Diabetes Mellitus
Diabetes Mellitus
Diabetes Mellitus
O R I G I N A L A R T I C L E
High-Intensity Resistance Training Improves Glycemic Control in Older Patients With Type 2 Diabetes
DAVID W. DUNSTAN, PHD1 ROBIN M. DALY, PHD2 NEVILLE OWEN, PHD3 DAMIEN JOLLEY, MSC2 MAXIMILIAN DE COURTEN, MD1 JONATHAN SHAW, MD1 PAUL ZIMMET, PHD1 ommend the use of resistance training as part of a well-rounded exercise program for older individuals. However, the role of progressive resistance training as a treatment regimen for improving the metabolic prole of older patients with type 2 diabetes has received little attention. Given that the prevalence of type 2 diabetes increases with age (9) and that aging is associated with a reduction in muscle strength and metabolic control, both of which are inuenced by the progressive age-related decline in muscle mass (sarcopenia) (10), resistance training may represent an effective exercise alternative for older adults. Furthermore, several studies in older patients without diabetes have demonstrated that resistance training can improve muscular strength and may be an effective tool for the prevention of age-related sarcopenia (1113). Due to the limited information on the role of resistance training for older patients with type 2 diabetes, it has been recommended that resistance training programs use moderate weights and high repetitions (7). However, it appears that the impact of progressive resistance training on muscle mass and muscle strength in both young and older individuals is more pronounced if higher training intensities (70 and 90% of the onerepetition maximum strength [1-RM]) are used (14). In older adults without diabetes, high-intensity progressive resistance training programs have been reported to have signicant effects on daily energy expenditure (15), body composition (16), and insulin sensitivity (17,18). To date, no study has examined the long-term effects of high-intensity progressive resistance training in combination with moderate weight loss in subjects with type 2 diabetes. The absence of such data has precluded specic recommendations by the American Diabetes Association with respect to the merits of highintensity resistance training for older individuals with type 2 diabetes (7). The aim of this randomized controlled trial was to examine the effects of a 6-month high-intensity progressive resistance
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OBJECTIVE To examine the effect of high-intensity progressive resistance training combined with moderate weight loss on glycemic control and body composition in older patients with type 2 diabetes. RESEARCH DESIGN AND METHODS Sedentary, overweight men and women with type 2 diabetes, aged 60 80 years (n 36), were randomized to high-intensity progressive resistance training plus moderate weight loss (RT & WL group) or moderate weight loss plus a control program (WL group). Clinical and laboratory measurements were assessed at 0, 3, and 6 months. RESULTS HbA1c fell signicantly more in RT & WL than WL at 3 months (0.6 0.7 vs. 0.07 0.8%, P 0.05) and 6 months (1.2 1.0 vs. 0.4 0.8%, P 0.05). Similar reductions in body weight (RT & WL 2.5 2.9 vs. WL 3.1 2.1 kg) and fat mass (RT & WL 2.4 2.7 vs. WL 2.7 2.5 kg) were observed after 6 months. In contrast, lean body mass (LBM) increased in the RT & WL group (0.5 1.1 kg) and decreased in the WL group (0.4 1.0) after 6 months (P 0.05). There were no between-group differences for fasting glucose, insulin, serum lipids and lipoproteins, or resting blood pressure. CONCLUSIONS High-intensity progressive resistance training, in combination with moderate weight loss, was effective in improving glycemic control in older patients with type 2 diabetes. Additional benets of improved muscular strength and LBM identify high-intensity resistance training as a feasible and effective component in the management program for older patients with type 2 diabetes. Diabetes Care 25:1729 1736, 2002
xercise, along with diet and medication, plays an important role in the management of type 2 diabetes. However, whereas the therapeutic benets of exercise have been studied extensively in middle-aged men and women with type 2 diabetes (13), little is known about the impact of exercise training in older people with this condition. Aerobic
or endurance exercise programs have been traditionally recommended for older patients with type 2 diabetes and have been associated with weight loss, improved glucose tolerance, and cardiovascular tness (4 6). Recent position statements from both the American Diabetes Association (7) and the American College of Sports Medicine (8) also rec-
From the 1International Diabetes Institute, Melbourne, Australia; the 2School of Health Sciences, Deakin University, Melbourne, Australia; and the 3School of Population Health, University of Queensland, Brisbane, Australia. Address correspondence and reprint requests to Dr. David Dunstan, International Diabetes Institute, 250 Kooyong Rd., Cauleld, Victoria, Australia 3162. E-mail: [email protected]. Received for publication 26 May 2002 and accepted in revised from 12 July 2002. Abbreviations: 1-RM, one-repetition maximum strength; HOMA, homeostasis model assessment; LBM, lean body mass; RT & WL group, high-intensity progressive resistance training plus moderate weight loss group; WL group, moderate weight loss plus a control program group. A table elsewhere in this issue shows conventional and Syste ` me International (SI) units and conversion factors for many substances.
