INTRODUCTION
The global proportion of older adults is increasing, leading to a rise in those requiring long-term care, which poses significant social challenges, such as higher medical costs and a shortage of caregiving personnel. In Japan and other developed countries, the number of older adults needing long-term care due to cognitive and physical decline is increasing.1,2) Therefore, early assessment and intervention in nutrition and physical function are essential to prevent further decline in physical health among older adults.3,4)
Sarcopenia, defined as the age-related loss of skeletal muscle mass, strength, and physical function, is associated with adverse outcomes, such as increased falls, functional decline, frailty, hospital readmissions, and mortality in older adults. This makes early detection and intervention crucial.5-9) The 2019 Asian Working Group for Sarcopenia (AWGS) guidelines are considered appropriate diagnostic criteria for Asians. These guidelines recommend measuring grip strength, the five-chair rise test, the Short Physical Performance Battery, or walking speed, along with assessing skeletal muscle mass using bioelectrical impedance analysis (BIA) or dual-energy X-ray absorptiometry (DXA) for diagnosis.5)
DXA provides a fairly accurate estimate of body composition and has been found to correlate highly with gold standards, magnetic resonance imaging (MRI), and computed tomography (CT).10,11) However, because the DXA method uses a small amount of X-rays, it is only available in a limited number of facilities in clinical settings; therefore, the BIA method is used instead.12,13) However, the instruments that measure skeletal muscle mass are expensive,5) making it impossible to assess sarcopenia in nursing homes and in older adults at home, where such equipment is unavailable.
Indeed, the possibility of diagnosing sarcopenia using the calf circumference (CC) in institutional and home settings without special equipment has been reported.14-17) Sarcopenia diagnosed using lower-extremity circumference has also been reported to be associated with reduced activities of daily living (ADL).18) However, CC may be affected by obesity, which may compromise its clinical relevance in the diagnosis of sarcopenia.19) Previous studies have reported that calf muscle circumference (CMC), CC minus subcutaneous fat, correlates better with skeletal muscle mass and is less affected by body fat than the previously existing method of CC.20) Subcutaneous fat measurement using calipers is a commonly used, non-invasive, inexpensive, and simple measurement method. Thus, CMC may be an important measure to diagnose sarcopenia instead of skeletal muscle mass. However, previous studies have not verified the concordance between sarcopenia diagnosis using alternative methods of skeletal muscle mass measurement and that using BIA. Therefore, this study aimed to clarify the association between CMC and sarcopenia and to determine the reliability of CMC in diagnosing sarcopenia.
MATERIALS AND METHODS
Study Design
This single-center, cross-sectional study was conducted between September 2023 and March 2024. The Ethics Review Board of International University of Health and Welfare approved the study protocol (Approval No. 21-Io-22-2 and 17-Io-189-7), and all participants (or their family members) provided signed informed consent. This study was conducted in accordance with the principles of the Declaration of Helsinki.
Study Setting and Participants
The study population comprised 159 individuals who agreed to participate in the study, were eligible to have their body composition measured, and were in need of support or care at day-care rehabilitation facilities under the Japanese long-term care insurance system.21) Fig. 1 shows a flowchart of the study participants; 63 older adults were included in the analysis. The exclusion criteria were as follows: age <65 years; age >100 years; requirement of assistance in daily living (Barthel Index <85); refusal to answer questions; requirement of assistance in walking; internal edema (extracellular water to total body water ratio <0.400)22); and missing data.
Data Collection and Measurement
Calf circumference/calf muscle circumference
The study collaborator (a physical therapist) measured the CC and CMC of patients at a day-care facility. CC was measured in millimeters using a measuring tape. CC was measured once on each side per participant, and the maximum value was taken as the representative value. A strong correlation exists between ultrasonography and skin measurements of calves made using calipers, and it has been reported that skin thickness measurements of calves made using calipers are reliable.23) A standard method of measuring lower leg subcutaneous fat was used with reference to previous studies.24) Measurements were taken at the site of maximal distention, with the knee flexed in a sitting position. Calf skinfold thickness was measured once on each side by pinching the skin ventral to the maximal distention of the calf using a subcutaneous fat meter (Abbott Japan Co. Ltd., Tokyo, Japan). Based on these measurements, CMC was calculated by subtracting the calf subcutaneous fat thickness from the total CC. The subcutaneous fat thickness was measured using a caliper. The CMC was determined as the maximum value obtained from measurements taken on both sides of the calf.20)
Calf muscle circumference (cm) = Calf circumference (cm) – Calf skinfold thickness (mm) × π/10 (calculated as π = 3.14).
