Effective Exercise Modality to Reduce Insulin Resistance in Women With Type 2 Diabetes

Darcye J. Cuff, MSC; Graydon S. Meneilly, MD; Alan Martin, PHD; Andrew Ignaszewski, MD, FRCPC; Hugh D. Tildesley, MD; Jiri J. Frohlich, MD, FRCPC

Disclosures

Diabetes Care. 2003;26(11) 

In This Article

Conclusions

We tested the effect of adding resistance training to an aerobic training program on insulin sensitivity and changes in abdominal obesity and skeletal muscle characteristics in postmenopausal women with type 2 diabetes. The principal finding is that a combined aerobic plus resistance training program elicited significant improvements in insulin sensitivity compared with the control group. Both training regimes resulted in reductions in body weight and total abdominal obesity, specifically from the subcutaneous component of abdominal AT. Training reduced the low-density component of thigh muscle, with a concomitant increase in the normal-density component, with an incremental effect seen with aerobic plus resistance training. The change in insulin resistance was related to changes in abdominal subcutaneous and visceral adipose and muscle cross-sectional area and density.

The addition of resistance training to an aerobic program resulted in an improved glucose disposal, which was not evident in this study after aerobic training alone. This supports the initial hypothesis that the addition of resistance training would prove effective in improving insulin sensitivity. Resistance training alone has been seen to exert a beneficial effect on glucose disposal in young nonobese women,[20] men with impaired glucose tolerance,[8] and healthy postmenopausal women.[7] This work indicates that the outcome of a combined aerobic plus resistance training program may be more successful in improving insulin resistance than a program with aerobics alone.

Improvement in insulin sensitivity was seen in the Ae+RT group but was not evident in the Ae only group. Other work has demonstrated improved insulin sensitivity in response to aerobic only training programs in nonobese, obese, or impaired glucose tolerant subjects. Subjects with established diabetes may be more insulin resistant, perhaps requiring a longer timeframe to respond to an aerobic training stimulus. It appears that using a more effective exercise stimulus, i.e., one that includes resistance training, may bring about changes within the timeframe investigated.

Beneficial improvements in insulin sensitivity brought about by exercise training attenuate within 3-6 days after the last exercise session.[21,22,23] Our results may reflect the impact of the most recent exercise session, or a training adaptation or an interaction of both. In clinical application, this suggests the value of consistent exercise frequency to maintain the beneficial effects on carbohydrate metabolism.

No change was seen in this study in glycosylated hemoglobin levels. Recent reviews of the response of glycosylated hemoglobin levels to exercise training found a modest response (0.5-1.0%) or no response to training interventions.[24,25] Variable findings have been attributed to small sample sizes and the complex pathophysiology of type 2 diabetes, which could have contributed to the lack of findings in this study.

Our finding of improved insulin sensitivity in response to a combined aerobic plus resistance training program suggests that resistance training may be a valuable aspect of exercise programming. This may be particularly true in light of the lack of significant response to an aerobic training only program in this study population. These are the first data demonstrating the effectiveness of resistance training in older women with type 2 diabetes and the effectiveness of a combined training program.

In the combined exercise group, total abdominal AT was decreased, with the loss more apparent from the subcutaneous depot than from the visceral depot. These findings differ from reports in which exercise training without weight loss resulted in decreases in both abdominal AT areas in diabetic men[2] or decreased visceral but not subcutaneous abdominal depot in nonobese postmenopausal women.[26] In studies where exercise training is accompanied by substantial weight loss, decreases in both abdominal regions have been documented in obese women[27,28] and obese men.[18,29] The variable differences across studies may be attributable to small adiposity changes (in studies with no weight change), small sample sizes, and large variability in these depots seen in most studies. This study group was characterized by abdominal obesity (BMI of ~34 kg/m2 and waist circumference of ~112 cm) by selection criteria, but considerable heterogeneity in abdominal adipose patterning was apparent. Two studies with large sample sizes have shown changes in both visceral and subcutaneous abdominal AT after exercise training with small weight loss in obese postmenopausal women[30] or no weight loss in normal-weight premenopausal women.[31]