training program, combined with healthy eating designed to elicit moderate weight loss, on HbA1c and body composition in older adults with type 2 diabetes. More specically, we asked the following questions: 1) is a high-intensity progressive resistance training program feasible for previously sedentary, overweight older patients with type 2 diabetes? and 2) does high-intensity progressive resistance training combined with moderate weight loss reduce HbA 1c , increase muscle strength and lean body mass (LBM), and decrease fat mass in older patients with type 2 diabetes compared with a control program (exibility exercise) plus moderate weight loss? RESEARCH DESIGN AND METHODS Men and women, aged between 60 and 80 years, with treated (diet and/or medication) type 2 diabetes were recruited from the clinics of the International Diabetes Institute and by a local media campaign. Subjects were overweight (BMI 27 kg/m2 and 40 kg/ m2), were sedentary (no strength training and 150 min of brisk walking/moderate exercise per week and 60 min of vigorous exercise per week in the preceding 6 months), had established (6 months) but not optimally controlled type 2 diabetes (HbA1c range 710%), were not taking insulin, and were nonsmokers. After telephone screening, 110 potential volunteers were invited to attend a more detailed screening visit involving a comprehensive medical examination, including medical history, physical examination, resting blood pressure, resting 12-lead electrocardiogram, and HbA1c measurement. Of these, 47 (24 men and 23 women) met the full entry criteria, and 36 agreed to participate in the study. Reasons for exclusion included history or physical ndings suggestive of ischemic heart disease, systemic diseases, uncontrolled hypertension (160/90 mmHg), and advanced diabetic neuropathy or retinopathy. Subjects with severe orthopedic, cardiovascular, or respiratory conditions that would preclude participation in an exercise program or those with a medical condition listed in the American College of Sports Medicine absolute exercise contraindications (19) were excluded. Of the 36 subjects who agreed to participate, 20 had a history of hypertension, 3 had a history of neuropathy, 1 had a history of retinopathy, and 7 reported a history of arthritis.
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Antidiabetic and antihypertensive medications were continued during the study. The study was approved by the International Diabetes Institute and Deakin University Human Research Ethics Committees, and written consent was obtained from all subjects. The study was a 6-month randomized controlled clinical trial, with repeated measurements performed at 3-month intervals. Subjects were randomly assigned to either a high-intensity progressive resistance training plus moderate weight loss group (RT & WL, n 19) or a 2) moderate weight loss group plus control program (exibility exercise) (WL, n 17). Two subjects from the RT & WL group and four subjects from the WL group withdrew from the study during the rst 8 weeks. The reasons for withdrawal included health problems not related to the intervention (n 2) or other commitments that precluded ongoing participation (n 4). One participant from the RT & WL group was placed on insulin treatment within the rst 6 weeks of the trial and was not included in any analysis. Therefore, of the 36 who began the study, 29 subjects (16 [84%] RT & WL and 13 [76%] WL) successfully completed the intervention, yielding a dropout rate of 19%. Healthy eating plan For the initial 4-week baseline period, all subjects were placed on a healthy eating plan, supplying 30% of total energy intake from fat and 10% from saturated fat), with the remainder distributed between carbohydrates and protein. The healthy eating plan was designed to elicit a moderate weight loss of 0.25 kg/week over the course of the intervention and was individually prescribed by a dietitian using two separate 3-day food records performed during the baseline. Compliance with the healthy eating plan was assessed by interviews every 2 weeks with the dietitian and by completion of a weekly food checklist. A 3-day food record was obtained at 3 and 6 months to assess changes in nutrient intake. All nutritional information obtained from food records was analyzed by a dietitian using the Foodworks nutrient analysis software program (Xyris Software, Brisbane, Queensland, Australia).
Exercise intervention During the 6-month intervention, all subjects attended the exercise laboratory on 3 nonconsecutive days per week. Resistance training consisted of a 5-min warm-up and 5-min cool-down period of low-intensity stationary cycling and 45 min of high-intensity resistance training (dynamic exercise involving concentric and eccentric contractions). During the rst and second weeks of training, the resistance was set at 50 60% of each individuals 1-RM. The 1-RM was dened as the maximum amount of resistance that could be moved through the full range of motion of an exercise for no more than one repetition. Thereafter, the goal was to achieve between 75 and 85% of the current 1-RM. Subjects followed an individually monitored progressive resistance training program using free weights and a multiple-station weight machine. Nine exercises were used for training: bench press, leg extension, upright row, lateral pull-down, standing leg curl (ankle weights), dumbbell seated shoulder press, dumbbell seated biceps curl, dumbbell triceps kickback, and abdominal curls. All subjects were required to perform each repetition in a slow, controlled manner, with a rest of 90 120 s between sets. Three sets of 8 10 repetitions were performed for all exercises (except abdominal curls) at each training session. All sessions were supervised to ensure correct technique and to monitor the appropriate amount of exercise and rest intervals. Training workload was increased regularly as tolerated for each muscle group after subjects had successfully achieved three sets of 10 repetitions with appropriate technique. 