseline and repeated at posttest (after a mean 13 [SD, 1.6] weeks of intervention or control condition). Posttesting was scheduled 1 to 3 days following the child's last exercise session to minimize acute effects. Assessors were not blinded to these outcomes. Children were scheduled for the posttest in the order in which they were tested at baseline, balanced by group assignment, to avoid confounding by time between baseline and posttest or the duration of intervention. Most posttesting (eg, blood tests, dual-energy x-ray absorptiometry, fitness) was completed in 2006; magnetic resonance posttesting was completed in 2007. Parents reported age, sex, race (black or white), ethnicity, and family history of diabetes in biological parents or grandparents.

Blood Tests. The oral glucose tolerance test (OGTT) was used to measure diabetes risk at baseline and posttest.19 Fasting glucose and insulin levels were determined by averaging serum samples at 15, 10, and 5 minutes prior to glucose ingestion (1.75 g/kg of dextrose based on ideal body weight, up to 75 g). Serum samples were taken every 30 minutes for 2 hours after glucose was consumed. Insulin AUC was calculated via the trapezoidal rule. Glucose was measured using the glucose oxidase method (Analox) and insulin using radioimmunoassay (human-specific insulin, Linco Research Inc). The mean intra-assay coefficients of variation for glucose and insulin assays are 0.61% and 4.5% and interassay coefficients of variation are 1.45% and 2.3%, respectively. Prediabetes status was determined by impaired fasting glucose (fasting serum glucose, 100-125 mg/dL) or impaired glucose tolerance (2-hour glucose, 140-199 mg/dL) at baseline.20

Diabetes risk indexes that were either validated in children21 or demonstrated to predict the incidence of diabetes in adults22 were exploratory outcomes. The Matsuda index of insulin sensitivity was calculated.23,24 There is no clinically normal range for these indexes. Higher values on the Matsuda index indicate more insulin sensitivity, less insulin resistance, and less diabetes risk. At baseline, the Matsuda index range was 0.55 to 9.30; at posttest it was 0.75 to 7.20. Beta cell function was assessed in 2 ways. The disposition index based on the OGTT (DIOGTT) was calculated as the product of the Matsuda index and insulinogenic index (ie, Δinsulin0-30/Δglucose0-30).22,25 The disposition index based on fasting insulin (DIFI) was the product of fasting insulin−1 and the insulinogenic index.21 Higher values on the disposition indexes indicate better beta cell function (insulin secretion relative to insulin resistance) and lower diabetes risk. At baseline, the range for DIOGTT was 0.22 to 19.35 and for DIFI was 0.5 to 0.48. At posttest, the range for DIOGTT was 0.22 to 19.01 and for DIFI was 0.03 to 0.55. Twenty-nine individuals were excluded from the analyses for insulin AUC and Matsuda index and 6 from disposition indexes because of missing OGTT data points at baseline.

Estradiol was measured in girls by double-antibody radioimmunoassay and testosterone in boys by coated-tube radioimmunoassay (Diagnostic Products Corp). Intra-assay and interassay coefficients of variation for estradiol are 3.6% and 5.2% and for testosterone are 2.7% and 8.6%, respectively. Testosterone and estradiol values were normalized and combined into a composite variable to adjust for potential effects of pubertal development on insulin resistance.

Body Composition. Dual-energy x-ray absorptiometry (Hologic QDR-4500W) of the whole body was used to measure fatness. Abdominal visceral and subcutaneous fat content was measured with magnetic resonance imaging (1.5T; General Electric Medical Systems) of five 1-cm transverse slices around the L4-L5 disk.26

Cardiovascular Fitness. Cardiovascular fitness was determined using a multistage treadmill test modified from the protocol for poorly fit children (oxygen consumption [V. O2] relative to body mass in milliliters per kilogram per minute; Sensormedics Vmax 229).27,28 The modified protocol incorporated a warm-up period of 2.5 mph, 0% slope for 2 minutes before the warm-up at 3 mph, 3% slope for 2 minutes in the original protocol. After the warm-up, the speed remained at 3 mph and slope increased by 2% every 2 minutes until the child decided to stop or until maximum oxygen consumption (V. O2max) was reached. Because not all children attain V. O2max, the peak V. O2 value during the treadmill test was used as the primary fitness outcome.

Anthropometrics. Anthropometrics were measured at least twice until consistent measures were obtained. Body mass index percentiles and z scores were determined from body weight (in shorts and t-shirt; Detecto) and height (without shoes; HR100; Tanita).17 Tanner stages were assessed by pediatricians.

Physical Activity and Energy Intake. Physical activity was self-reported using questions from the Youth Risk Behavior Survey.29,30 Moderate physical activity (days per week) was determined by the question “On how many of the past 7 days did you participate in physical activity for at least 30 minutes that did not make you sweat or breathe hard, such as fast walking, slow bicycling, skating, pushing a lawn mower, or mopping floors?” Vigorous physical activity (days per week) was determined by the question “On how many of the past 7 days did you exercise or participate in physical activity for at least 20 minutes that made you sweat or breathe hard, such as bicycling, fast dancing, or similar aerobic activities?”

To assess compensation for energy expenditure in the exercise programs, three 24-hour diet recalls with food records were obtained to provide mean daily energy intake (kilocalories; Nutrition Data System for Research software; version 2006). Prior to recall, children and parents were trained in how to maintain a diet record using food models, portion booklets, and containers for estimating serving size.

Energy Expenditure During Aerobic Training. Energy expenditure during the exercise sessions was estimated by first regressing V. O2 on heart rate from each treadmill test. Participants' mean slope between baseline and posttest was used to adjust for improved fitness elicited by the intervention. Energy expenditure (kilocalories) and intensity (metabolic equivalents) in the exercise program were then estimated for 123 children (85% of those so assigned who provided adequate data during treadmill tests) using daily attendance and average heart rate. A coefficient of 5 kcal/L was used for estimation of energy expenditure from V. O2.