Diagnosis of sarcopenia
AWGS 2019: Grip strength was measured twice in the sitting position (left and right) using a grip strength meter (model TKK5401 Grip-D; Takei Instruments, Niigata, Japan), and the maximum value was taken as the representative value. The walking speed was measured twice at a normal walking speed between the 3 m and 8 m (5 m) points of an 11-m walking path, and the average value was used as the representative value. The skeletal muscle mass index (SMI) was measured using a body composition analyzer (InBodyS10; InBody, Seoul, Korea) in the sitting position. For men, low muscle strength was defined as a grip strength of less than 28 kg, low physical function as a gait speed of less than 1.0 m/s, and low skeletal muscle mass as a SMI of less than 7.0 kg/m2. For women, low muscle strength was defined as a grip strength of less than 18 kg, low physical function as a walking speed of less than 1.0 m/s and low skeletal muscle mass as an SMI of less than 5.7 kg/m2. The diagnostic criteria for sarcopenia followed the AWGS 2019 guidelines, which are suitable for Asian populations. In this study, the patients were classified into sarcopenia (severe sarcopenia and sarcopenia) and non-sarcopenia groups.
According to AWGS 2019, sarcopenia is defined as follows: for males, SMI <7.0 kg/m2 or grip strength <28 kg, and/or walking speed <1.0 m/s; for females, SMI <5.7 kg/m2 or grip strength <18 kg, and/or walking speed <1.0 m/s.
CC/CMC sarcopenia: For men, a grip strength of <28 kg was defined as low muscle strength, and a walking speed of <1.0 m/s as low physical function. For women, a grip strength of <18 kg was defined as low muscle strength, and a walking speed of <1.0 m/s as low physical function. Low skeletal muscle mass for diagnosing sarcopenia was assessed using CMC and CC, with cutoff values established to identify reduced skeletal muscle mass.
- CMC sarcopenia: Defined as having a CMC of <31.1 cm for men and <28.7 cm for women, combined with a grip strength of <28 kg for men and <18 kg for women and/or a walking speed of <1.0 m/s.
- CC sarcopenia: Defined as having a CC of <34.0 cm for men and <32.3 cm for women, combined with a grip strength of <28 kg for men and <18 kg for women and/or a walking speed of <1.0 m/s.
Other Covariates
Age, sex, height, pre-existing diseases, and Barthel Index were obtained from the patients’ medical records. Nutritional status was assessed using the Mini Nutritional Assessment Scale-Short Form (MNA-SF), which is recommended for older adults.25) MNA-SF scores of 0–7, 8–11, and 12–14 indicated undernourishment, risk for undernourishment, and no undernourishment, respectively. The Geriatric Depression Scale-15 (GDS-15) was used to assess depression.26) The GDS-15 scores ranged from 0 to 5, 6 to 9, and 10 to 15 for no depression, depressive tendencies, and depression, respectively.
Statistical Analysis
Comparisons of attributes by sex were determined using the Shapiro–Wilk test to assess normality. Depending on the distribution, statistical analyses included the χ2 test, the independent t-test, and the Mann–Whitney U test. Factors related to CMC were subjected to multiple regression analysis with multicollinearity, with CMC and sarcopenia as the dependent and independent variables, respectively.
Subsequently, recipient operating characteristic curves were developed to determine the sensitivity and specificity of predicting low SMI (<7.0 kg/m2 and 5.7 kg/m2 for male and female participants, respectively) in CC and CMC. The area under the curve (AUC), sensitivity, and specificity were calculated using the Youden index to determine the optimal cutoff point; for AUC values, >0.9, 0.7–0.9, and <0.7 indicated high, moderate, and low accuracy, respectively.27) The concordance between low skeletal muscle mass and sarcopenia, as determined by the cutoffs for CMC, and low skeletal muscle mass and sarcopenia, as defined by the AWGS 2019 diagnostic criteria, was calculated using the kappa coefficient: kappa coefficient of 0–0.20, none; 0.21–0.39, minimal; 0.40–0.59, weak; 0.60–0.79, moderate; 0.80–0.90, strong; and >0.90, almost perfect.28) All statistical analyses were performed using IBM SPSS Statistics for Windows version 25 (IBM Corp., Armonk, NY, USA). Statistical significance was set at p<0.05. Power analysis was performed using G*Power version 3.1.2.1 (Heinrich-Heine-University Düsseldorf, Germany).
RESULTS
Overall, 159 older adults requiring long-term care were included in this cross-sectional study. Based on the inclusion and exclusion criteria, 63 individuals ultimately participated in this study (40 male and 23 female participants). Fig. 1 shows a flowchart of the study participants. Table 1 summarizes the results of the comparison of the basic attributes. The prevalence of sarcopenia was 30.4% and 40.0% in female and male participants, respectively. We identified significant sex differences in CMC, height, weight, cancer prevalence, grip strength, SMI, and body fat percentage. The factors associated with CMC are presented in Table 2. Multiple regression analysis showed that CMC was independently and significantly associated with sarcopenia (β=-0.36, p<0.001, R2=0.66). A post-hoc analysis was conducted to assess statistical power. In this analysis, a linear multiple regression analysis using the F-test yielded a power of 1.00, based on an alpha error of 0.05, sample size of 63, and R2=0.66, calculated from the regression equation. The results by sex are shown in Supplementary Table S1.