1-RM testing was repeated every 12 weeks to establish a new baseline. The control program (WL) was designed to provide participative involvement but not to elicit change in muscle strength or cardiovascular tness. Each session involved stationary cycling with no workload for 5 min, followed by a series of static stretching exercises (30 min). Subjects were not blinded to treatment and were informed that improved exibility was an expected outcome. Testing procedures Anthropometry and body composition. Height (cm) was measured using a Holtain stadiometer (Holtain, Crosswell, Wales). Body weight (kg) was assessed us-
ing SECA electronic scales to the nearest 0.1 kg. Waist circumference was measured using a nonelastic measuring tape at the midpoint between the lower border of the ribcage and the iliac crest. Fat mass and LBM were measured by dual-energy X-ray absorptiometry using a DPX-L densitometer (Lunar, Madison, WI). All scanning and analyses were performed by the same operator. The coefcient of variation for repeated measurement was 1.2% for fat mass and 1.7% for LBM. Muscle strength. Before the determination of their initial 1-RM, subjects attended two separate familiarization sessions, where they were shown proper exercise techniques by a trained instructor and given the opportunity to become accustomed to the selected exercises. To determine the 1-RM, each participant initially performed a warm-up set of eight repetitions with a light weight. After the successful completion of a further three to ve repetitions at a moderate to heavy weight selected by the instructor, and after a brief rest (12 min), the workload was incrementally increased until only one repetition with correct technique could be completed. The 1-RM testing on the bench press and leg extension exercises was used to document the respective changes in upper body and lower body strength. Habitual physical activity. Habitual physical activity was estimated using a 7-day physical activity recall questionnaire (20) to measure changes in physical activity patterns. The questionnaire was interviewer administered and the total hours spent sleeping and performing moderate, hard, and very hard activity were used to calculate daily energy expenditure (20,21). The resistance training activity that the RT & WL group participated in as part of the intervention was not included in the nal analysis of the habitual physical activity data. Clinical and laboratory measurements. Resting supine blood pressure was assessed using the Dinamap automatic blood pressure monitor (Critikon, Tampa, FL). Four separate readings were taken at one-minute intervals, and the mean of the nal three readings was recorded. All blood pressure measurements were performed at least 24 h postexercise. Blood samples were obtained from each participants antecubital vein after an overnight fast for the determination of plasma glucose, serum insulin, lipids and
Table 1Descriptive characteristics of the RT & WL and WL groups RT & WL n Age (years) Sex (M/F) Duration of diabetes (years) Oral hypoglycemic medication use (n) Anthropometry Height (cm) Weight (kg) BMI (kg/m2) Waist circumference (cm) Body composition Fat mass (kg) LBM (kg) Blood pressure Systolic (mmHg) Diastolic (mmHg) Serum glucose and insulin Fasting glucose (mmol/l) Fasting insulin (pmol/l) Insulin sensitivity (HOMA) HbA1c (%) Serum lipids Total cholesterol (mmol/l) HDL cholesterol (mmol/l) LDL cholesterol (mmol/l) Triglycerides (mmol/l) Total energy intake (kcal/day) Estimated energy expenditure (kcal/day)*
Data are means SD. *Calculated from 7-day recall.
WL 13 66.9 5.3 6/7 8.8 7.9 10 166.0 9.1 89.5 12.1 32.5 3.8 103.3 11.4 35.6 6.8 49.7 9.5 147 15.5 75 6.4 9.4 2.1 101.9 25.8 20.8 6.2 7.5 1.1 5.7 1.2 1.4 0.3 3.5 0.9 1.8 0.8 1,815 431 3,109 428
16 67.6 5.2 10/6 7.6 5.4 15 167.8 8.7 88.7 10.9 31.5 3.7 105.3 7.5 33.1 7.4 51.8 8.1 145 17.8 78 8.8 9.5 2.3 132.9 63.0 17.7 6.5 8.1 1.0 5.1 0.8 1.2 0.2 3.1 0.8 1.8 0.8 1,783 349 3,022 413
lipoproteins, and HbA1c. All samples were collected at least 48 h postexercise. Serum samples for insulin were stored at 80C until assayed. HbA1c was measured with the Roche Unimate 5HbA1c kit using the Olympus AU600 automated analyzer. Plasma glucose levels were measured enzymatically (glucose oxidase) within 12 h of collection using the Olympus AU600 automated analyzer. Serum total cholesterol, HDL cholesterol, and triglycerides were determined enzymatically on the Olympus AU600 analyzer. LDL cholesterol was calculated from the Friedewald formula (22). Serum insulin was measured using a human insulin specic radioimmuoassay kit (Linco Research, St Charles, MO). Homeostasis model assessment (HOMA) was used to estimate insulin sensitivity from fasting insulin and glucose concentrations (23). Statistical analysis Statistical analysis was conducted using SPSS version 10.0.5 for Windows (SPSS,
