Decreased Muscle Strength and Quality in Older Adults With Type 2 Diabetes: The Health, Aging, and Body Composition Study

Seok Won Park; Bret H. Goodpaster; Elsa S. Strotmeyer; Nathalie de Rekeneire; Tamara B. Harris; Ann V. Schwartz; Frances A. Tylavsky; Anne B. Newman


Diabetes. 2006;55(6):1813-1818. 

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In our study, older adults with type 2 diabetes had a greater muscle mass in their arms and legs than those without diabetes. But despite this larger muscle mass, those with diabetes were either weaker (men) or not stronger (women) than those without diabetes. This finding was somewhat surprising because the quantity of muscle mass had been known as a primary determinant of muscle strength.[13,18,19,20] We have clearly demonstrated that muscle quality was consistently lower in older adults with type 2 diabetes, regardless of sex and muscle groups examined (arm or leg). This is a novel finding possibly explaining a pathophysiological mechanism for increased risk of functional limitations and disability in older adults with type 2 diabetes, because low muscle strength or poor muscular function is predictive of physical disability.[8,9,10,11,12] Our finding is consistent with the study in patients with type 1 diabetes.[21] We have also found that lower muscle quality in older adults with diabetes was largely attenuated by adjustment for BMI, indicating that obesity might have an important role in this association. We have previously reported that skeletal muscle attenuation coefficient determined by computerized tomography was lower with increasing BMI, and it was independently associated with muscle strength and quality.[22] Low muscle attenuation was also found in older adults with impaired glucose tolerance or type 2 diabetes.[23] Reduced muscle attenuation values have been associated with reduced oxidative enzyme activity[24] and lower maximal aerobic capacity.[25] It is possible that alterations of muscle composition with increased fat infiltration into the skeletal muscle as evidenced by low muscle attenuation in type 2 diabetes, which is also associated with combined obesity, may result in poor muscle quality. Further research will be needed to determine whether diabetes itself or the higher levels of body fat in the diabetes is a direct cause of poor muscle quality in a prospective study.

There had been no report on skeletal muscle strength or function in type 2 diabetes until Andersen et al.[26] reported muscle weakness at the ankle and knee in a case-control study. They showed a 7-17% lower muscle strength at the ankle and knee in patients with type 2 diabetes compared with control subjects. Although control subjects were matched for sex, age, weight, height, and physical activity, it was impossible to evaluate whether muscle weakness in subjects with type 2 diabetes was due to reduced muscle mass or poor muscle quality because muscle mass was not assessed in their study. In the present study, we measured arm and leg regional muscle mass separately by DEXA. The concurrent measures of muscle mass and strength allowed us to evaluate in vivo muscle quality, which was defined as muscle strength per unit muscle mass in kilograms. This definition has been consistently used to assess muscle function in human subjects.[13,27,28] The specific force of arm and specific torque of leg represent the maximal contractile capacity of each appendicular skeletal muscle group adjusted for the quantity of muscle mass. Therefore, these measures of muscle quality are a more reasonable indicator of contractile function of skeletal muscle than crude muscle strength, which is largely dependent on the quantity of muscle mass. This concept might be important, particularly for the comparison of skeletal muscle function between subjects with different body sizes like those with and without diabetes.

The discrepancy between men and women in terms of differences in absolute muscle strength can be explained by the magnitude of differences in muscle mass between those with and without diabetes. Older men with diabetes had only slightly (~4-5%) higher appendicular muscle mass than those without diabetes ( Table 2 ). This small difference in muscle mass may not be enough to overcome poor muscle quality of diabetes, resulting in lower muscle strength in men with diabetes. But women with diabetes had moderately (~12-14%) higher appendicular muscle mass than those without diabetes, which may be enough to compensate poor muscle quality and result in absolute muscle strength comparable with the nondiabetic women. However, despite having similar muscle strength, older women with diabetes showed poor physical function in our previous report using the same cohort,[7] suggesting that their strength might be insufficient to carry their heavy weight.

Another important finding of this study is a linear relationship showing that both longer duration of diabetes and poor glycemic control are associated with much poorer muscle quality (Figs. 1 and 2). These findings are consistent with our previous observation that poor glycemic control in diabetic individuals explained the association with subclinical functional limitation.[7] A metabolic consequence of uncontrolled hyperglycemia is catabolism, which depending on the severity, is accompanied by muscle protein breakdown and inadequate energy use, potentially resulting in poor muscle function. Diabetes with poor glycemic control is also associated with increased systemic inflammatory cytokines, such as tumor necrosis factor-α and interleukin-6, which have detrimental effects on muscle function.[29,30,31,32]

Neuropathic processes involving motor neurons might be another possible underlying mechanism for the poor muscle function in diabetes. In the mouse model, after 4 weeks of diabetes, the relative loss of torque via nerve stimulation (~43%) was greater than the force loss in the directly stimulated muscle (~24%), indicating a functional neural deficit.[33] Although it is unclear in humans, a greater and selective atrophy of type IIb fibers has been observed in diabetic animal muscles,[34,35,36] which may contribute to strength loss. In humans, the presence and severity of diabetic neuropathy has been shown to be associated with decreased muscle strength in both type 1 and type 2 diabetes.[26,37] Electrophysiological studies suggest that loss of muscle strength in diabetic patients is due to incomplete reinnervation after axonal loss.[38]

The present study is the first epidemiological study to assess skeletal muscle function in subjects with and without type 2 diabetes in apparently healthy, community-dwelling older adults. The population includes white and black older men and women with type 2 diabetes in various clinical stages. We found a significantly lower muscle quality in older adults with diabetes, although the difference is relatively small in magnitude. For the clinical implications, we have to consider that subjects with diabetes in this study were all well functioning without physical disability. The inclusion of asymptomatic subjects as diabetes group by fasting plasma glucose cut-point attenuated the difference in muscle quality (data not shown). In other words, older adults with diabetes seen in clinical setting might have even poorer muscle quality. It has been well established that lower muscle strength is an important contributor to disability.[10,11,12] However, the clinical significance of poor muscle function in diabetes for the development of disability can only be answered by a prospective study.

This study has several limitations. First, this is a cross-sectional study showing only an association between type 2 diabetes and poor muscle function. It does not necessarily mean that type 2 diabetes in older adults results in poor muscle strength and quality. It is also possible that lower muscle quality is a causative factor related to the development of type 2 diabetes in older adults. However, even lower muscle quality in diabetic subjects with longer duration and poor glycemic control may suggest that poor muscle quality is likely a consequence rather than a cause of diabetes in older adults (Figs. 1 and 2). Second, we have no data on diabetic neuropathy at baseline, which may have an important mediating role in muscle weakness. Despite these limitations, this study might have important public health implications because older adults with diabetes are at increased risk of developing physical disability and potential preventive strategies are available, including resistive-training exercise program to improve skeletal muscle function in subjects with diabetes.[39]

In conclusion, in community-dwelling older adults, type 2 diabetes is associated with lower skeletal muscle strength and quality. These characteristics may contribute to development of physical disability in older adults with diabetes. Prospective studies are needed to investigate whether type 2 diabetes in older adults is associated with longitudinal declines in muscle strength and to examine the relationship to the loss of muscle mass and muscle quality.


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