Statistical Analyses

A planned sample size of 80 per group, allowing for 20% attrition resulting in 64 per group at posttest, was selected to provide 80% or more power using a 2-sided α level of .05 to detect group differences on most primary outcomes (insulin resistance and body fat, each 96%; visceral fat, 71%; and fitness, 98% power) based on results from prior studies that showed group differences in change in fasting insulin (−4.2 μU/mL), body fat (−1.6%),12 visceral fat (−2.0 cm3),31 and fitness (+2.2 mL/kg/min).32 All statistical analyses were performed using SAS software, version 9.2, and a 2-sided α level of .05 was set as significant. Data were examined for normality and logarithmic transformations applied if necessary. Group differences at baseline were determined using analysis of variance and χ2 tests.

Repeated-measures mixed models were used with maximum likelihood estimation and a Kenward-Rogers adjustment to the degrees of freedom in an intention-to-treat analysis of each outcome measure using all available data. Base models for each outcome measure included the fixed effects of group and measurement period (baseline or posttest) and their interaction, and controlled cohort, race, and sex. Participant nested within group was considered a random effect. The modeled covariance structure between measurement periods was unstructured because there were only 2 measurement periods. Other potential covariates included Tanner stages, sex hormone levels, and family history of diabetes at baseline. If either Tanner stage variable was significant, both were included. Prespecified moderators (sex, race, and sex × race) were tested to determine generalizability, and exploratory moderators (family history of diabetes, prediabetes status) were tested to see if higher-risk groups were more likely to benefit, each controlling for covariates. Final models included effects in the base model, any statistically significant covariates, and any statistically significant interactions with group and measurement time. A priori linear contrasts across the 3 groups of the change from baseline to posttest tested dose-response effects of exercise intervention. Pairwise comparisons of change between groups were performed.

Participant flow is presented in Figure 1. We randomized 222 children to the control (n = 78), low-dose exercise (n = 71), or high-dose exercise (n = 73) condition. Similar baseline characteristics were observed in the 3 groups (Table 1). A majority of children (85%) were obese and 28% had prediabetes.

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Figure 1. Participant Flow
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Table Graphic Jump LocationTable 1. Baseline Participant Characteristicsa

The numbers of minor adverse events that occurred during testing were similar between groups (5, 7, and 6 in control, low-dose, and high-dose groups, respectively; P = .85), as was the duration between baseline and posttest (mean, 129 [SD, 19], 129 [SD, 15], and 128 [SD, 13] days, respectively; P = .91). Duration of intervention, number of minor adverse events during intervention, attendance, heart rate, and intensity were similar in the low- and high-dose exercise groups (Table 2). There was 1 serious adverse event (foot fracture in the low-dose exercise group). As expected, daily and total energy expenditure were higher in the high-dose vs the low-dose exercise group. Ninety-four percent of the sample (n = 209) was retained at posttest. No effect of group was observed on dietary intake or physical activity self-reports. Significant covariates included Tanner stage for insulin AUC, Matsuda index, fasting insulin and glucose, and sex hormones for body fat.

Table Graphic Jump LocationTable 2. Measurements Obtained During the Intervention Perioda
Primary Outcomes: Insulin Resistance, Fatness, and Fitness

Changes in outcomes by exercise dose are shown in Figure 2, Figure 3, and Table 3. Significant downward linear dose-response trends, with larger reductions between baseline and posttest for the high-dose exercise group than for the control group, were observed for insulin AUC (adjusted mean difference, −3.56 ×103 μU/mL; 95% CI, −6.26 to −0.85 ×103 μU/mL; P = .01), body fat (adjusted mean difference, −1.4%; 95% CI, −2.2% to −0.7%; P < .001), and visceral fat (adjusted mean difference, −3.9 cm3; 95% CI, −6.0 to −1.7 cm3; P < .001). Reductions in the low-dose exercise group, which were larger than changes in the control group, were also observed for insulin AUC (adjusted mean difference, −2.96 ×103 μU/mL; 95% CI, −5.69 to −0.22 ×103 μU/mL; P = .03), body fat (adjusted mean difference, −0.8%; 95% CI, −1.6% to −0.07%; P = .03), and visceral fat (adjusted mean difference, −2.8 cm3; 95% CI, −4.9 to −0.6 cm3; P = .01). Although adjusted mean differences in change were larger in the high-dose vs low-dose exercise group for these outcomes, the difference in change between the exercise groups was not significant. Very similar increases for both exercise groups were observed for fitness, with each group's change significantly larger than that of the control condition (adjusted mean difference in peak V. O2, 2.4 mL/kg/min; 95% CI, 0.4-4.5 mL/kg/min; P = .02 in the high-dose exercise group and 2.4 mL/kg/min; 95% CI, 0.3-4.5 mL/kg/min; P = .02 in the low-dose exercise group vs the control group), with no significant difference between exercise doses.

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Figure 2. Intention-to-Treat Mixed-Model Repeated-Measures Analysis of Variance of the Effect of Group on Primary Outcomes
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The P value in each panel indicates the test of the dose-response trend; ie, whether change between baseline and posttest differed between the control and high-dose exercise (40-min/d) groups. Error bars indicate 95% confidence intervals. AUC indicates area under the curve; V. O2, oxygen consumption.

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Figure 3. Intention-to-Treat Mixed-Model Repeated-Measures Analysis of Variance of the Effect of Group on Secondary and Exploratory Outcomes
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The P value in each panel indicates the test of the dose-response trend; ie, whether change between baseline and posttest differed between the control and high-dose (40-min/d) exercise groups. Error bars indicate 95% confidence intervals. DIOGTT indicates disposition index based on oral glucose tolerance test measurement of insulin sensitivity (Matsuda index × insulinogenic index); DIFI, disposition index based on fasting estimate of insulin sensitivity (1/fasting insulin × insulinogenic index); BMI, body mass index.