Chicago). Independent t tests were used to assess between-group comparisons at baseline. Net differences at 3 and 6 months were calculated by subtracting the within-group changes from baseline for the WL group from the within-group changes for the RT & WL group. Time, group, and interaction effects were examined using a two-way ANOVA or ANCOVA with repeated measures on one factor (time). Fasting plasma insulin levels were log transformed to yield a normal distribution before parametric analysis. All other data were normally distributed. RESULTS Subject characteristics There were no differences in the baseline characteristics of the subjects in the RT & WL or WL groups (Table 1). During the 6-month intervention, four subjects (three RT & WL and one WL) decreased their oral hypoglycemic medication dos1731
Table 2Absolute changes in fasting glucose, insulin, lipids, and HbA1c from baseline for the RT & WL and WL groups, and the net difference between groups 3-month change from baseline RT & WL WL Net difference (95% CI) 6-month change from baseline RT & WL WL Net difference (95% CI)
Fasting plasma glucose (mmol/l) 0.5 2.3 0.09 2.5 0.6 (2.4 to 1.3) 1.4 2.7 0.6 2.4 0.8 (2.8 to 1.2) Fasting serum insulin (pmol/l) 7.1 43.3 16.4 60.3 9.3 (48.8 to 30.2) 10.5 46.3 4.7 27.2 15.2 (14.7 to 45.1) Insulin sensitivity (HOMA) (%) 1.3 4.6 0.3 6.1 1.0 (5.2 to 3.1) 0.03 5.2 0.8 6.5 0.8 (5.2 to 3.7) HbA1c (%) 0.6 0.7* 0.07 0.8 0.5 (1.1 to 0.01) 1.2 1.0* 0.4 0.8 0.8 (1.5 to 0.1) Serum lipids (mmol/l) Total cholesterol 0.03 0.6 0.2 0.9 0.2 (0.4 to 0.7) 0.09 0.8 0.5 0.8 0.4 (0.3 to 1.1) HDL cholesterol 0.02 0.1 0.07 0.2 0.05 (0.1 to 0.05) 0.06 0.1 0.07 0.2 0.01 (0.1 to 0.1) LDL cholesterol 0.03 0.4 0.2 0.9 0.2 (0.3 to 0.7) 0.06 0.7 0.5 0.9 0.4 (0.2 to 1.0) Triglycerides 0.2 0.7 0.05 0.9 0.2 (0.8 to 0.4) 0.2 0.7 0.08 0.6 0.1 (0.7 to 0.4)
Data are means SD or means (95% CI). Net difference refers to the within-group change from baseline in the RT & WL group minus the within-group change from baseline in the WL group. *P 0.01 within-group difference from baseline; P 0.05 between-group difference from baseline.
age and two subjects from each groups had their medication increased. Adherence to the interventions One-hundred percent adherence to the exercise sessions was set at 72 training sessions (three times per week for 24 weeks). Adherence to the exercise sessions among the 29 subjects averaged 88% (95% CI 81.794.1) for the RT & WL group and 85% (95% CI 77.9 92.4) for the WL group. Other than transient musculoskeletal soreness, no major complications or injuries were reported from either the RT & WL group or the WL group. Changes in metabolic variables HbA1c. The net and percent change in HbA1c from baseline for both groups are shown in Table 2 and Fig. 1. The RT & WL program was associated with a significant reduction in HbA 1c at both 3 months (0.6 0.7%, P 0.01) and 6 months (1.2 0.9%, P 0.01). No detectable changes were observed in HbA1c for the WL group. There was a signicant group-by-time interaction (P 0.05), with the magnitude of the decrease in HbA1c being greater in the RT & WL group than in the WL group. The overall net difference between groups in mean HbA1c from baseline was 0.5% (P 0.05) at 3 months and 0.8% (P 0.05) at 6 months. The results remained unchanged after adjustment for age, sex, duration of diabetes, use of oral hypoglycemic medication, medication change, baseline HbA1c levels, and change in waist circumference.
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Fasting insulin and glucose. Fasting plasma insulin levels remained unchanged throughout the 6-month intervention for both the RT & WL and WL groups (Table 2). For fasting plasma glucose, no changes were detected in either group after 3 months, but a 1.4-mmol/l decrease (P 0.06) was observed in the RT & WL group after 6 months (Table 2). However, there were no differences between the groups for either serum insulin or plasma glucose at any time point. Furthermore, insulin sensitivity (HOMA) remained unchanged in both groups. Changes in anthropometric and body composition In both the RT & WL and WL groups, there was a signicant reduction in body
weight and waist circumference after 3 and 6 months (Table 3). Fat mass also decreased in both groups after 6 months. However, there were no between-group differences in the net change from baseline for any of these variables at any time. LBM increased in the RT & WL group after 6 months training (0.5 1.2 kg, P 0.09), but decreased in the WL group (0.4 1.0 kg), which led to a signicant group-by-time interaction (P 0.05). The overall net percentage change from baseline for LBM in the RT & WL group relative to the WL group was 1.9% (95% CI 0.16 3.55). Changes in muscle strength As expected, resistance training and weight loss resulted in signicant in-
Figure 1Relative changes (percent) in HbA1c from baseline in the RT & WL and WL groups after 3 and 6 months. *P 0.01 within-group difference from baseline; P 0.05 between-group difference for the change from baseline. Values are means SE.
