Reviews/Commentaries/ADA Statements

M E T A - A N A L Y S I S

Effects of Different Modes of Exercise
Training on Glucose Control and Risk
Factors for Complications in Type 2
Diabetic Patients
A meta-analysis
NEIL J. SNOWLING, MSC1 uals who maintain a physically active life-
WILL G. HOPKINS, PHD2 style are less likely to develop insulin
resistance, impaired glucose tolerance, or
type 2 diabetes (2,5). The effects of exer-
OBJECTIVE — We sought to meta-analyze the effects of different modes of exercise training cise training on glucose control and re-
on measures of glucose control and other risk factors for complications of diabetes. lated physiological parameters have also
been extensively studied in patients with
RESEARCH DESIGN AND METHODS — The 27 qualifying studies were controlled type 2 diabetes. In 2001, Boulé et al. (6)
trials providing, for each measure, 4 –18 estimates for the effect of aerobic training, 2–7 for published a meta-analysis showing bene-
resistance training, and 1–5 for combined training, with 1,003 type 2 diabetic patients (age 55 ⫾ ficial effects of exercise training on one
7 years [mean ⫾ between-study SD]) over 5–104 weeks. The meta-analytic mixed model in-
aspect of glucose control in diabetic pa-
cluded main-effect covariates to control for between-study differences in disease severity, sex,
total training time, training intensity, and dietary cointervention (13 studies). To interpret tients, the percent of HbA1c (A1C) in
magnitudes, effects were standardized after meta-analysis using composite baseline between- blood. They also found reductions in two
subject SD. measures of abdominal obesity and little
effect on the only other parameter they
RESULTS — Differences among the effects of aerobic, resistance, and combined training on meta-analyzed: body mass.
HbA1c (A1C) were trivial; for training lasting ⱖ12 weeks, the overall effect was a small beneficial Of the 14 studies in the meta-analysis
reduction (A1C 0.8 ⫾ 0.3% [mean ⫾ 90% confidence limit]). There were generally small to of Boulé et al. (6), 12 used aerobic training
moderate benefits for other measures of glucose control. For other risk factors, there were either and 2 used resistance training. Some
small benefits or effects were trivial or unclear, although combined training was generally physiological adaptations to resistance
superior to aerobic and resistance training. Effects of covariates were generally trivial or unclear,
training differ from those of aerobic train-
but there were small additional benefits of exercise on glucose control with increased disease
severity. ing, so their effects on glucose control
may differ (7). Boulé et al. (6) found little
CONCLUSIONS — All forms of exercise training produce small benefits in the main mea- difference between effects of aerobic and
sure of glucose control: A1C. The effects are similar to those of dietary, drug, and insulin resistance training, but there were insuf-
treatments. The clinical importance of combining these treatments needs further research. ficient studies of resistance training for
this finding to be anything more than ten-
Diabetes Care 29:2518 –2527, 2006 tative. Since then, there have been numer-
ous new studies of aerobic, resistance,
and combined training. We have there-

D
iabetes is a group of metabolic dis- ing to the increasing prevalence of obesity
orders characterized by hyperglyce- and sedentary lifestyles. fore meta-analyzed the effects of these
mia resulting from defects in Physical activity or structured exer- three modes of training on A1C and other
insulin secretion, insulin action (hepatic cise training used alone or in combination measures of glucose control in type 2 di-
and peripheral glucose uptake), or both. with diet, insulin injections, or oral hypo- abetic patients. We have included physi-
The type 2 form of the disease is associ- glycemic drugs are the foundations of ological parameters related to
ated with obesity (1) and physical inactiv- therapy for type 2 diabetes (3,4). Evi- complications of diabetes, and we have
ity (2), and the prevalence of this form is dence for the benefit of physical activity dealt with study characteristics and mag-
nitude of effects in more detail than in the
increasing in Westernized countries, ow- comes from studies showing that individ-
previous meta-analyses.
● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ●
From the 1Faculty of Health and Environmental Sciences, Centre for Physical Activity and Nutrition Re- RESEARCH DESIGN AND
search, Auckland University of Technology, Auckland, New Zealand; and the 2Division of Sport and Rec-
reation, Faculty of Health and Environmental Sciences, Institute of Sport and Recreation Research New
METHODS — Searches of PubMed
Zealand, Auckland University of Technology, Auckland, New Zealand. and SportDiscus databases were per-
Address correspondence and reprint requests to Prof. Will Hopkins, Division of Sport and Recreation, formed for studies published in English
Auckland University of Technology, Private Bag 92006, Auckland, New Zealand. E-mail: will@clear.net.nz. up to and including May 2006. Reference
Received for publication 23 June 2006 and accepted in revised form 9 August 2006. lists of review articles and all included ar-
A table elsewhere in this issue shows conventional and Système International (SI) units and conversion
factors for many substances. ticles identified by the search were exam-
DOI: 10.2337/dc06-1317 ined for other eligible studies. Only
© 2006 by the American Diabetes Association. controlled trials of supervised exercise

2518 DIABETES CARE, VOLUME 29, NUMBER 11, NOVEMBER 2006
©

an integer value of 1 (easy walking) either area under the glucose curve fol- Of the 27 included studies. Other reasons with a program (54) for the mixed. we and healthy subjects (30 –32). insulin for at least one measure of glucose con. methods based on P values. In an additional analysis for A1C. analyzed following log transformation. expressed the effect of exercise relative to cise program was interrupted (33. dietary (41. funnel SDs of change scores in control and exer. In one of these studies (36). Exercise modality (aerobic. there was a 1. assessment (39). session duration. estimates for the Some studies were excluded because the when analyses were repeated. NOVEMBER 2006 2519 © . blood lipids (LDL SDs in the two groups. Owing to the limited number of (39. randomized.05) or. control in each study as a percent. its effect was mean percent effects.52. The baseline cisers. tween studies was estimated where possi- tracted any measures of body mass (in. study. P value of the outcome statistic or from cluded as main effects only. into equal groups is 2. parallel-group. we also limited the covariates to plots of the inverse of the SE of the esti- DIABETES CARE. HDL cholesterol.59).60.2. Waist circumference was the weighting factor is the inverse of the cointervention was included as a binary either the circumference (in centimeters) square of the sampling SE of the statistic. equivalently. We included studies with two steps on this scale. for exclusion were as follows: subjects modeling procedure (PROC MIXED) in When different scales were used in were a combination of diabetic patients the SAS (version 8. Exercise intensity fixed-effects model for these variables. Finally. fasting glucose. its effect was evaluated for sensitivity was measured using the insulin randomization. visceral fat mass. VOLUME 29.52. 1 was a randomized crossover trial.47.46. body mass. (38. reported a significant reduction (P ⬍ mally distributed variable dichotomized since the wide range in baseline values 0. and triglycerides). healthy diet and in which there was a re.04) model was simplified.05 or P ⬎ ercise. subjects was included as a numeric effect methodological differences.41. all fixed effects were in. Insulin and 8 were controlled trials with unclear achieved a 5). ⬎85% 1 repetition maximum.41. and magnetic resonance imaging statistic from the various studies. son.3 SDs. tance. NUMBER 11. postpran. hydrostatic weighing The main outcome from meta-analysis is a ⱖ12 weeks) to account for the possibility (57.05). To limit the num. fasting insulin. Sex of the between studies may reflect systematic pare eight exercisers with eight nonexer.60. the values of all outcome statistics and ble as one or more random effect. although the ities between estimates prevented conver- Numerous studies were excluded on standardized effects and their confidence gence on a solution).47. fat mass (including fat mass their SEs. variation (heterogeneity) within and be- sensitivity). so it was included or the BMI (weight in kilograms divided was assessed with diaries in all but one after log transformation and its effect was by the square of height in meters) study (43).63. estimation from skinfolds weighted mean of values of the outcome that changes in A1C would require 8 –12 (47. weekly fre. making full effects removed from the model were pro- control group consisted of healthy sub. We included studies inferential information reported for one and that might be expected on physiolog- that had at least one measure of glucose or more outcome statistics was either a P ical grounds to moderate the effect of ex- control (A1C.46. Snowling and Hopkins training programs on type 2 diabetic pa.48. for this rea.64. controlled mum oxygen uptake.50.56) or glucose concentration at a trials.50. total cho.50). and insulin 0. aimed at reducing bias that might arise insufficient estimates of the measure to lesterol. resis. rived from analysis of posttest means and produce a solution with the full fixed- and skinfold sums). different studies for a similar measure.51. (derived from the unweighted mean of sensitivity.65).62).53. use of the P values in all studies. variable. NC).50. the within-study variances) because the circumference. 18 were through 5 (aerobic exercise ⬎80% maxi. this variable was approximately log kilograms) (38 – 45. Fasting insulin was also thors provided no values for A1C but difference between the means of a nor. Dietary compliance normally distributed. We adopted this ap- of the mean effect (36) and/or its SE (37) evaluated for two between-subject SDs proach with postprandial glucose. Baseline mean value of the given measure sure for estimation of standardized effects Only two studies were excluded because was included as a covariate to control for and used back transformation to estimate of insufficient data to calculate magnitude the effect of disease severity. total time spent exercising during the Body mass was either the mass (weight in duction in body mass in at least the con. The remaining unexplained true dial glucose. where weeks to plateau (55). Body fat included total fat talized and provided with food. total mass and fat at specific sites determined exercise time was replaced in the model by dual X-ray absorptiometry Analyses by study duration (two levels: ⬍12 and (39.44. no studies specific time (42.65).05) using a nonparametric test to com. irrespective of P value. cise groups. the presence or ab. In the other (37). resistance exercise 48. homeostasis model a dietary cointervention in which the in. and waist trol. but the confidence limits for group exercised (25–29).34).65) or the waist-to-hip ratio The SE was derived from either the CI or studies available. the exer.59). For these studies we ex.44. ber of covariates in the model. evaluated for a doubling of exercise time.5% (coded as proportion of male subjects in mean value could not be included in the decrease in concentration of A1C in 14 the study [range 0 –1]).57– 63) trol group (38 – 43). the fixed-effects grounds of no control group (8 –18). Cary. SAS Institute. sensitivity index (57). vided by a traditional fixed-effects meta- jects (19 –25) or because the control The meta-analyses were performed analysis. sence of statistical significance (42–53). limits showed little change (⬃⫾0. For studies where the only those that were included in most studies tients were eligible.52).50. When cluding BMI). or combined) was the most impor. and study euglycemic glucose clamp (43. these effects are less trustworthy. (46. body fat. were de. exercisers relative to 10 nonexercisers was included as a numeric effect having Postprandial glucose was measured using (P ⬎ 0. quency. the random-effect meta-analysis failed to as percent body mass.61). value inequality (usually P ⬍ 0. in which patients were hospi. lowing a glucose challenge (40. For each outcome measure. scribed a caloric-restriction or other duration were included in the model as a and insulin tolerance test (49. meta-analyzed the log-transformed mea- icantly increase physical activity (35). This strategy was effects model (either because there were cholesterol.58).57. hyperinsulinemic- tervention and control groups were pre.50. we then and program participation did not signif. and blood from adopting different computational include in the analysis or because dispar- pressure (systolic and diastolic). tant effect in the fixed-effects model. the au.