The method of expressing changes in adiposity may affect study conclusions. If the change is expressed relative to initial levels (i.e., as a percentage), it may lead to the conclusion that visceral adipose losses are greater than abdominal subcutaneous losses. But if evaluated as an absolute change value, losses from abdominal subcutaneous AT are equal to or greater than that from the visceral area.[18,27,28,31] Cross-sectional associations have demonstrated a stronger relationship of subcutaneous abdominal AT with insulin resistance.[32,33] Subcutaneous abdominal AT has been identified as the source of free fatty acids,[34] which are thought to be involved in the negative health impacts of increased abdominal obesity. These data, taken in conjunction with the data from our study indicating a greater loss of subcutaneous abdominal AT after exercise training, support the suggestion that visceral AT is not of singular importance[32,33,35] but that subcutaneous abdominal AT also plays a role.

Low-density muscle tissue is thought to contain greater amounts of inter- and intracellular lipid and has been linked to insulin resistance. It has been unclear how exercise training affects this aspect of muscle composition. An endurance training effect could include depletion of intramuscular lipid, and the addition of resistance training could stimulate muscle mass development and possibly lipid depletion.

Muscle cross-sectional area did not change after aerobic training but displayed a trend to increase after aerobic plus resistance training. This confirms other findings of no change with aerobic training, with muscle hypertrophy after resistance training.[18,20,26,29,36]

In both training groups, low-density muscle area decreased and normal-density muscle area increased. The increment in normal-density muscle was greater in the aerobic plus resistance training group. Others have reported similar changes in muscle composition after aerobic training with[27] or without[20] weight loss and after resistance training.[20,36] These findings indicate that exercise training reduces the proportion of low-density muscle and increases the proportion of normal-density muscle, changes that are thought to reflect changes in intermuscular lipid content. Results from magnetic resonance imaging studies have also demonstrated a reduction in intermuscular fat after either aerobic or resistance training, although these studies have involved larger weight losses.[28] Our results extend these findings and suggest that using both exercise modalities is additive in the effects on muscle composition change. Furthermore, muscle composition characteristics, linked to insulin resistance, can thus be ameliorated in postmenopausal women with type 2 diabetes.

Our results suggest that improvements in glucose disposal after exercise training are independently related to changes in subcutaneous abdominal obesity and to muscle cross-sectional area and muscle density in obese postmenopausal women with type 2 diabetes. Change in visceral adipose did not show a relationship with glucose disposal independent of subcutaneous abdominal AT. Few published reports are available that directly assess insulin sensitivity relative to changes in body composition after a training program. One study reported a significant association between glucose disposal and changes in visceral AT in obese men, although possible relationships to subcutaneous AT were not reported.[29]

The independent relationship of muscle characteristics to glucose disposal after exercise training is a new finding. One study was unable to relate muscle mass (assessed by magnetic resonance imaging) to insulin sensitivity after aerobic training.[29] The difference may by due to the added effectiveness of muscular strength training. The improvement in glucose disposal in young nonobese women seen after strength training disappeared when indexed for whole-body fat-free mass,[20] suggesting that the increase in lean body tissue (including skeletal muscle) was responsible for the improvement. An endurance-trained group in the same study retained insulin sensitivity improvements after accounting for fat-free mass. These authors were not able to demonstrate a relationship between increased attenuation value and glucose disposal in either the endurance- or resistance-trained groups. Muscle density or intramuscular lipid may play a more significant role in the older diabetic group of this study than in the healthy younger normal-weight group.

Enhanced glucose uptake was seen in postmenopausal women with type 2 diabetes after a combined aerobic plus resistance training program. This improvement was related to losses of AT area from abdominal subcutaneous depot and to increases in thigh muscle cross-sectional area and thigh muscle attenuation characteristics. We conclude that a combined endurance plus resistance training program is most effective in improving insulin sensitivity in these women and that the improvements are associated with changes in muscle characteristics brought about by strength training.

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