Table 3Absolute changes in anthropometry, body composition, muscle strength, blood pressure, energy expenditure, and energy intake from baseline for the RT & WL and WL groups, and the net difference between groups 3-month change from baseline RT & WL Anthropometry Body mass (kg) 1.8 2.0* Waist circumference (cm) 3.8 3.5* Body Composition Fat mass (kg) LBM (kg) Muscle strength Upper body (% change) 30.5 18.8* Lower body (% change) 8.0 17.1 Resting blood pressure (mmHg) Systolic 4.9 13.9 Diastolic 3.6 7.4 Energy expenditure (kcal/ 38 209 day) Total energy intake (kcal/day) 275 343 WL 2.0 1.5* 3.1 3.2* 7.6 15.7 2.1 18.4 3.8 13.6 0.9 6.8 80 207 241 311 Net difference (95% CI) 0.2 (1.2 to 1.6) 0.7 (3.3 to 2.0) 22.9 (7.638.2) 5.9 (8.9 to 20.6) 1.1 (11.7 to 9.4) 2.7 (8.1 to 2.8) 42 (117 to 202) RT & WL 2.5 2.9* 6.9 5.7* 2.4 2.8* 0.5 1.2 43.2 34.2* 33.0 21.7* 6-month change from baseline WL 3.1 2.1* 6.7 6.1* 2.1 2.5* 0.4 1.0 1.5 17.7 5.0 16.9 Net difference (95% CI) 0.6 (1.3 to 2.6) 0.2 (4.8 to 4.2) 0.3 (2.4 to 1.8) 0.9 (0.051.8) 41.7 (14.469.0) 28.0 (9.146.9)
6.7 10.0 2.5 15.8 4.2 (14.1 to 5.7) 4.4 6.9 0.9 10.1 3.5 (10.0 to 3.0) 97 204 55 253 42 (216 to 131)
Data are means SD or means (95% CI). Net difference refers to the within-group change from baseline in the RT & WL group minus the within-group change from baseline in the WL group. *P 0.01, P 0.05 within-group differences from baseline; P 0.01, P 0.05 between-group difference from baseline.
creases in upper and lower body muscle strength throughout the intervention (Table 3). There were no changes in muscle strength in the WL group. The overall net percentage change from baseline in upper body strength in the RT & WL group was 22.9% (95% CI 7.6 38.2, P 0.01) at 3 months and 41.7% (95% CI 14.4 69.0, P 0.01) at 6 months. For lower body strength, the net percentage change from baseline in the RT & WL group was 5.8% (95% CI 8.9 to 20.6, P 0.6) at 3 months and 28.0% (95% CI 9.1 46.9, P 0.01) at 6 months. Changes in blood pressure and serum lipids Resting blood pressure did not change from baseline in either group after 3 months (Table 3). After 6 months, a signicant reduction was observed in both systolic (6.7 10.0 mmHg, P 0.05) and diastolic (4.4 6.9, P 0.05) blood pressure in the RT & WL group. However, no between-group differences were observed for the net change in either systolic or diastolic blood pressure at any time. Serum lipids and lipoproteins were unchanged from baseline in both groups (Table 2). Changes in energy intake and habitual physical activity Analysis of the dietary records indicated that the mean total energy intake at 3 and
6 months was decreased from baseline in both the RT & WL and WL groups (Table 3). However, no differences were observed between the groups at any time. Furthermore, habitual physical activity (estimated energy expenditure, kilocalories per day) did not change from baseline in either group (Table 3). CONCLUSIONS This study has demonstrated that a supervised progressive high-intensity resistance training program performed 3 days/week for 6 months was safe and well tolerated by older patients with type 2 diabetes and was effective in improving glycemic control and muscle strength. The combination of resistance training and moderate weight loss was associated with a threefold greater decrease in HbA1c levels after 6 months compared with moderate weight loss without resistance exercise, and this was not mediated by concomitant reductions in body weight, waist circumference, and fat mass. The addition of resistance training also contributed to the maintenance of LBM despite moderate weight loss. Traditionally, aerobic activities have been recommended for people with type 2 diabetes because of the known benets on insulin sensitivity and glucose tolerance (7). However, for many older patients with type 2 diabetes, the presence of diabetic complications or coexisting
conditions, such as obesity, degenerative arthritis, or cardiovascular disease, may preclude participation in aerobic activities that involve prolonged periods of weight bearing, such as walking. In the present study, we found that a highintensity (75 85% of maximum strength) progressive resistance training program involving nine upper and lower body exercises (three sets of 8 10 repetitions) performed 3 days/week led to a signicant reduction in HbA1c after 3 months, which was decreased further after 6 months of training. Data from the U.K. Prospective Diabetes Study show that for every percentage point reduction in HbA1c, there is a 35% reduction in microvascular complications (24). Furthermore, recent data from the EPIC (European Prospective Investigation of Cancer and Nutrition)Norfolk prospective population study show that HbA1c concentration explains most of the excess mortality risk of diabetes, with an increase of one percentage point in HbA1c associated with a 28% increase in risk of death, independent of other well-established cardiovascular risk factors (25). In light of these ndings, it seems plausible to suggest that the mean 1.2% reduction in HbA1c after resistance training is likely to offer a prognostic advantage in older patients with type 2 diabetes. In recognition of the potential to improve muscular strength, endurance, and
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muscle mass, recent guidelines have supported the inclusion of resistance exercise as part of a well-rounded program for the lifestyle management of patients with type 2 diabetes (7,8). However, of the few studies that have assessed the impact of resistance training on glycemic control in this population (26 30), none have investigated the long-term effects of highintensity progressive resistance training combined with moderate weight loss in older adults with type 2 diabetes. Recent studies in middle-aged subjects with type 2 diabetes have reported improved insulin sensitivity using the hyperinsulinemic-euglycemic clamp (29) and improved glucose tolerance (28) after shortterm moderate-intensity resistance training, although most (28,29), but not all (30), have failed to detect an improvement in HbA1c. However, in all of these studies, the resistance training period was restricted to 8 weeks and, in contrast to the high-intensity (75 85% of maximum strength) resistance training program used in the present study, all used moderate intensity (40 50% of maximum strength) training protocols, including circuit weight training, which has both aerobic and resistance exercise components. The mechanisms for the improvement in glycemic control observed after resistance training in the present study are unclear. It is unlikely that differences in the magnitude of the changes in body weight and total fat mass accounted for the improved glycemic control, because both groups experienced similar changes throughout the study duration. Since improved insulin action has been positively associated with an exercise-induced increase in LBM in healthy young women (31), older men (17), and postmenopausal women (18) after resistance training, it is possible that the small increase in LBM observed in the resistance-trained individuals may be an important mediator of the improved glycemic control seen in the resistance-trained subjects. It has been suggested that the improved insulin sensitivity after resistance training occurs via different mechanisms from endurance training, with resistance training probably inducing a mass effect without altering the intrinsic capacity of the muscle to respond to insulin (31). However, it has also been proposed that improved insulin sensitivity after resistance training may be mediated by concomitant decreases in