Table Graphic Jump LocationTable 3. Changes in Diabetes Risk, Fitness, and Fatness Outcomesa
Other Outcomes

No significant effect of exercise was detected for the secondary outcome of fasting glucose level. Dose-response benefits of exercise were indicated by significant downward trends across groups for fasting insulin level (adjusted mean difference, −3.98 μU/mL; 95% CI, −7.04 to −0.91 μU/mL; P = .01 for high-dose exercise and −3.55 μU/mL; 95% CI, −6.67 to −0.43 μU/mL; P = .03 for low-dose exercise vs control), and subcutaneous abdominal fat (adjusted mean difference, −24 cm3; 95% CI, −32 to −15 cm3; P < .001 for high-dose exercise and −15 cm3; 95% CI, −24 to −7 cm3; P < .001 for low-dose exercise vs control). For BMI z score, there was a significant downward trend, and differences in change were observed for the high-dose exercise group vs the other groups (adjusted mean difference, −0.1; 95% CI, −0.14 to −0.05; P < .001 vs control and −0.05; 95% CI, −0.10 to −0.01; P = .02 vs low-dose exercise), but there was no difference in effect between the low-dose exercise and control groups.

A significant upward trend with exercise dose was seen on the Matsuda index (adjusted mean difference, 0.67; 95% CI, 0.26-1.08; P = .002 for high-dose exercise and 0.56; 95% CI, 0.14-0.97; P = .009 for low-dose exercise vs control). An upward trend and difference in change between the high-dose exercise and control groups was shown for DIOGTT (adjusted mean difference, 0.84; 95% CI, 0.02-1.65; P = .04), but the change in the low-dose exercise group was similar to those in the high-dose exercise and control groups. No group difference in change was detected for DIFI.

For fasting insulin level, a significant interaction of family history of diabetes × group × time was found. However, excluding an extreme fasting insulin value at posttest (136 μU/mL) without excluding other data for that child (a control group participant with no family history of diabetes) eliminated the interaction (Table 3). There were no other significant interactions of group × time with family history, race, sex, or prediabetes status.

This randomized clinical trial in sedentary overweight and obese children, 28% of whom had prediabetes, quantified the efficacy of monitored aerobic exercise training to reduce diabetes risk (ie, insulin resistance) and other indexes of cardiometabolic risk. The trial had exceptional adherence and retention. A daily aerobic exercise intervention with a duration of 13 weeks and no dietary restrictions showed dose-response benefits as assessed by insulin response to OGTT and fasting insulin. The high-dose exercise intervention demonstrated significant benefit on DIOGTT, a surrogate index of diabetes risk integrating insulin resistance and beta cell function and an excellent predictor of diabetes incidence in adults.22,33 The reductions in fasting insulin recategorized most participants in the exercise groups from high to borderline high clinical status for insulin resistance.34 No intervention effects were detected on fasting glucose or the DIFI. Dose-response improvements in detailed measures of fatness were observed, and the 2 exercise doses showed similar improvements in fitness. No evidence for energy expenditure compensation was found.

No difference in efficacy was observed between boys and girls, black and white children, or children with prediabetes vs normoglycemic children. These consistent effects of intervention do not conflict with cross-sectional race differences reported in the literature (lower visceral adiposity, greater insulin resistance, and higher disposition index in black children)3537 but contrast with the prospective finding that black girls were less sensitive than white girls to the effects of physical activity on fat accretion.38 An effect modification for the effect of exercise on fasting insulin was detected for family history, but this appeared to be due to 1 extreme value, probably caused by nonadherence to fasting. Therefore, the cardiometabolic effects of exercise appear to be generalizable to overweight black and white boys and girls, regardless of prediabetes or family history of diabetes.

The increment of benefit between the control and low-dose exercise conditions was larger than the additional benefit observed between the low- and high-dose exercise groups. Greater benefit has been obtained from a given amount of physical activity in the most sedentary people, with smaller benefits accruing to people who are already moderately active.39 The low- and high-dose exercise groups showed similar effects on insulin resistance. A similar result for insulin resistance was obtained by the STRRIDE study, where the low-volume exercise group had similar improvements as the high-volume exercise group at the same intensity. Moderate as well as vigorous activity was linked with insulin sensitivity in a population study.40 Inflammation from a large volume or high intensity of exercise may impair insulin sensitivity.41 The low- and high-dose exercise interventions showed nearly identical effects on fitness. Fitness benefits may be gained based on intensity rather than volume of exercise.42 This study was powered to detect a dose-response gradient but was unable to distinguish between these daily volumes of aerobic activity, except for subcutaneous abdominal fat and BMI z score, for which greater benefits were observed with 40 minutes vs 20 minutes of daily vigorous activity.

Although several exercise studies have now used an 8- to 9-month training period, more than twice that of the current study, the 5-d/wk frequency in this study is rare.43 The Cochrane review of obesity treatment trials44 includes only 9 focused on physical activity in children younger than 12 years and only 1 of comparable size (N = 218). In the larger studies, interventions consisted of clinical advice rather than monitored exercise. Most interventions were of similar or shorter duration. Physical activity interventions were of lower intensity and frequency (contacts with participants from once a month to 3 times a week) and few studies isolated exercise, instead combining it with a dietary intervention.

Large, well-conducted school-based studies have tested effects of physical activity on obesity in children and have failed to reduce obesity, perhaps because of inadequate dose45,46; 1 study succeeded only in girls.47 The HEALTHY study was designed to reduce risk of type 2 diabetes using multiple school-wide strategies to improve nutrition and physical activity over 3 years; it improved adiposity measures and fasting insulin by a small amount. This efficacy study, with a more intensive, focused intervention, achieved 3 times the effect on BMI z score and 8 times the effect on fasting insulin in overweight children in a short time. These results contrast with a similar exercise intervention in black girls that, despite longer duration (10 months) and improved adiposity and fitness, did not reduce fasting insulin concentration.11 That study did not restrict enrollment to overweight or obese children, who are more insulin resistant and may be more sensitive to intervention than normal-weight peers.