Six of the 27 publications included in the of magnitudes. a small additional benefit of exercise for large. or small meta-analysis (Table 1) provided two out.2 for small. All studies ap. but the large degree of un. The effect generally negligible or small. moderate. Longer (i. (39 – 42. aerobic exercise had a clear but small bias based on asymmetry in the funnel Eight studies with a total of eight benefit for total cholesterol. allows for the true effect to be small to In the additional analysis of the effect 2520 DIABETES CARE. One study The effects of initial mean value of A1C fects were interpreted using thresholds of with two outcomes did not mention and fasting glucose show that there was 0. and dropouts (59).9 ⫾ 1. respectively (42). e. these pairwise SD (derived as square root of unweighted plain dropouts. Means and be.e. tendance at exercise sessions was stated patients with increased disease severity. mates and too wide a range in the SEs for intensity of 3.7 on the 1. giving 4 –18 estimates for the effect sensitivity. otherwise.g. “met the requirement” was indicated try and blood pressure could not be es- cent trends in inferential statistics (e. there of combined exercise on insulin sensitiv. insulin other effects were unclear or trivial. Effects of exercise total duration of exercise was generally stantially positive and negative were both The effects of exercise on the various out. postprandial glucose.59. cise. men and in A1C with all three exercise modes. baseline A1C 8.50. showing resistance training (Table 2.. Bias in the standard. in either trivial or unclear.g. lation to exercise adherence. accounted for the between-study varia- training on systolic blood pressure and 18 certainty (only one study contributed) tion in effects of exercise. but the uncertainty al- effects by expressing the uncertainty in tion-to-treat basis (i. In keeping with re. years.org). all expressed in had a moderately harmful effect on one Descriptive statistics standardized units with an interpretation measure of glucose control. Higher exercise intensity study characteristics.34.. and 1–5 for combined aerobic.. whereas the effects on blood lipids were the modifications are based primarily on tendance rate was high (mean 86%). as 0. otherwise. all three and one because of an unrealistically ranging from 5 to 104 weeks. ized effects was negligible and not cor. shown in Table 2. modes of exercise produced trivial or un- small SE (60).61). a total train. and 0. and fasting insulin). HDL choles- dardized (Cohen) effects (66) by dividing tervention. 3). 3. all groups combined (64). 0. and diastolic blood pressure (Table by the average baseline between-subject four outcomes did not adequately ex.41. ful effects to the effect of exercise.8 or of small benefit. Aerobic and combined scatter away from the center of the plot). ⬎5%).50. proportion of male subjects 0. combined Meta-analyzed effects for each mea. 0.53. The effect of congruence with Cohen’s thresholds for two studies it was “good” (58. and 1. the other effects of sex were effect was deemed unclear if its CI over. Table 3 shows the time would have little further effect on RESULTS meta-analyzed means and the effects of any measures.5 ⫾ the exception of a small benefit of com- that presumably represent computational 1. the effects were unclear.e.0 ⫾ 0. Twelve studies had no comment timated. and all are consistent lapped the thresholds for substantiveness with trivial or small differences. For studies in which at. fects on blood pressure. VOLUME 29. The ing). although the rate was differences between the exercise modes mean of variances). most of unexplained differences between studies of aerobic training. and its training. at.57. Studies included in