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visceral and abdominal subcutaneous adipose tissue or abdominal obesity (32). In the present study, although abdominal fat mass was not directly assessed, waist circumference, which is a very robust predictor of abdominal visceral fat (33), was decreased to a similar extent in both the RT & WL and WL groups, implying that mechanisms other than abdominal obesity changes may have been involved in the more pronounced effect on HbA1c observed after resistance training. Because improved glucose disposal and metabolism may last for several hours, or perhaps days, after the cessation of acute exercise (34), it is uncertain whether the improved insulin sensitivity observed after exercise training in patients with type 2 diabetes is due to the cumulative effects of the individual acute exercise bouts or a speci c traininginduced adaptation (35). To avoid the possible residual effects of the last exercise bout on fasting glucose and insulin levels, all blood samples were assessed at least 48 h after the last exercise session. This interval may explain the absence of signicant differences between the RT & WL and WL groups with respect to both of these variables as well as insulin sensitivity estimated using the HOMA model. Other explanations may relate to the sample size being inadequate to detect a signicant fall in fasting glucose and insulin levels or the possibility that the major effect of the resistance training program was on postprandial glucose and postprandial insulin sensitivity, which are dependent on muscle insulin sensitivity. Nevertheless, regardless of whether the changes detected in HbA1c reect the summation of acute training or a chronic effect of training, our ndings provide strong support for the notion that resistance training performed on a regular basis has signicant therapeutic value and should be incorporated into initiatives designed to manage glycemic control in older patients with type 2 diabetes. In agreement with previous studies in middle-aged patients with type 2 diabetes (28,30) and middle-aged men at high risk for coronary heart disease (36,37), in this study, resistance training did not induce changes in the lipid prole. Common to all these studies, resistance training has either not altered body weight or led to relatively small weight loss during the intervention period. Since it appears that there is a positive association between ex-
ercise-induced changes in lipid proles and weight loss (38), our ndings, along with previous studies (28,30,36,37), suggest that a greater change in body weight and fat mass may be necessary to have a signicant effect on the lipid prole after resistance training. Similarly, although there was a trend for blood pressure to be reduced from baseline levels in the resistance-trained subjects, no differences were observed between the groups at either 3 or 6 months in the present study. This nding is consistent with other studies in patients with type 2 diabetes (3,30) and in men with an increased risk of coronary heart disease (37) after resistance training and may be inuenced by the initial baseline levels of the subjects and the magnitude of change in body weight and fat mass (37,39 41). Nonetheless, our ndings support earlier investigations in both normotensive and hypertensive subjects suggesting that long-term resistance training does not stimulate elevations in blood pressure, thereby supporting the appropriateness of this form of exercise for individuals with an elevated risk of hypertension. Maintenance of both upper and lower body muscle strength is important for older people to accomplish many of the tasks of daily living requiring static or dynamic efforts as well as for the prevention of falls (42). Previous studies in middleaged and older patients with type 2 diabetes that have used moderate training intensities have also observed muscular strength changes (28 30), but our ndings suggest that high-intensity resistance training may be more effective, since the magnitude of the improved muscular strength was considerably higher in our program than that previously reported. In addition to improved muscle strength, our ndings concur with previous studies that have demonstrated that combining resistance training with moderate energy restriction preserves LBM during dietinduced weight loss while contributing to loss in fat mass (43,44). Collectively, these results provide evidence to support the inclusion of high-intensity resistance training within lifestyle management strategies designed to reduce fat mass in older patients with type 2 diabetes. Furthermore, the high compliance and adherence to the high-intensity resistance training program observed in the present study indicates that this type of exercise training was well tolerated, feasible, and
safe for older patients with type 2 diabetes. Nevertheless, further long-term studies are needed to examine whether the benets can be maintained or even enhanced beyond the 6-month intensive training period and to determine whether similar programs conducted outside the intensive laboratory-based setting can improve glycemic control. Additional work is also required to assess the appropriateness of such programs for patients with type 2 diabetes who also have ischemic heart disease or the presence of advanced diabetes complications such as neuropathy and retinopathy. In conclusion, the results of this study demonstrate that a 6-month supervised high-intensity resistance training program was safe and well tolerated by older patients with type 2 diabetes. When combined with moderate weight loss, resistance training was more effective for improving HbA1c than moderate weight loss without resistance training, and this observation could not be explained by differences in body weight, waist circumference, and fat mass changes during the intervention. Furthermore, the addition of resistance training contributed to the preservation of LBM during moderate weight loss. These ndings provide strong support for the recommendation of this form of exercise in the therapeutic management of glycemic control of older patients with type 2 diabetes.