The relatively short duration of the intervention and lack of follow-up assessment of possible lasting effects are limitations of the current study. In addition, participants were not blinded to condition because it was a behavioral intervention; measurement staff were not blinded; the control group was not offered an attention-control intervention program; and the daily snack offered only to the exercise groups may have affected outcomes.

Twenty minutes of aerobic exercise per school day for just a few months showed benefits vs the control condition on insulin resistance, fitness, and fatness. Thus, measurable health benefits could be achieved through a daily dose of safe, vigorous physical activity, which could be provided during the school day in daily fitness-focused physical education classes, recess, and other physical activity opportunities.4852 However, to achieve the benefits of 40 min/d of vigorous physical activity (the basis for the 60-min/d recommendation for physical activity for free-living children),14 after-school physical activity programs may be necessary. Schools are the logical focus for such public health interventions.49 An ancillary study showed benefits of this exercise intervention on cognition and mathematics achievement, which may increase its appeal to educators.53 Elements of the program that may have contributed to its success were limiting enrollment to overweight and obese children; use of inclusive, appealing interventions with fun, simple games that minimized barriers to participation; use of heart rate as a physiological index of effort; and provision of contingent rewards for effort rather than athletic performance to encourage even unfit children to exercise intensely.

In conclusion, in this randomized controlled trial, 13 weeks of 20- or 40-min/d aerobic training resulted in improvement in diabetes risk as estimated by insulin resistance, fitness, and general and visceral adiposity in sedentary overweight or obese children regardless of race or sex, with a dose-response gradient for insulin resistance and adiposity.

Corresponding Author: Catherine L. Davis, PhD, Georgia Prevention Center, Institute for Public and Preventive Health, Department of Pediatrics, Medical College of Georgia, 1120 15th St, Ste 1640, Augusta, GA 30912 (cadavis@georgiahealth.edu).

Author Contributions: Dr Davis 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.

Study concept and design: Davis, Waller, Allison, Bassali, Boyle, Gower.

Acquisition of data: Davis, Allison, Bassali, Boyle.

Analysis and interpretation of data: Davis, Pollock, Waller, Allison, Dennis, Bassali, Meléndez, Gower.

Drafting of the manuscript: Davis, Pollock, Waller, Dennis, Meléndez.

Critical revision of the manuscript for important intellectual content: Davis, Pollock, Waller, Allison, Dennis, Bassali, Boyle, Gower.

Statistical analysis: Davis, Pollock, Waller.

Obtained funding: Davis.

Administrative, technical, or material support: Davis, Pollock, Allison, Meléndez, Boyle, Gower.

Study supervision: Davis, Allison, Bassali, Boyle.

Conflict of Interest Disclosures: All authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest and none were reported.

Funding/Support: This work was supported by grants R01 DK060692, R01 HL087923, and P30 DK056336 from the National Institutes of Health and grant PR2006-0125 from the Salvador de Madariaga Program of the Spanish Ministry of Education and Science.

Role of the Sponsor: Funding agencies had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; or preparation, review, or approval of the manuscript.

Additional Contributions: We thank the study participants and staff who made this research possible, Catrina Creech, BA, for coordinating the study, Rachel Elam, ScM, for assistance with manuscript preparation, and Bernard Gutin, PhD, for contributions to study design; each received salary support for this work at the Department of Pediatrics, Medical College of Georgia. Dr Gutin is now with the Department of Nutrition, University of North Carolina, Chapel Hill. We also thank David Allison, PhD, and John Dawson, PhD, of the School of Public Health, University of Alabama at Birmingham, who provided consultation on statistical analyses. Neither received compensation.