the meta. proportion using medication for di. There were too few esti. male relative to female subjects for in- ences about true (population) values of pear to have been analyzed on an inten. fasting glucose. ing time of 58 ⫾ 44 h. ial effect. moderate. outcomes had no dropouts.55 ⫾ exercise had clear small or moderate ef- Six estimates were thereby excluded. low: 2 of 12 and 1 of 13 in exercise and were trivial or unclear. in disease severity on the other measures correlation coefficients (available at one it was “very good” (49). abetes 0. duration of diabetes 4. Diet cointervention con- comes (via multiple groups. sulin sensitivity. while the effects shown in Table 2: five because of unreal.to 5-point In comparison with resistance exer- any firm conclusion about publication scale.5. For the anthropometric mea- estimate were examined qualitatively for characteristics of the 1. hen’s thresholds of 0. An excluding noncompliant subjects) in re.71 ⫾ 0. 2 of rected.2.47. 2–7 for resistance the effects were clearly beneficial and of represented by the random effect were training. only one effect of exercise was un- evidence of outliers (points judged visu. respectively. a modification of Co.003 subjects from sures. for its effect on A1C).. respectively (42).3%. owing to the large number of 15 and 0 of 15 in exercise and control Moderating effects of study degrees of freedom in the estimate of the groups. and in com- plot.48. NUMBER 11. or aerobic and combined train. (69). we made magnitude-based infer. NOVEMBER 2006 © .8 (66).2. For ferred several small beneficial and harm- women.6 ⫾ of resistance exercise were unclear. on exercise attendance. studies with 19 outcomes had dropouts exercise had a clear but small benefit for sure in each study were expressed as stan. trivial. There were clear but small reductions and beneficial.Effects of exercise training on type 2 diabetes mate of the effect versus the value of the tween-study SDs for the study-mean moderate.6. ing glucose. Sixteen parison with aerobic exercise. without lows for this effect to be trivial through the effects as 90% confidence limits. along with the meta. mainly unclear. With istically large positive or negative effects 1.and 6-month durations of all other measures of glucose control (fast. There was a large benefit for 67).51. and baseline fasting glucose 9.38. small to moderate magnitude.7 mmol/l. the 27 studies were as follows: age 55 ⫾ 7 clear and the remainder were either trivial ally to be more than ⬃4 SDs of horizontal years. and in one of glucose control and on anthropome- http://newstats. control groups.62) analysis had an intervention duration aerobic exercise on triglycerides. body mass. the magnitude of the come measures expressed as changes in and the one small harmful effect had effect was reported as the magnitude of its absolute or percent units in each study are confidence limits consistent with a triv- observed value (68). Magnitudes of the standardized ef. A further doubling of exercise analyzed mean effects. that the meta-analytic model adequately were 4 estimates for the effect of aerobic ity was large. Two studies with a total of terol. For all other outcomes.60). bined exercise on HDL cholesterol and or transcriptional errors (38. and 4 of 85 in characteristics SD. if the chances of the effect being sub. explained as being unrelated to the in. and a training clear effects on blood lipids. associated with unclear or trivial effects.