Acknowledgments D.W.D. and R.M.D. are supported by National Health and Medical Research Council Post-Doctoral Research Fellowships. This study was nancially supported by a grant from the Victorian Health Promotion Foundation (VicHealth). Funds for the purchase of exercise equipment were kindly provided by the Rotary Club of Kew, Victoria, Australia, and by Soroptimist International, Brighton Division. We wish to thank Elena Lekhtman and Lucy Robinson for their kind assistance in the clinical management of our volunteers. We are also grateful for the dietary assistance of Kathy McConell and Helen Bauzon. Many thanks to Dr. Ronald Sigal for his review of this manuscript. Most importantly, the authors are indebted to the volunteers whose cooperation and dedication made this study possible.
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References 1. Kaplan RM, Hartwell SL, Wilson DK, Wallace JP: Effects of diet and exercise interventions on control and quality of life
13.
in non-insulin-dependent diabetes mellitus. J Gen Intern Med 2:220 228, 1987 Wing RR, Epstein LH, Paternostro-Bayles M, Kriska A, Nowalk MP, Gooding W: Exercise in a behavioural weight control programme for obese patients with type 2 (non-insulin-dependent) diabetes. Diabetologia 31:902909, 1988 Dunstan DW, Mori TA, Puddey IB, Beilin LJ, Burke V, Morton AR, Stanton KG: The independent and combined effects of aerobic exercise and dietary sh intake on serum lipids and glycemic control in NIDDM: a randomized controlled study. Diabetes Care 20:913921, 1997 Agurs-Collins TD, Humanyika SK, Ten Have TR, Adams-Campbell LL: A randomized controlled trial of weight reduction and exercise for diabetes management in older African-American subjects. Diabetes Care 20:15031511, 1997 Ligtenberg PC, Hoekstra JBL, Bol E, Zonderland ML, Erkelens DW: Effects of physical training on metabolic control in elderly type 2 diabetes mellitus patients. Clin Sci 93:127135, 1997 Tessier D, Menard J, Fulop T, Ardilouze JL, Roy MA, Dubuc N, Dubois MF, Gauthier P: Effects of aerobic physical exercise in the elderly with type 2 diabetes mellitus. Arch Gerontol Geriatr 31:121132, 2000 American Diabetes Association: Diabetes mellitus and exercise (Position Statement). Diabetes Care 23 (Suppl. 1):S50 S54, 2000 Albright A, Franz M, Hornsby G, Kriska A, Marrero D, Ullrich I, Verity LS: American College of Sports Medicine position stand: exercise and type 2 diabetes. Med Sci Sports Exerc 32:13451360, 2000 Dunstan DW, Zimmet PZ, Welborn TA, De Courten MP, Cameron AJ, Sicree RA, Dwyer T, Colagiuri S, Jolley D, Knuiman M, Atkins R, Shaw JE: The rising prevalence of diabetes and impaired glucose tolerance: the Australian Diabetes, Obesity and Lifestyle Study. Diabetes Care 25: 829 834, 2002 Evans WJ: Effects of exercise on body composition and functional capacity of the elderly. J Gerontol A Biol Sci Med Sci 50A:147150, 1995 Frontera WR, Meredith CN, OReilly KP, Knuttgen HG, Evans WJ: Strength conditioning in older men: skeletal muscle hypertrophy and improved function. J Appl Physiol 64:1038 1044, 1988 Brown AB, McCartney N, Sale DG: Positive adaptations to weightlifting training in the elderly. J Appl Physiol 69:1725 1733, 1990 Pyka G, Lindenberger E, Charette S, Marcus R: Muscle strength and ber adaptations to a year-long resistance training program in elderly men and women. J
Gerontol 49:M22M27, 1994 14. Fielding RA: The role of progressive resistance training and nutrition in the preservation of lean body mass in the elderly. J Am Coll Nutr 14:587594, 1995 15. Campbell WW, Crim MC, Young VR, Evans WJ: Increased energy requirements and changes in body composition with resistance training in older adults. Am J Clin Nutr 60:167175, 1994 16. Treuth MS, Ryan AS, Pratley RE, Rubin MA, Miller JP, Nicklae BJ, Sorkin J, Harman SM, Goldberg AP, Hurley BF: Effects of strength training on total and regional body composition in older men. J Appl Physiol 77:614 620, 1994 17. Miller JP, Pratley RE, Goldberg AP, Gordon P, Rubin M, Treuth MS, Ryan AS, Hurley BF: Strength training increases insulin action in healthy 50- to 65-yr-old men. J Appl Physiol 77:11221127, 1994 18. Ryan AS, Pratley RE, Goldberg AP, Elahi D: Resistive training increases insulin action in postmenopausal women. J Gerontol 51A:M199 M205, 1996 19. American College of Sports Medicine: ACSMs Guidelines for Exercise Testing and Prescription. Philadelphia, Lippincott Williams & Wilkins, 2000 20. Sallis JF, Haskell WL, Wood PD, Fortmann SP, Rogers T, Blair SN, Paffenbarger RS Jr: Physical activity assessment methodology in the Five-City project. Am J Epidemiol 121:91106, 1985 21. Blair SN: How to assess exercise habits and physical tness. In Behavioral Health. Miller NE, Matarazzo JD, Weiss SM, Herd JA, Eds. New York, John Wiley & Sons, 1984, p. 424 447 22. Friedewald WT, Levy RI, Fredrickson DS: Estimation of the concentration of lowdensity lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 18:499 502, 1972 23. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC: Homeostasis model assessment: insulin resistance and B-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28:412 419, 1985 24. UK Prospective Diabetes Study Group: Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risks of complications in patients with type 2 diabetes (UKPDS 33). Lancet 352:837 853, 1998 25. Khaw K, Wareham N, Luben R, Bingham S, Oakes S, Welch A, Day N: Glycated haemoglobin, diabetes and mortality in men in Norfolk cohort of European Prospective Investigation of Cancer and Nutrition (EPIC-Norfolk). BMJ 322:1 6, 2001 26. Eriksson J, Taimela S, Eriksson K, Parviainen S, Peltonen J, Kujala U: Resistance
1735
27.