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American Diabetes Association.  Type 2 diabetes in children and adolescents.  Diabetes Care. 2000;23(3):381-389
PubMed   |  Link to Article
Knowler WC, Barrett-Connor E, Fowler SE,  et al; Diabetes Prevention Program Research Group.  Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin.  N Engl J Med. 2002;346(6):393-403
PubMed   |  Link to Article
Johnson JL, Slentz CA, Houmard JA,  et al.  Exercise training amount and intensity effects on metabolic syndrome (from Studies of a Targeted Risk Reduction Intervention Through Defined Exercise).  Am J Cardiol. 2007;100(12):1759-1766
PubMed   |  Link to Article
Barbeau P, Johnson MH, Howe CA,  et al.  Ten months of exercise improves general and visceral adiposity, bone, and fitness in black girls.  Obesity (Silver Spring). 2007;15(8):2077-2085
PubMed   |  Link to Article
Ferguson MA, Gutin B, Le NA,  et al.  Effects of exercise training and its cessation on components of the insulin resistance syndrome in obese children.  Int J Obes Relat Metab Disord. 1999;23(8):889-895
PubMed   |  Link to Article
Gutin B, Owens S, Okuyama T, Riggs S, Ferguson M, Litaker M. Effect of physical training and its cessation on percent fat and bone density of children with obesity.  Obes Res. 1999;7(2):208-214
PubMed   |  Link to Article
Strong WB, Malina RM, Blimkie CJ,  et al.  Evidence based physical activity for school-age youth.  J Pediatr. 2005;146(6):732-737
PubMed   |  Link to Article
Institute of Medicine.  Adequacy of Evidence for Physical Activity Guidelines Development: Workshop Summary. Washington, DC: National Academies Press; 2007
Glickman D, ed, Parker L, ed, Sim LJ, ed, Cook HDV, ed, Miller EA, edAccelerating Progress in Obesity Prevention: Solving the Weight of the Nation. Washington, DC: National Academies Press; 2012. http://www.iom.edu/Reports/2012/Accelerating-Progress-in-Obesity-Prevention.aspx. Accessed May 9, 2012
Ogden CL, Kuczmarski RJ, Flegal KM,  et al.  Centers for Disease Control and Prevention 2000 growth charts for the United States: improvements to the 1977 National Center for Health Statistics version.  Pediatrics. 2002;109(1):45-60
PubMed   |  Link to Article
Howe CA, Freedson PS, Feldman HA, Osganian SK. Energy expenditure and enjoyment of common children's games in a simulated free-play environment.  J Pediatr. 2010;157(6):936-942
PubMed   |  Link to Article
Yeni-Komshian H, Carantoni M, Abbasi F, Reaven GM. Relationship between several surrogate estimates of insulin resistance and quantification of insulin-mediated glucose disposal in 490 healthy nondiabetic volunteers.  Diabetes Care. 2000;23(2):171-175
PubMed   |  Link to Article
 Report of the Expert Committee on the Diagnosis and Classification of Diabetes Mellitus.  Diabetes Care. 1997;20(7):1183-1197
PubMed
Sjaarda LG, Bacha F, Lee S, Tfayli H, Andreatta E, Arslanian S. Oral disposition index in obese youth from normal to prediabetes to diabetes: relationship to clamp disposition index.  J Pediatr. 2012;161(1):51-57
PubMed   |  Link to Article
Abdul-Ghani MA, Williams K, DeFronzo RA, Stern M. What is the best predictor of future type 2 diabetes?  Diabetes Care. 2007;30(6):1544-1548
PubMed   |  Link to Article
Matsuda M, DeFronzo RA. Insulin sensitivity indices obtained from oral glucose tolerance testing: comparison with the euglycemic insulin clamp.  Diabetes Care. 1999;22(9):1462-1470
PubMed   |  Link to Article
Yeckel CW, Weiss R, Dziura J,  et al.  Validation of insulin sensitivity indices from oral glucose tolerance test parameters in obese children and adolescents.  J Clin Endocrinol Metab. 2004;89(3):1096-1101
PubMed   |  Link to Article
Hanson RL, Pratley RE, Bogardus C,  et al.  Evaluation of simple indices of insulin sensitivity and insulin secretion for use in epidemiologic studies.  Am J Epidemiol. 2000;151(2):190-198
PubMed   |  Link to Article
Owens S, Gutin B, Ferguson M, Allison J, Karp W, Le NA. Visceral adipose tissue and cardiovascular risk factors in obese children.  J Pediatr. 1998;133(1):41-45
PubMed   |  Link to Article
Rowland TW. Aerobic Exercise Testing Protocols. Champaign, IL: Human Kinetics; 1993
American College of Sports Medicine.  ACSM's Guidelines for Exercise Testing and Prescription. 6th ed. Baltimore, MD: Lippincott Williams & Wilkins; 2000
Brener ND, Kann L, Kinchen SA,  et al.  Methodology of the Youth Risk Behavior Surveillance System.  MMWR Recomm Rep. 2004;53(RR-12):1-13
PubMed
Brener ND, Collins JL, Kann L, Warren CW, Williams BI. Reliability of the Youth Risk Behavior Survey Questionnaire.  Am J Epidemiol. 1995;141(6):575-580
PubMed
Owens S, Gutin B, Allison J,  et al.  Effect of physical training on total and visceral fat in obese children.  Med Sci Sports Exerc. 1999;31(1):143-148
PubMed   |  Link to Article
Gutin B, Yin Z, Humphries MC, Barbeau P. Relations of moderate and vigorous physical activity to fitness and fatness in adolescents.  Am J Clin Nutr. 2005;81(4):746-750
PubMed
Utzschneider KM, Prigeon RL, Faulenbach MV,  et al.  Oral disposition index predicts the development of future diabetes above and beyond fasting and 2-h glucose levels.  Diabetes Care. 2009;32(2):335-341
PubMed   |  Link to Article
Williams CL, Hayman LL, Daniels SR,  et al.  Cardiovascular health in childhood: a statement for health professionals from the Committee on Atherosclerosis, Hypertension, and Obesity in the Young (AHOY) of the Council on Cardiovascular Disease in the Young, American Heart Association.  Circulation. 2002;106(1):143-160
PubMed   |  Link to Article
Liese AD, D’Agostino RB Jr, Hamman RF,  et al; SEARCH for Diabetes in Youth Study Group.  The burden of diabetes mellitus among US youth: prevalence estimates from the SEARCH for Diabetes in Youth Study.  Pediatrics. 2006;118(4):1510-1518
PubMed   |  Link to Article
D’Adamo E, Northrup V, Weiss R,  et al.  Ethnic differences in lipoprotein subclasses in obese adolescents: importance of liver and intra-abdominal fat accretion.  Am J Clin Nutr. 2010;92(3):500-508
PubMed   |  Link to Article
Gower BA, Nagy TR, Trowbridge CA, Dezenberg C, Goran MI. Fat distribution and insulin response in prepubertal African American and white children.  Am J Clin Nutr. 1998;67(5):821-827
PubMed
White J, Jago R. Prospective associations between physical activity and obesity among adolescent girls: racial differences and implications for prevention.  Arch Pediatr Adolesc Med. 2012;166(6):522-527
PubMed   |  Link to Article
Haskell WL. Physical activity in the prevention and management of coronary heart disease.  PCPFS Research Digest. 1995;2(1):1-12
Mayer-Davis EJ, D’Agostino R Jr, Karter AJ,  et al.  Intensity and amount of physical activity in relation to insulin sensitivity: the Insulin Resistance Atherosclerosis Study.  JAMA. 1998;279(9):669-674
PubMed   |  Link to Article
Suzuki K, Nakaji S, Yamada M, Totsuka M, Sato K, Sugawara K. Systemic inflammatory response to exhaustive exercise: cytokine kinetics.  Exerc Immunol Rev. 2002;8:6-48
PubMed
Gutin B, Barbeau P, Owens S,  et al.  Effects of exercise intensity on cardiovascular fitness, total body composition, and visceral adiposity of obese adolescents.  Am J Clin Nutr. 2002;75(5):818-826
PubMed
Kesten JM, Griffiths PL, Cameron N. A systematic review to determine the effectiveness of interventions designed to prevent overweight and obesity in pre-adolescent girls.  Obes Rev. 2011;12(12):997-1021
PubMed   |  Link to Article
Oude Luttikhuis H, Baur L, Jansen H,  et al.  Interventions for treating obesity in children.  Cochrane Database Syst Rev. 2009;(1):CD001872
PubMed
Webber LS, Osganian SK, Feldman HA,  et al.  Cardiovascular risk factors among children after a 2½-year intervention—the CATCH study.  Prev Med. 1996;25(4):432-441
PubMed   |  Link to Article
Sallis JF, McKenzie TL, Alcaraz JE, Kolody B, Hovell MF, Nader PR. Project SPARK: effects of physical education on adiposity in children.  Ann N Y Acad Sci. 1993;699:127-136
PubMed   |  Link to Article
Gortmaker SL, Peterson K, Wiecha J,  et al.  Reducing obesity via a school-based interdisciplinary intervention among youth: Planet Health.  Arch Pediatr Adolesc Med. 1999;153(4):409-418
PubMed   |  Link to Article
Sallis JF, McKenzie TL, Alcaraz JE, Kolody B, Faucette N, Hovell MF. The effects of a 2-year physical education program (SPARK) on physical activity and fitness in elementary school students: Sports, Play and Active Recreation for Kids.  Am J Public Health. 1997;87(8):1328-1334
PubMed   |  Link to Article
Pate RR, Davis MG, Robinson TN, Stone EJ, McKenzie TL, Young JC.American Heart Association Council on Nutrition, Physical Activity, and Metabolism (Physical Activity Committee); Council on Cardiovascular Disease in the Young; Council on Cardiovascular Nursing.  Promoting physical activity in children and youth: a leadership role for schools: a scientific statement from the American Heart Association Council on Nutrition, Physical Activity, and Metabolism (Physical Activity Committee) in collaboration with the Councils on Cardiovascular Disease in the Young and Cardiovascular Nursing.  Circulation. 2006;114(11):1214-1224
PubMed   |  Link to Article
Donnelly JE, Greene JL, Gibson CA,  et al.  Physical Activity Across the Curriculum (PAAC): a randomized controlled trial to promote physical activity and diminish overweight and obesity in elementary school children.  Prev Med. 2009;49(4):336-341
PubMed   |  Link to Article
Mahar MT, Murphy SK, Rowe DA, Golden J, Shields AT, Raedeke TD. Effects of a classroom-based program on physical activity and on-task behavior.  Med Sci Sports Exerc. 2006;38(12):2086-2094
PubMed   |  Link to Article
Kibbe DL, Hackett J, Hurley M,  et al.  Ten Years of TAKE 10!: integrating physical activity with academic concepts in elementary school classrooms.  Prev Med. 2011;52:(suppl 1)  S43-S50
PubMed   |  Link to Article
Davis CL, Tomporowski PD, McDowell JE,  et al.  Exercise improves executive function and achievement and alters brain activation in overweight children: a randomized, controlled trial.  Health Psychol. 2011;30(1):91-98
PubMed   |  Link to Article

