In our study, a low erector spinae muscle area was associated with mCHS-defined frailty in older patients with diabetes of both sexes in the univariate analysis and in women in the multivariate analysis. In addition, a high L/S was associated with KCL-defined frailty in males in the multivariate analysis.
Among the various abdominal muscle measurements that can be obtained by CT scans, the area of the erector spinae was the most associated with mCHS-defined frailty. To our knowledge, this is the first study to show an association between low trunk muscle mass and frailty in older adults with diabetes. As for the diagnostic components of mCHS-defined frailty, the area of the erector spinae muscle was associated with both hand grip strength and walking speed. These results suggest that the association between low trunk muscle mass and frailty may be attributable to low muscle strength as well as low physical performance.
Several reports have shown that in addition to the lower limb muscles, the trunk muscles are also involved in mobility in older adults. Masaki et al. reported that a reduction in maximal walking speed is associated with a reduction in erector spinae muscle mass in community-dwelling older adults [11]. Lim et al. reported that the erector spinae and gluteus maximus are engaged in maintaining balance during the early stance of walking in older adults [12]. Golubić et al. reported that the strength of the trunk extensor muscles, including the erector spinae muscle, is related to balance ability in healthy older women [13]. These findings indicate that a reduced erector spinae muscle area can predict activities of daily living (ADL) disabilities and even mortality in older adults. Yamashita et al. reported that the erector spinae muscle area evaluated by CT imaging was significantly associated with dependency in ADL at discharge in middle-aged and older patients who showed COVID-19 infection, although they did not evaluate the masses of other trunk muscles [14]. Low erector spinae muscle area has also been reported to be associated with increased mortality in patients with chronic obstructive pulmonary disease [15] and lung transplantation recipients [16].
Surprisingly, visceral fat area was not associated with frailty prevalence in our patients. Visceral fat deposition is known to induce insulin resistance, which is a risk factor for cardiovascular diseases and frailty. Indeed, a recent study in China reported that frail older inpatients had significantly higher waist circumference than non-frail patients [17]. Another study of Japanese community-dwelling older adults also showed that a high visceral fat area was a risk factor for pre-frailty [18]. This conflicting relationship between fat accumulation and frailty can be explained by the differences in the backgrounds of the participants in the previous studies, which included non-diabetic patients, and our study, which was limited to inpatients with poor glycemic control levels. Since other risk factors for frailty, such as glycemic control and cognitive dysfunction, may play a considerable role in these patients, the influence of visceral fat accumulation on the incidence of frailty may be blunted in comparison with that in patients without diabetes.
The L/S ratio was positively associated with KCL-defined frailty in men. We had expected a negative association since patients with nonalcoholic fatty liver disease, which presents with a low L/S, are susceptible to frailty and the disease is generally associated with insulin resistance [9] and atherosclerotic lesions [19]. However, the results were contrary to our expectations. This could also be attributed to the effects of poor glycemic control, diabetes treatment, and the age of our participants. Another possible explanation may be that the effect of undernutrition, which presents with a high L/S ratio, on frailty may have been greater than the effect of fat accumulation in the liver on frailty in this population. In this context, it is reasonable to assume that L/S is associated only with KCL-defined frailty, which includes questions concerning body weight loss and underweight, and not with mCHS-defined frailty. Although we could not determine why the association was found exclusively in males, a sub-analysis in our previous report investigating the association between energy intake and mortality in The Japanese Elderly Intervention Trial cohort showed that low energy intake was more strongly associated with mortality in males than females [20]. Although the precise mechanism underlying this association remains unclear, it may be based on the more deteriorated malnutrition-induced outcomes in men than in women. However, since the significant association persisted even after the addition of BMI and serum albumin level as covariates, some mechanisms other than undernutrition may be related to the association between low L/S values and frailty.
Most of the results of multiple regression analyses were within our expectations: the area of the erector spinae and L/S value were positively and negatively, respectively, associated with BMI and serum albumin level, indicating that both indices reflect the nutritional condition of the patients. L/S values were further associated with the TG level, and liver fat content in nonalcoholic fatty liver disease has been previously reported to be associated with higher serum TG levels. Notably, both the area of the erector spinae (positive) and L/S values (negative) were associated with MMSE scores only in women. The reason for these sex differences is unclear. Since males are known to be more susceptible to atherosclerosis [21], other factors such as cerebral microvessel diseases might attenuate the influence of these indices on cognitive function in men.
The strength of this study is that we analyzed a considerable number of images of trunk muscles and L/S in older patients with diabetes who underwent CT scans during hospitalization. Moreover, we evaluated four trunk muscles separately: the erector spinae, iliopsoas, rectus abdominis, and abdominal oblique muscles.
Nevertheless, our study also had some limitations that require consideration. First, data from hospitalized patients at a single institution in Japan who underwent CT scans for some reason were used in the study. Thus, some selection bias may have existed, and our study cohort may not represent the population of community-dwelling older patients with diabetes. Second, since this was a cross-sectional study, the causal relationship between the imaging indices and frailty was unclear. Further longitudinal studies should be planned to clarify the associations between these markers and the incidence of frailty in non-frail patients or between these markers and mortality in frail patients. Third, we evaluated only the areas of each trunk muscle and not their density. Recent studies have shown that the CT values of muscles, which indicate fat deposition in the muscle, are another indicator of poor prognosis [16, 22]. Sugai et al. reported that low CT values in the iliopsoas predicts major adverse cardiovascular and limb events after endovascular therapy [22]. Finally, we did not assess the level of insulin resistance in each patient, which could be associated with both the area of the erector spinae and L/S as well as the incidence of frailty. However, since our participants were patients with poorly controlled diabetes, even if the insulin or C-peptide levels were available, they might not have reflected the true levels of insulin resistance due to the so-called glucose toxicity.