28.
29.
30.
31.
32.
33.
training in the treatment of non-insulindependent diabetes mellitus. Int J Sports Med 18:242246, 1997 Honkola A, Forsen T, Eriksson J: Resistance training improves the metabolic prole in individuals with type 2 diabetes. Acta Diabetol 34:245248, 1997 Dunstan DW, Puddey IB, Beilin LJ, Burke V, Morton AR, Stanton KG: Effects of a short-term circuit weight training program on glycaemic control in NIDDM. Diabetes Res Clin Pract 40:53 61, 1998 Ishii T, Yamakita T, Sato T, Tanaka S, Fujii S: Resistance training improves insulin sensitivity in NIDDM subjects without altering maximal oxygen uptake. Diabetes Care 21:13531355, 1998 Maiorana A, ODriscoll G, Goodman C, Taylor R, Green D: Combined aerobic and resistance exercise improves glycemic control and tness in type 2 diabetes. Diabetes Res Clin Pract 56:115123, 2002 Poehlman ET, Dvorak RV, de Nino WF, Brochu M, Ades PA: Effects of resistance training and endurance training on insulin sensitivity in nonobese, young women: a randomized controlled trial. J Clin Endocrinol Metab 85:24632468, 2000 Rice B, Janssen I, Hudson R, Ross R: Effects of aerobic or resistance exercise and/or diet on glucose tolerance and plasma insulin levels in obese men. Diabetes Care 22:684 691, 1999 Pouliot MC, Despres JP, Lemieux S, Moorjani S, Bouchard C, Tremblay A,
34.
35.
36.
37.
38.
Nadeau A, Lupien PJ: Waist circumference and abdominal sagittal diameter: best simple anthropometric indexes of abdominal visceral adipose tissue accumulation and related cardiovascular risk in men and women. Am J Cardiol 73:460 468, 1994 Mikines KJ, Sonne B, Farrell PA, Tronier B, Galbo H: Effect of physical exercise on sensitivity and responsiveness to insulin in humans. Am J Physiol 254:E248 E259, 1988 Schneider SH, Amorosa LF, Khachadurian AK, Ruderman NB: Studies on the mechanism of improved glucose control during regular exercise in type 2 (noninsulin-dependent) diabetes. Diabetologia 26:355360, 1984 Kokkinos PF, Hurley BF, Smutok MA, Farmer C, Reece C, Shulman R, Charabogos C, Patterson J, Will S, Devane-Bell J, Goldberg AP: Strength training does not improve lipoprotein-lipid proles in men at risk for CHD. Med Sci Sports Exerc 23: 1134 1139, 1991 Smutok MA, Reece C, Kokkinos PF, Farmer C, Dawson P, Shulman R, DeVane-Bell J, Patterson J, Charabogos C, Goldberg AP, Hurley BF: Aerobic versus strength training for risk factor intervention in middle-aged men at high risk for coronary heart disease. Metabolism 42:177184, 1993 Leon AS, Sanchez OA: Response of blood lipids to exercise training alone or com-
39.
40.
41.
42.
43.
44.
bined with dietary intervention. Med Sci Sports Exerc 33:S502S520, 2001 Fagard RH: Exercise characteristics and the blood pressure response to dynamic physical training. Med Sci Sports Exerc 33: S484 S492, 2001 Harris KA, Holly RG: Physiological response to circuit weight training in borderline hypertensive subjects. Med Sci Sports Exerc 19:246 252, 1987 Gilders RM, Malicky ES, Falke JE, Staron RS, Dudley GA: The effect of resistance training on blood pressure in normotensive women. Clin Physiol 11:307314, 1991 Pollock ML, Franklin BA, Balady GJ, Chaitman BL, Fleg JL, Fletcher B, Limacher M, Pina IL, Stein RA, Williams M, Bazzarre T: Resistance exercise in individuals with and without cardiovascular disease: an advisory from the Committee on Exercise, Rehabilitation, and Prevention, Council on Clinical Cardiology, American Heart Association. Circulation 101:828 833, 2000 Ballor DL, Katch VL, Becque MD, Marks CR: Resistance weight training during caloric restriction enhances lean body weight maintenance. Am J Clin Nutr 47: 19 25, 1988 Ross R, Pedwell H, Rissanen J: Response of total and regional lean tissue and skeletal muscle to a program of energy restriction and resistance exercise. Int J Obes 19: 781787, 1995
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