Figures

Place holder to copy figure label and caption
Figure 1. Participant Flow
Graphic Jump Location
Place holder to copy figure label and caption
Figure 2. Intention-to-Treat Mixed-Model Repeated-Measures Analysis of Variance of the Effect of Group on Primary Outcomes
Graphic Jump Location

The P value in each panel indicates the test of the dose-response trend; ie, whether change between baseline and posttest differed between the control and high-dose exercise (40-min/d) groups. Error bars indicate 95% confidence intervals. AUC indicates area under the curve; V. O2, oxygen consumption.

Place holder to copy figure label and caption
Figure 3. Intention-to-Treat Mixed-Model Repeated-Measures Analysis of Variance of the Effect of Group on Secondary and Exploratory Outcomes
Graphic Jump Location

The P value in each panel indicates the test of the dose-response trend; ie, whether change between baseline and posttest differed between the control and high-dose (40-min/d) exercise groups. Error bars indicate 95% confidence intervals. DIOGTT indicates disposition index based on oral glucose tolerance test measurement of insulin sensitivity (Matsuda index × insulinogenic index); DIFI, disposition index based on fasting estimate of insulin sensitivity (1/fasting insulin × insulinogenic index); BMI, body mass index.

Tables

Table Graphic Jump LocationTable 1. Baseline Participant Characteristicsa
Table Graphic Jump LocationTable 2. Measurements Obtained During the Intervention Perioda
Table Graphic Jump LocationTable 3. Changes in Diabetes Risk, Fitness, and Fatness Outcomesa