The cut-off points for CMC for identifying the risk of skeletal muscle mass loss are presented in Table 3. CMC was shown to have predictive power in both male and female participants. Based on calculations to identify the risk of low skeletal muscle mass, the optimal cutoff values for CC were 34.0 cm for males (AUC=0.88, sensitivity 81.8%, specificity 88.9%) and 32.3 cm for females (AUC=0.81, sensitivity 78.6%, specificity 88.9%) participants. The optimal cut-off values for CMC were 31.1 cm for males (AUC=0.89, sensitivity 86.4%, specificity 94.4%) and 28.7 cm for females (AUC=0.92, sensitivity 71.4%, specificity 100.0%) participants.
The reliability of sarcopenia diagnosis based on CMC is shown in Tables 4 and 5. The agreement between the low skeletal muscle mass using the BIA method and the low skeletal muscle mass discriminated from the cutoff values of CMC and CC calculated in this study was a kappa coefficient of 0.75 and 0.68, respectively. The agreement between the AWGS 2019 sarcopenia diagnosis and sarcopenia diagnosis using CMC and CC was a kappa coefficient of 0.80 and 0.70, respectively. The results by sex are shown in Supplementary Tables S2 and S3.
DISCUSSION
In this study, CMC was independently associated with sarcopenia. Additionally, CMC highly discriminated against low skeletal muscle mass, and the diagnosis of sarcopenia based on CMC was consistent with the AWGS sarcopenia diagnostic criteria. To the best of our knowledge, this is the first study to demonstrate the reliability of sarcopenia diagnosis based on CMC.
In this study, the predictive power of CMC for skeletal muscle mass loss was higher in both male and female participants, with CMC tending to have a higher predictive power, especially in female participants. A previous study reported that CC correlated with body fat, whereas CMC did not correlate with body fat percentage. Furthermore, CMC was more highly correlated with SMI than CC.20) Previous studies have also shown that older male participants have more skeletal muscle mass than female participants and that older female participants have more body fat than male participants.29) Other studies have reported significant sex differences in fat distribution, with female participants tending to accumulate significantly more peripheral subcutaneous adipose tissue (e.g., buttocks and thighs) and male participants tending to accumulate more central adipose tissue.30) This indicates that female participants tended to accumulate subcutaneous fat in their lower extremities, whereas male participants tended to accumulate visceral fat in their abdomen.31) The results of this study support those of previous research and confirm significant sex differences in body fat percentage. This suggests that CMC is highly discriminatory, especially in female participants, because it is less affected by body fat.
In this study, sarcopenia diagnosed using CC or CMC was highly consistent with the AWGS diagnostic criteria using the BIA method. Gonzalez-Correa et al.14) reported that CC was highly correlated with skeletal muscle mass. Because skeletal muscle mass is not adaptable to institutional settings without special equipment, several alternative methods have been reported to diagnose sarcopenia using CC, which correlates well with skeletal muscle mass.14-17) Champaiboon et al.17) reported that the discriminatory cutoff for low skeletal muscle mass in CC was <33 cm in females (sensitivity 80.1%, specificity 60.5%) and <34 cm in males (sensitivity 85.4%, specificity 70.2%). In other studies, low skeletal muscle mass for sarcopenia diagnosis reported that the optimal CC cutoff for prediction was <34 cm in males (sensitivity 88%, specificity, 91%) and <33 cm in females (sensitivity 76%, specificity 73%).5) Abe et al. also reported that sarcopenia based on CC was associated with ADL decline.18) The results of this study showed that CC had a cutoff value similar to that reported in a previous study, and the kappa coefficient for sarcopenia diagnosis in CC was 0.70, in accordance with the AWGS 2019 sarcopenia diagnostic criteria. The results of this study indicate that CC can be used as an alternative method for measuring skeletal muscle mass to detect sarcopenia. Interestingly, this study also found that CMC was more consistent with the AWGS sarcopenia diagnostic criteria than CC. The clinical relevance of CC may be compromised by obesity, sarcopenia-obesity, or a combination of sarcopenia and obesity.19) The kappa coefficient in this study showed that diagnosis using CMC was more consistent with low skeletal muscle mass than that using CC, indicating that diagnosis using CMC is a better indicator of sarcopenia than that using CC. These findings indicate that sarcopenia may be diagnosed using caliper measurements of CMC in community, institutional, and home settings, where skeletal muscle mass cannot be measured.
This study had some limitations. First, this was a single-center study with a small sample size. A multicenter study is preferable to generalize the results of this study. Second, this was a cross-sectional study. As the causal relationship between CMC and sarcopenia remains unknown, a longitudinal study is desirable. In the future, it would be desirable to examine consistency with the the Global Leadership Initiative on Malnutrition (GLIM) criteria,32) which is also the gold standard in nutritional science, and to longitudinally follow up with the individuals evaluated to examine the validity of the measurement method. Third, the reliability of measurements using the skinfold method has not been fully established. Future research should investigate the agreement between CMC measured by the skinfold method and those measured by CT. Finally, further studies using DXA, CT, and MRI are needed to assess the relevance of BIA, as it is not the gold standard for measuring appendicular skeletal muscle.
In conclusion, CMC was found to be independently associated with sarcopenia, and sarcopenia diagnosis based on CMC was consistent with AWGS 2019 sarcopenia diagnostic criteria. This finding suggests that CMC is a useful surrogate marker for skeletal muscle mass.
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