Abstract
Objective
This study examined the relationships among lower limb skeletal muscle characteristics, walking function, and daily physical activity in community-dwelling, independently living older women. This serves as a fundamental study for the prevention and early detection of sarcopenia, using ultrasonography-based muscle mass and quality assessment.
Patients and Methods
The participants were 53 community-dwelling women aged 66–89 years, who were independent in activities of daily living (ADL). Age, physical characteristics (height, weight, body fat percentage, skeletal muscle mass, and skeletal muscle index [SMI]), walking function, physical activity level, fall occurrence in the past month, and gastrocnemius muscle parameters (muscle thickness, fascial thickness, and muscle echo intensity) were assessed. Correlation analyses were conducted and intra-examiner reliability was confirmed using the intraclass correlation coefficient.
Results
The participants’ median age was 77.0 years, height was 150.3 cm, weight was 51.0 kg, body fat percentage was 30.6%, and SMI was 6.5 kg/m2. Overall, 11.3% of participants had an SMI below the sarcopenia threshold. The gastrocnemius muscle parameters showed the strongest correlations; muscle thickness had weak positive correlations with SMI, walking function, and physical activity, but negative correlations with age and total movement time. Fascial thickness correlated positively with weight and body fat percentage but negatively with walking function. Muscle echo intensity was positively correlated with age and negatively correlated with SMI, walking speed, step count, and housework time.
Conclusion
Although all the participants lived independently, 11.3% had an SMI below the sarcopenia threshold, highlighting the need for early prevention. Gastrocnemius muscle parameters were significantly associated with age, physical characteristics, walking function, and activity level. Reduced physical activity may contribute to muscle degeneration and impaired walking even in independent individuals. Combining muscle echo intensity and fascial thickness may enhance muscle quality assessment, aiding in the prevention and early detection of sarcopenia.
Keywords: sarcopenia, skeletal muscle index, geriatrics
Introduction
Japan has the longest life expectancy in the world, and the percentage of the total elderly population is 29.1%, which is the highest ever1). For women, the difference between mean life expectancy and mean healthy life expectancy is 12 years2). Thus, the length of time spent in poor health, during which daily activities are limited, is longer for women than for men. To shorten the time spent in poor health and enable an individual to live in a familiar environment in a manner that suits them, there is a need to extend healthy life expectancy.
Sarcopenia is one of the causes of shortened life expectancy. Sarcopenia is defined as a decrease in skeletal muscle mass resulting in decreased muscle strength and physical function. Numerous epidemiological studies have found it to be associated with increased mortality, physical disability, and risk of long-term care3). An investigation of sarcopenia prevalence by Kitamura et al.4) showed that its prevalence increased with age and, in those aged ≥80 years, it was higher in women than in men, at 48% and 32%, respectively. In addition, it has been reported that the decrease in skeletal muscle mass associated with sarcopenia begins in late middle age, and by 80 years of age, it progresses to approximately 40% of the skeletal muscle mass of that of persons in their 20s5). In women, the largest change in age-related skeletal muscle mass by site is a decrease in skeletal muscle mass in the lower limbs, where rapid progression of muscle atrophy is seen6). The Asian Working Group for Sarcopenia 2019 (AWGS 2019), published by the Asian Working Group for Sarcopenia, was used in Japan7). Skeletal muscle mass is emphasized in sarcopenia assessments and evaluated using bioelectrical impedance analysis (BIA) or dual-energy X-ray absorptiometry (DXA). DXA is expensive, exposes the body to radiation, and can only be performed at a limited number of sites. In contrast, BIA is inexpensive and provides excellent mobility. However, it cannot be used to visualize and evaluate skeletal muscle, and the water content in the body, in the form of edema, causes skeletal muscle mass to be overestimated7). Diagnostic ultrasound systems have attracted considerable attention in recent years. It is minimally invasive, inexpensive, and enables easy measurement. Measurements of muscle volume have been shown to correlate strongly with those obtained by magnetic resonance imaging (MRI). Moreover, diagnostic ultrasound evaluation enables the assessment by location not only of skeletal muscle thickness, a quantitative index, and muscle echo intensity, an index of muscle quality8).