References

Strauss RS, Pollack HA. Epidemic increase in childhood overweight, 1986-1998.  JAMA. 2001;286(22):2845-2848
PubMed   |  Link to Article
Ogden CL, Carroll MD, Curtin LR, Lamb MM, Flegal KM. Prevalence of high body mass index in US children and adolescents, 2007-2008.  JAMA. 2010;303(3):242-249
PubMed   |  Link to Article
Davis CL, Kapuku G, Snieder H, Kumar M, Treiber FA. Insulin resistance syndrome and left ventricular mass in healthy young people.  Am J Med Sci. 2002;324(2):72-75
PubMed   |  Link to Article
Davis CL, Flickinger B, Moore D, Bassali R, Domel Baxter S, Yin Z. Prevalence of cardiovascular risk factors in schoolchildren in a rural Georgia community.  Am J Med Sci. 2005;330(2):53-59
PubMed   |  Link to Article
Pinhas-Hamiel O, Dolan LM, Daniels SR, Standiford D, Khoury PR, Zeitler P. Increased incidence of non-insulin-dependent diabetes mellitus among adolescents.  J Pediatr. 1996;128(5 pt 1):608-615
PubMed
McGill HC Jr, McMahan CA, Zieske AW,  et al.  Association of coronary heart disease risk factors with microscopic qualities of coronary atherosclerosis in youth.  Circulation. 2000;102(4):374-379
PubMed   |  Link to Article
Daniels SR, Arnett DK, Eckel RH,  et al.  Overweight in children and adolescents: pathophysiology, consequences, prevention, and treatment.  Circulation. 2005;111(15):1999-2012
PubMed   |  Link to Article
American Diabetes Association.  Type 2 diabetes in children and adolescents.  Diabetes Care. 2000;23(3):381-389
PubMed   |  Link to Article
Knowler WC, Barrett-Connor E, Fowler SE,  et al; Diabetes Prevention Program Research Group.  Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin.  N Engl J Med. 2002;346(6):393-403
PubMed   |  Link to Article
Johnson JL, Slentz CA, Houmard JA,  et al.  Exercise training amount and intensity effects on metabolic syndrome (from Studies of a Targeted Risk Reduction Intervention Through Defined Exercise).  Am J Cardiol. 2007;100(12):1759-1766
PubMed   |  Link to Article
Barbeau P, Johnson MH, Howe CA,  et al.  Ten months of exercise improves general and visceral adiposity, bone, and fitness in black girls.  Obesity (Silver Spring). 2007;15(8):2077-2085
PubMed   |  Link to Article
Ferguson MA, Gutin B, Le NA,  et al.  Effects of exercise training and its cessation on components of the insulin resistance syndrome in obese children.  Int J Obes Relat Metab Disord. 1999;23(8):889-895
PubMed   |  Link to Article
Gutin B, Owens S, Okuyama T, Riggs S, Ferguson M, Litaker M. Effect of physical training and its cessation on percent fat and bone density of children with obesity.  Obes Res. 1999;7(2):208-214
PubMed   |  Link to Article
Strong WB, Malina RM, Blimkie CJ,  et al.  Evidence based physical activity for school-age youth.  J Pediatr. 2005;146(6):732-737
PubMed   |  Link to Article
Institute of Medicine.  Adequacy of Evidence for Physical Activity Guidelines Development: Workshop Summary. Washington, DC: National Academies Press; 2007
Glickman D, ed, Parker L, ed, Sim LJ, ed, Cook HDV, ed, Miller EA, edAccelerating Progress in Obesity Prevention: Solving the Weight of the Nation. Washington, DC: National Academies Press; 2012. http://www.iom.edu/Reports/2012/Accelerating-Progress-in-Obesity-Prevention.aspx. Accessed May 9, 2012
Ogden CL, Kuczmarski RJ, Flegal KM,  et al.  Centers for Disease Control and Prevention 2000 growth charts for the United States: improvements to the 1977 National Center for Health Statistics version.  Pediatrics. 2002;109(1):45-60
PubMed   |  Link to Article
Howe CA, Freedson PS, Feldman HA, Osganian SK. Energy expenditure and enjoyment of common children's games in a simulated free-play environment.  J Pediatr. 2010;157(6):936-942
PubMed   |  Link to Article
Yeni-Komshian H, Carantoni M, Abbasi F, Reaven GM. Relationship between several surrogate estimates of insulin resistance and quantification of insulin-mediated glucose disposal in 490 healthy nondiabetic volunteers.  Diabetes Care. 2000;23(2):171-175
PubMed   |  Link to Article
 Report of the Expert Committee on the Diagnosis and Classification of Diabetes Mellitus.  Diabetes Care. 1997;20(7):1183-1197
PubMed
Sjaarda LG, Bacha F, Lee S, Tfayli H, Andreatta E, Arslanian S. Oral disposition index in obese youth from normal to prediabetes to diabetes: relationship to clamp disposition index.  J Pediatr. 2012;161(1):51-57
PubMed   |  Link to Article
Abdul-Ghani MA, Williams K, DeFronzo RA, Stern M. What is the best predictor of future type 2 diabetes?  Diabetes Care. 2007;30(6):1544-1548
PubMed   |  Link to Article
Matsuda M, DeFronzo RA. Insulin sensitivity indices obtained from oral glucose tolerance testing: comparison with the euglycemic insulin clamp.  Diabetes Care. 1999;22(9):1462-1470
PubMed   |  Link to Article
Yeckel CW, Weiss R, Dziura J,  et al.  Validation of insulin sensitivity indices from oral glucose tolerance test parameters in obese children and adolescents.  J Clin Endocrinol Metab. 2004;89(3):1096-1101
PubMed   |  Link to Article
Hanson RL, Pratley RE, Bogardus C,  et al.  Evaluation of simple indices of insulin sensitivity and insulin secretion for use in epidemiologic studies.  Am J Epidemiol. 2000;151(2):190-198
PubMed   |  Link to Article
Owens S, Gutin B, Ferguson M, Allison J, Karp W, Le NA. Visceral adipose tissue and cardiovascular risk factors in obese children.  J Pediatr. 1998;133(1):41-45
PubMed   |  Link to Article
Rowland TW. Aerobic Exercise Testing Protocols. Champaign, IL: Human Kinetics; 1993
American College of Sports Medicine.  ACSM's Guidelines for Exercise Testing and Prescription. 6th ed. Baltimore, MD: Lippincott Williams & Wilkins; 2000
Brener ND, Kann L, Kinchen SA,  et al.  Methodology of the Youth Risk Behavior Surveillance System.  MMWR Recomm Rep. 2004;53(RR-12):1-13
PubMed