†including a diet high in fish. 10 exercises. 50–85% 1 RM Honkola et al. 2 F 14 M. 2 F Yes† 3 8 40 16 3 50–65% VO2max Fujii et al. repetition maximum. 29 F 28 M. 8 F 7 M. . 3 F Yes 3 8 40 16 3 50–65% VO2max Dunstan et al. 8–10 exercises Ishii et al. 7 F Yes 3 13 45 29. 10 reps. 12 reps.2 3 Heart rate 110–140 bpm Yamnouchi et al.5 3 50–70% VO2max Ligtenberg et al. 20 reps. 0 F No 4 52 45 156 3 65–75% VO2max. 5 F No 3 17 75 63. (38) African 62 30 25 Yes 3 26 30 39 3 Low impact aerobic American Boudou et al. 9 exercises. 3 F Yes 7 7 120‡ 14 1 Exercise group 19. 50–85% 1 RM Dunstan et al. 10–20 reps. (58) European 53 13 12 No 6 17. (42) European 54 10 12 Yes 3 10 60 30 3 4. 3 F 9 M. 2 F 11 M. (44) European 51 8 M.5 52 45 135. 5 exercises Loimaala et al. 0 F No 3 10 60 30 3 2 sets. 10 reps.50 3 2 sets. 10–12 reps.8 km/h Verity and Ismail (62) European 59 0 M. 48 9 M. 4 F 9 M. 45 s each with 15 s rest Tessier et al. 0 F No 2 104 45 156 4 75% VO2max © Vanninen et al. (39) European 67 10 M. 4 F 10 M. (59) European 61 0 M. (43) Japanese 42 8 M. 0 F 24 M. 12 F No 3 12 55 33 3 65% VO2max Ronnemaa et al. 6 F 5 M. 40–50% 1 RM Combined training Balducci et al. 10 exercises European Castaneda et al. 3 F 5 M.5 45 78. (38) African 62 31 27 Yes 3 13 30 19. 9 F 0 M. (60) Hispanic 66 9 M. 8 reps. 0 F 25 M. ‡estimated. (47) European 52 14 M. (49) European 62 25 26 No 3 6 50 15 4 60–80% VO2max Mourier et al. (40) European 53 10 M. 7 F 11 M. 20 F 12 M. (46) Japanese 49 9 8 No 5 5 60 25 2 2 sets. 0 F 9 M. 6 exercises Cuff et al. 19 F No 3 16 45 36 4 3 sets. 9 F No 3 16 60 48 3 60–79% VO2max.200 steps/day. 12 F 7 M.5 52 45 135. 11 F Yes 3 14 50 35 3 65–70% VO2max Khan and Rupp (63) European 50 21 18 No 5 15 50 63 2 40–60% VO2max Lehmann et al. (65) European 61 28 M. (64) European 53 21 M. NOVEMBER 2006 Resistance training Baldi and Snowling (57) Polynesian.Frequency Duration time Total Intensity Study (ref. 0 F No 3 8 45 18 4 75% VO2max 2 days/week ⫹ 85% VO2max 1 day/week Cuff et al. (52) European 45 8 M. 6 F No 5 26 30 65 2 40% VO2max Giannopoulou et al.) Ethnicity (years) Exercise Control vention* (weeks⫺1) (weeks) (min) time (h) rating Intensity description Aerobic training Agurs-Collins et al. (56) Japanese 40 6 M. (64) European 54 0 M. 0 F 8 M. RM.50 4 3 sets. 11 F 0 M. (42) European 56 13 15 Yes 4 10 60 40 3 4. 6 F 6 M. 3 sets. 12–15 reps. (48) European 69 12 M. 9 F No 3 16 75 60 3 60–70% heart-rate reserve on 5 machines. 5 F No 3 8 60 24 2 2–3 sets. 10 F 0 M. (45) European 65 12 M. 10–15 reps. (53) European 59 8 M. (40) European 53 8 M. 9 exercises. 7 F Yes 3 26 45 58.500 steps/day Wing et al. 12 reps. 16 F No 3. (39) European 67 10 M. NUMBER 11. control group 4. (41) European 57 0 M. 6 F 6 M. 6 F No 3 13 90 58. 0 F No 3. 1 set. (61) European 56 6 M.5 3 Low impact aerobic American Agurs-Collins et al. 27 F No 3 52 60 156 3 40–80% heart-rate reserve.75 4 65–80% heart-rate reserve DIABETES CARE. VOLUME 29. 12–15 reps. 9 F No 3 16 75 60 2 Low impact aerobic Dunstan et al.75 3 70% VO2max Skarfors et al. 2521 Snowling and Hopkins Table 1—Descriptive statistics of studies included in the meta-analysis Sample size (n) Exercise intervention Dietary Session Age cointer. 2 sets. 15 F No 3 22 45 49. 2 F No 3 8 60 24 3 Circuit training: 8 aerobic ⫹ 7 resistance exercises. 5 F 0 M. 10 exercises.8 km/h Wing et al. 2 sets. 8 exercises Maiorana et al. 5 exercises Dunstan et al. (59) European 61 0 M.5 4 75% VO2max Raz et al. 17 F 0 M.25 4 3 sets.2 3 Heart rate 110–140 bpm Vanninen et al. (69) European 54 24 M. (51) European 57 7 M. 9 exercises *Applies to experimental and control groups. 40–60% 1 RM. (50) European 46 10 11 No 3 10 55 27. 50–55% 1 RM Dunstan et al. 0 F 8 M.

0.1 ⫾ 2. the cient studies to allow us to conclude that fits resulting from combining aerobic and reductions were small (0.3 6 months ⫺2.1 ⫺1. (50) ⴚ2.3 ⫾ 7. NUMBER 11. ⫺5) 28 (9.5 ⫾ 1.7 ⫾ 2.5 ⫾ 0.6 — 61 ⫾ 38 ⫺8 ⫾ 48 ⫺0.0 ⫾ 0.7 (⫺1. (44) ⫺0.5 ⫺0.3 ⫾ 0. ⫺0.3.0 0.26).) A1C (%) Fasting (mmol/l) Postprandial (%) Insulin sensitivity (%) Fasting insulin (%) Body mass (%) Aerobic training Agurs-Collins et al.5 — — — — ⫺2. (47) ⫺0.7 ⫾ 1. some related risk factors for complica- dence limit).Effects of exercise training on type 2 diabetes Table 2—Changes in measures of blood glucose control and related physiological parameters for the individual studies included in the meta-analysis and for the meta-analyzed means after controlling for moderating effects of study characteristics Blood glucose Study (ref. there is in studies lasting ⬍12 weeks was only CONCLUSIONS — There are suffi.3.7 Women 0.3 ⫾ 1.9 Meta-analyzed mean (upper.0.4 — — — 1.2 ⫺1.2 ⫾ 0.1 (⫺7.2 — — — ⫺0.6 ⫾ 1. 10) 0. visceral adipose tissue.1 ⫾ 0.3.2 ⫾ 0. and the differ.1 ⫾ 1. ⫺0. S.5 ⫾ 0.5 Meta-analyzed mean (upper.6 ⫾ 0.6 Fujii et al.5 — — 75 ⫾ 45 — ⫺5. 49) ⫺20 (⫺41. ⫺1. (⫺0.4 Loimaala et al.1 Dunstan et al.6 — — — — ⫺3 ⫾ 12 Ishii et al. M.5 (⫺2. (53) — 0. ⫺0. 8) ⫺1.1.3 ⫺7 ⫾ 10 — ⫺28 ⫾ 33 ⫺0. Data in bold are outliers excluded from the meta-analysis.1) ⫺0.3 ⫾ 1.5 ⫾ 0. (40) (diet) ⫺0.6 — — — — — Maiorana et al.2 1.9 ⫺2.8 Honkola et al.7 ⫾ 1.1 ⫾ 1.8 ⫾ 0. the mean effect 0. of study duration on A1C.4 ⫺17 ⫾ 20 — ⫺7 ⫾ 39 ⫺3 ⫾ 13 Skarfors et al.5 Cuff et al.5 ⫾ 0.3 ⫾ 3.8 0.5 ⫾ 1.9 ⫺8 ⫾ 8 — — ⫺1. (52) ⫺3. (51) ⫺1. (60) ⫺1.5 ⫺1.1 ⫾ 1.6 ⴞ 0. some evidence of small additional bene- 0.2 ⫾ 1.7 ⫾ 1.2 — — — 0 ⫾ 12 Tessier et al. resistance. (46) ⫺0. (43) — ⫺0. ⫺0. 132) ⫺5.1) ⫺9 (⫺13.5 ⫺0.8 (⫺1.0 ⫾ 0.4 Dunstan et al.42 ⫾ 0.4 ⫾ 0.3 Lehmann et al. and combined exer. VOLUME 29. (56) — — ⫺23 ⫾ 16 — — — Giannopoulou et al. (49) ⫺0. (59) ⫺0.2 6 months ⫺0.6 — ⫺4 ⫾ 20 13 ⫾ 20 0.3 (⫺1.2 ⫾ 1. (65) ⫺1.6 ⫺0.8 ⫾ 1. (61) ⫺0.0.5 8 ⫾ 29 — 13 ⫾ 45 — Vanninen et al.1.0 ⫾ 5.1 ⫾ 2.5 ⫺1 ⫾ 21 — ⫺28 ⫾ 44 ⫺4 ⫾ 13 Verity and Ismail (62) 0.5 ⫾ 2.0 0. 280) ⫺7 (⫺63. ⫺0.5 (⫺1.4%.6 ⫾ 1.1 ⫾ 0.16 and aerobic.9 ⫺0.4 ⫾ 0.0 ⫾ 1.2 Khan and Rupp (63) ⫺0.5 ⫾ 0.2 ⫾ 0. 64 ⫾ 12 M ⫺18 ⫾ 30 ⫺4 ⫾ 16 Wing et al. ⫺0. NOVEMBER 2006 © .8 ⫾ 1.2 ⫾ 1.6 ⫾ 2. ⫺0.9 ⫾ 0.5 — — — ⫺0.5 (⫺0.6 ⫾ 5.4 ⫾ 1. (48) ⫺0.19 ⫾ 0. (41) ⫺1.4 — — 45 ⫾ 33 — 0.4 ⫾ 1.9 ⫺1.1 ⫾ 0.23 ⫾ 0. (39) 3 months ⫺0.1 ⫺0.1 ⫺9 ⫾ 10 — — ⫺1.6 Castaneda et al. 10) 12 (⫺6. (69) ⫺1. whereas the A1C reduction tions of diabetes.7 0. 0.4 — — — ⫺7.7 0. resistance exercise.5 (⫺1.7 Boudou et al. 1.0 ⫾ 0. 4) 106 (12. glucose infusion rate.5 ⫾ 2.2 ⫾ 1.2 ⫾ 1.6) ⫺2 (⫺13. ⫺0.8 ⫾ 0.5 Ronnemaa et al. cise have small to moderate beneficial ef- of all three modes of exercise in studies ence between the effects of long and short fects on glucose control in type 2 diabetic lasting ⱖ12 weeks was a reduction in studies was possibly trivial or small patients and small beneficial effects on A1C of 0.9 ⫺8 ⫾ 17 — ⫺66 ⫾ 71 ⫺0. (45) ⫺0.4 ⫾ 1. G.1 ⫾ 0.1 ⫾ 1.2 ⫾ 10.5 — ⫺5 ⫾ 18 ⫺8 ⫾ 29 0.4 — — 19 ⫾ 32 — ⫺3.0 — — — ⫺2 ⫾ 11 Yamnouchi et al.2 ⫾ 4. subcutaneous adipose tissue. (64) Men ⫺0. unless otherwise indicated. 33) ⫺31 (⫺57.8 Meta-analyzed mean (upper. In standardized units.7 — 45 ⫾ 10 G.6 ⴚ0.3 ⫾ 1.5 ⫺9 ⫾ 10 22 ⫾ 32 ⫺63 ⫾ 52 1.6 ⫾ 1. (58) ⫺0.4 ⫾ 0.2) ⫺1.0) lower 90% confidence limit) Resistance training Baldi and Snowling (57) ⫺0.0 ⫾ 10.1 — — — ⫺2.22.1 ⴞ 0.4) ⫺0. 2522 DIABETES CARE.5 ⫺0.2 2 ⫾ 16 54 ⫾ 34 2 ⫾ 40 ⫺2 ⫾ 12 Raz et al.4 ⫺1. metabolic clearance rate. ⫺2.6 ⫾ 0.8 ⫾ 9.1 — — — ⫺4.5 ⫾ 1.0 ⫾ 4.0 ⫾ 1. Furthermore.9 ⫾ 2.3 ⫾ 12. (42) A ⫺0. (38) 3 months ⫺1.1 ⫺1 ⫾ 17 — ⫺16 ⫾ 20 ⫺1 ⫾ 11 B ⫺0.7 — — — — ⫺2.5) lower 90% confidence limit) Data are mean ⫾ 90% confidence limit.7 ⫺11 ⫾ 6 — ⫺17 ⫾ 42 ⫺2 ⫾ 11 Dunstan et al.4) lower 90% confidence limit) Aerobic plus resistance training Balducci et al. (40) ⫺0.7 Cuff et al.6) ⫺6 (⫺15.8 0.3 ⫾ 2.6.4 ⫺0.2 0.0 ⫾ 1. V.4 — — ⫺67 ⫾ 42 ⫺1 ⫾ 12 Ligtenberg et al. respectively). (59) ⫺0.8 — — ⫺6 ⫾ 36 — — Mourier et al.3% (mean ⫾ 90% confi.8 Dunstan et al.5 (⫺2.9 ⫾ 1.9 ⫾ 1.