Brener ND, Collins JL, Kann L, Warren CW, Williams BI. Reliability of the Youth Risk Behavior Survey Questionnaire.  Am J Epidemiol. 1995;141(6):575-580
PubMed
Owens S, Gutin B, Allison J,  et al.  Effect of physical training on total and visceral fat in obese children.  Med Sci Sports Exerc. 1999;31(1):143-148
PubMed   |  Link to Article
Gutin B, Yin Z, Humphries MC, Barbeau P. Relations of moderate and vigorous physical activity to fitness and fatness in adolescents.  Am J Clin Nutr. 2005;81(4):746-750
PubMed
Utzschneider KM, Prigeon RL, Faulenbach MV,  et al.  Oral disposition index predicts the development of future diabetes above and beyond fasting and 2-h glucose levels.  Diabetes Care. 2009;32(2):335-341
PubMed   |  Link to Article
Williams CL, Hayman LL, Daniels SR,  et al.  Cardiovascular health in childhood: a statement for health professionals from the Committee on Atherosclerosis, Hypertension, and Obesity in the Young (AHOY) of the Council on Cardiovascular Disease in the Young, American Heart Association.  Circulation. 2002;106(1):143-160
PubMed   |  Link to Article
Liese AD, D’Agostino RB Jr, Hamman RF,  et al; SEARCH for Diabetes in Youth Study Group.  The burden of diabetes mellitus among US youth: prevalence estimates from the SEARCH for Diabetes in Youth Study.  Pediatrics. 2006;118(4):1510-1518
PubMed   |  Link to Article
D’Adamo E, Northrup V, Weiss R,  et al.  Ethnic differences in lipoprotein subclasses in obese adolescents: importance of liver and intra-abdominal fat accretion.  Am J Clin Nutr. 2010;92(3):500-508
PubMed   |  Link to Article
Gower BA, Nagy TR, Trowbridge CA, Dezenberg C, Goran MI. Fat distribution and insulin response in prepubertal African American and white children.  Am J Clin Nutr. 1998;67(5):821-827
PubMed
White J, Jago R. Prospective associations between physical activity and obesity among adolescent girls: racial differences and implications for prevention.  Arch Pediatr Adolesc Med. 2012;166(6):522-527
PubMed   |  Link to Article
Haskell WL. Physical activity in the prevention and management of coronary heart disease.  PCPFS Research Digest. 1995;2(1):1-12
Mayer-Davis EJ, D’Agostino R Jr, Karter AJ,  et al.  Intensity and amount of physical activity in relation to insulin sensitivity: the Insulin Resistance Atherosclerosis Study.  JAMA. 1998;279(9):669-674
PubMed   |  Link to Article
Suzuki K, Nakaji S, Yamada M, Totsuka M, Sato K, Sugawara K. Systemic inflammatory response to exhaustive exercise: cytokine kinetics.  Exerc Immunol Rev. 2002;8:6-48
PubMed
Gutin B, Barbeau P, Owens S,  et al.  Effects of exercise intensity on cardiovascular fitness, total body composition, and visceral adiposity of obese adolescents.  Am J Clin Nutr. 2002;75(5):818-826
PubMed
Kesten JM, Griffiths PL, Cameron N. A systematic review to determine the effectiveness of interventions designed to prevent overweight and obesity in pre-adolescent girls.  Obes Rev. 2011;12(12):997-1021
PubMed   |  Link to Article
Oude Luttikhuis H, Baur L, Jansen H,  et al.  Interventions for treating obesity in children.  Cochrane Database Syst Rev. 2009;(1):CD001872
PubMed
Webber LS, Osganian SK, Feldman HA,  et al.  Cardiovascular risk factors among children after a 2½-year intervention—the CATCH study.  Prev Med. 1996;25(4):432-441
PubMed   |  Link to Article
Sallis JF, McKenzie TL, Alcaraz JE, Kolody B, Hovell MF, Nader PR. Project SPARK: effects of physical education on adiposity in children.  Ann N Y Acad Sci. 1993;699:127-136
PubMed   |  Link to Article
Gortmaker SL, Peterson K, Wiecha J,  et al.  Reducing obesity via a school-based interdisciplinary intervention among youth: Planet Health.  Arch Pediatr Adolesc Med. 1999;153(4):409-418
PubMed   |  Link to Article
Sallis JF, McKenzie TL, Alcaraz JE, Kolody B, Faucette N, Hovell MF. The effects of a 2-year physical education program (SPARK) on physical activity and fitness in elementary school students: Sports, Play and Active Recreation for Kids.  Am J Public Health. 1997;87(8):1328-1334
PubMed   |  Link to Article
Pate RR, Davis MG, Robinson TN, Stone EJ, McKenzie TL, Young JC.American Heart Association Council on Nutrition, Physical Activity, and Metabolism (Physical Activity Committee); Council on Cardiovascular Disease in the Young; Council on Cardiovascular Nursing.  Promoting physical activity in children and youth: a leadership role for schools: a scientific statement from the American Heart Association Council on Nutrition, Physical Activity, and Metabolism (Physical Activity Committee) in collaboration with the Councils on Cardiovascular Disease in the Young and Cardiovascular Nursing.  Circulation. 2006;114(11):1214-1224
PubMed   |  Link to Article
Donnelly JE, Greene JL, Gibson CA,  et al.  Physical Activity Across the Curriculum (PAAC): a randomized controlled trial to promote physical activity and diminish overweight and obesity in elementary school children.  Prev Med. 2009;49(4):336-341
PubMed   |  Link to Article
Mahar MT, Murphy SK, Rowe DA, Golden J, Shields AT, Raedeke TD. Effects of a classroom-based program on physical activity and on-task behavior.  Med Sci Sports Exerc. 2006;38(12):2086-2094
PubMed   |  Link to Article
Kibbe DL, Hackett J, Hurley M,  et al.  Ten Years of TAKE 10!: integrating physical activity with academic concepts in elementary school classrooms.  Prev Med. 2011;52:(suppl 1)  S43-S50
PubMed   |  Link to Article
Davis CL, Tomporowski PD, McDowell JE,  et al.  Exercise improves executive function and achievement and alters brain activation in overweight children: a randomized, controlled trial.  Health Psychol. 2011;30(1):91-98
PubMed   |  Link to Article

Letters

January 9, 2013
Kevin R. Short, PhD
JAMA. 2013;309(2):133-134. doi:10.1001/jama.2012.148056.
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