4 — — — — — — — — — — — — — — ⫺0. 0.14 ⫺0.8 (⫺4.1 — ⫺4.2 V ⫺1.7 7.8 2.16 ⫺0.6 — — — — — 0.1 ⫾ 0. ⫺1) ⫺1.13 (0.4 — — ⫺0.5 0.5 ⫾ 2.5 4 ⫾ 13 2.6 2.5 ⫺0.1 ⫾ 0.9 ⫾ 0.3 0.07 0.12 ⫺0.05 ⫾ 0.3 ⫺0.5 0.5 — 0.8 — — — — — — — — — — — — — — 0.05 ⫾ 0.4 ⫾ 0.1 ⫾ 0.6 ⫾ 0. There was little syn.4 0.9 ⫺4.00 ⫾ 0.04 ⫾ 0.3) 0.3 ⫾ 3. ⫺0.4 ⫾ 9.3 ⫾ 0.2 ⫾ 1.0) ⫺3.3 ⫾ 0.11 ⫺0.1 ⫾ 0.7 0. The effect of duration of extra benefit from more exercise.4) 0.6 ⫾ 5.1 ⫾ 0.9) ⫺1.13 ⫺0.3.03 ⫾ 0.5 ⫺0.06 ⫾ 0.5 (⫺9.07.5 0. tent with the turnover time for Hb. 2.4 S.4.0 ⫾ 0.12 0.5 0.1 ⫾ 3.2 ⫾ 6.09 ⫺0.15 ⫺0. 10) ⫺2.0 0.4 ⫺0.7 ⫾ 4. NOVEMBER 2006 2523 © .3.0 — — ⫺0.0 ⫾ 18 — — — — — — — — ⫺0. most patients reaching a stable state in efit for those with more severe disease.09 ⫺0. 0.6 — 0.27 0.0 ⫾ 0.3 (⫺1. In the meantime.8) ⫺5. This finding is consistent with clear that there is a small additional ben.2 (⫺0.7 ⫺0.0 ⫾ 4.1.20 ⴞ 0.5 ⫺0.7 0.05 ⫾ 0.1 ⫾ 8.3. especially the effect of sex of the that the effects of diet will add linearly to on A1C and the other measures was at patients.3 (⫺6. — — — — — — — ⫺3.9 — — ⫺15 ⫾ 37 — ⫺3. ⫺1.0) 0.4) 0.20 ⫺0.2 ⫾ 0.6 ⫾ 0.3) 0.9 — ⫺7.9 — ⫺7.2 ⫺5.17 ⫾ 0.01.6.7) 0.02 (⫺0.01 ⫾ 0.3 ⫾ 0. Snowling and Hopkins Table 2—Continued Body fat (%) Waist Total LDL HDL Blood pressure (mmHg) circumference cholesterol cholesterol cholesterol Triglycerides Fat mass Abdominal fat (%) (mmol/l) (mmol/l) (mmol/l) (mmol/l) Systolic Diastolic — — ⫺0.03 ⫾ 0.5 ⫾ 0.5 — 0.8) ⫺10 ⫾ 8 — ⫺3.8 ⫾ 5.8) ⫺1.2 ⫾ 0.19 ⫺0.1 ⫾ 0.3 ⫾ 3.08 ⫺0.4 (⫺0.9 ⫾ 6.04 ⫾ 0. 0.8 (⫺3.8 2.5 0.1 ⫾ 0.3 ⫾ 0.4 ⴞ 1. NUMBER 11. 0. ⫺2) ⫺0.2 ⫾ 0. 3.6 — ⫺0.5 ⫾ 5.4 ⫺0.3 (⫺0.00 ⫾ 0.7) 0.2 ⫾ 0.6 0.2 ⫾ 0. 0.8 ⫺0.9 — ⫺0.4 ⫾ 0.06 ⫾ 0.0 (⫺4. affect the outcomes of an exercise pro.10 ⫾ 0.6 2.1 (⫺0.4.6 (⫺9.0 ⫾ 9.2 ⫾ 0.5 0.6 — — — — — — ⴚ48 ⴞ 15 V — — — ⫺0.2.0 ⫾ 0.5) 0.0 — — — ⫺0.6) ⫺0. 0.4.05) ⫺0.7 ⫾ 4.7 ⴞ 0.6 ⫺0.2 ⫾ 0.1) More research is needed for confident exercise to patients.3 — — — — 0.4.0 ⫾ 7.5 — ⫺0. 0.3 0.4 ⫾ 0. ⫺1. although the apparent best trivial.3 — — — — — — — — — — — ⫺2 ⫾ 16 ⫺8. 1.05 ⫺0.5 ⫺0.4 ⫺5.7 ⫾ 2.02 (⫺0.0 ⫾ 0.6 ⫺0.0 ⫾ 4.24 — — — — — — — — — — — — ⫺15 (⫺26.3 ⫾ 0.7 — — ⫺5.16 0.5 ⫾ 0.2 ⫾ 0.0 ⫾ 0.05 ⫾ 0.8 ⫾ 0.7 — — — ⫺0. but.04 ⫾ 0.2 S.4 ⫾ 4.2 ⫾ 0. ⫺1.2 ⫾ 0.6 0.5 — — — — — ⫺0.0 V — — — ⫺0.1 ⫾ 0.6 — 0.06 0.1 ⫾ 0. 0.1 — — 10 ⫾ 41 ⫺13 ⫾ 18 S.0 0.7 ⫺0.5.3 (⫺5.1 0.1 (⫺0.20) ⫺0.5 0.3 ⫺3. 0. the exercise program on A1C was consis- conclusions about other factors that could ergistic effect of a dietary cointervention. a vention on LDL and total cholesterol need their exercise programs and gaining no reassuring finding for those prescribing to be clarified.7.6) ⫺1.5 ⫾ 6.4 ⫺4. 0.7 0.2 ⫾ 4. this finding can also reassure clinicians otherwise.02 ⫾ 0.5 (⫺7.26 — — — ⫺11 (⫺20.07) 0.5 ⫺1. 0.3 ⫺0.5 ⫾ 8.0. — — — — — — — ⫺16 ⫾ 20 V — ⫺5.3 ⫾ 0.4 — — — — — — — ⫺0.3 ⫾ 6.1 (⫺0.9.2 — — 0.3.09 — — — — — — ⫺0.5 ⫺8.9 S.2 ⫾ 3.2 ⫾ 0.4 ⫾ 0.03.8 ⫾ 6.3 ⫾ 1.0 ⫾ 2. 0.5 ⫾ 0.01 ⫾ 0.08 ⫾ 0.06 ⫾ 0.2 ⫾ 0.09 ⫾ 0.6.4 ⫺5.9 ⫾ 4.1 ⫾ 0.4 ⫾ 3. small harmful effects of a dietary cointer.2 (⫺3.8 ⫺27 ⫾ 58 — — — — — — — — ⫺4 (⫺16.11 ⫺0. VOLUME 29.8) ⫺5.0 ⫾ 8. — — — — — — — ⫺10.1 (⫺0. 0.2 — 0.2 ⫾ 0.0 (⫺0.8 ⫺0.3 0.3 ⫾ 2.2 ⫾ 9.2 ⫾ 8. An in- DIABETES CARE. 0.6 — 0. it is reasonably those of exercise.11 ⫺0.5 0.7 ⫺3.3 — ⫺40 ⫾ 13 S.0 ⫾ 1.0 ⫾ 7.6 — — 0.1 ⫾ 0.9 ⫾ 0.0) ⫺9. the effect of total exercise time gram. 1.6.5 ⫺0.5 ⫾ 10.6.4 ⫾ 0.6 — ⫺9 ⫾ 29 — ⫺1.8 V — — — — — — — ⫺5.4 ⫾ 0. 0.8 2.0 ⫾ 3.7 ⫺2.4 ⫾ 7.

60 –1. DIABETES CARE. Nontrivial magnitudes are beneficial. NUMBER 11. unless stated otherwise.20. VOLUME 29. even for the simplest model (mode of exercise as the only fixed effect). trivial. 0. 0.20.60. *Random-effects analysis failed to produce estimates.20 – 0. Effects are shown in units standardized by dividing by the baseline between-subject SD averaged over all studies. †Insufficient studies to include study characteristics in random. NOVEMBER 2006 . Shaded cells indicate clear beneficial effects. Cells in boldface indicate clear harmful effects.20.2524 Table 3—Meta-analyzed effects of various modes of exercise and the moderating effects of study characteristics on measures of glucose control and related physiological parameters Effects of exercise training on type 2 diabetes © Data are means ⫾ 90% confidence limit.or fixed-effects analyses. moderate. Italics indicate estimates from a fixed-effects meta-analysis. small. and ⬎1. Magnitudes are based on the following scale: ⬍0. large.

Yale JF.7% in the short term for treated with oral hypoglycemic agents: is R. Gad P: Physical training insulin sensitivity enhanced only in nono. 1218 –1227. Hudson R. sedentary and trained. the practical impli. One possible men and women. 2003 cose tolerance. Ludwig S. Paffenbarger RS Jr: Physical activity and Bonnard RA. Zinman B. NUMBER 11. 1991 Kilpatrick K. dependent diabetes mellitus. Zois CE. Carta Q. Ragland DR. Weinstock RS. Bruce CR. explanation is that patient compliance 832– 837.0% was associated with 8. Tesson F: Influence of Nunnold T. Parson HK. Vitali S. Vasquez B. Kohrt WM. Prud’homme D. Dalsky GP. 1997 mechanism of improved glucose control drug or insulin therapy (0. Broderick T. Diabetes 28 bined small effects of drug therapy. in intensity.5–3. fat and improves insulin sensitivity in Miller CS. Meltzer S. type 2 (non-insulin-dependent) diabetes diabetic patients. 2005 as we know. Eur large study with clearly defined monitor. Bjorntorp P: The effects DIABETES CARE. 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