Many previous studies that used quantitative and qualitative evaluations of skeletal muscles with diagnostic ultrasound systems examined the lower limb skeletal muscles as the target muscles. Some of these studies found that with aging, decreases in thickness and increases in echo intensity of the quadriceps femoris muscle, which is involved in lower limb extension and is susceptible to atrophy with aging, affect lower limb muscle strength and walking function8, 9). However, muscle atrophy in elderly individuals tends to occur in the antigravity muscles, not only in the quadriceps femoris but also in the triceps surae muscles, which are involved in lower limb flexion10). Decreased skeletal muscle mass in the lower limbs due to muscle atrophy leads to decreased walking function11). In addition to the quadriceps femoris muscle, which supports the lower limbs while standing and walking, the triceps surae muscles, which facilitate forward movement by pressing against the floor, play a role in decreasing walking speed and stride length, which are susceptible to the effects of aging12). Consequently, in evaluating lower-limb skeletal muscles using a diagnostic ultrasound system, attention should also be paid to the triceps surae muscles, as they are related to decreased walking function.
Atrophy, the mechanism for the quantitative and qualitative decrease in lower limb skeletal muscle and is caused by aging and decreased activity levels, leads to a decrease in muscle thickness. In addition, ectopic fat infiltration and fibrosis occur in the muscle fiber interstitium and fascia in the tissue near the atrophic muscle fibers, resulting in increased muscle echo intensity13). Previous studies using diagnostic ultrasound systems have reported that increased muscle echo intensity in lower limb skeletal muscles reflects intramuscular changes, including thickening of the endomysium and perimysium due to muscle atrophy, as well as fatty infiltration and fibrosis within the muscle fiber interstitium and the surrounding fascia. However, muscle echo intensity is a relative value, and can be influenced by differences in image illuminance resulting from differences in equipment or other factors, making consistency and comparison across studies difficult. Consequently, the thickness of the fascia, the connective tissue surrounding the muscle, has attracted attention as an index that enables the evaluation of muscle quality based on absolute values. Some international studies have investigated fascial thickness using diagnostic ultrasound systems. For instance, Choi et al.14) reported an association between fascial thickness and muscle stiffness in stroke patients with spasticity, whereas Schadmy et al.15) demonstrated the reliability of measuring deep fascial thickness and its association with restricted mobility.
Although these studies suggest a relationship between the fascial structure and certain clinical characteristics, their findings are limited to specific patient populations or patients with localized impairments. Additionally, although fascial thickness has been reported to be associated with aging, flexibility, and obesity16), no study has comprehensively examined its relationship with physical performance (e.g., gait speed and handgrip strength) and daily physical activity in community-dwelling older women.
Therefore, the present study aimed to evaluate lower limb skeletal muscle quality using a diagnostic ultrasound system by incorporating fascial thickness and conventional muscle echo intensity in the muscle parenchyma. We sought to provide a multifaceted assessment of muscle quality and clarify its relationship with physical function and habitual physical activity.
Accordingly, this study was designed as a basic research study aimed at the prevention and early detection of sarcopenia through the assessment of lower limb muscle mass and quality using a diagnostic ultrasound system. Specifically, we investigated the influence of walking function on lower-limb skeletal muscles and its association with daily physical activity in independently living community-dwelling older women who did not require long-term care or support.
Patients and Methods
Study design
This was a cross-sectional study.
Patients
Community-dwelling women aged 66–89 years, who lived independently in Prefecture A and consented to participate in the study, were selected. Patients with dementia, undergoing cancer treatment or dialysis, and with lower limb impairment were excluded from the study. The method used to recruit participants involved explaining the study to the supervisors of senior centers and community centers that offer exercise classes for seniors in Prefecture A. Using a study request form, the study was explained to older women at the facilities that cooperated in study recruitment who fulfilled the study requirements, and those who consented to participate were included in the study.
Study period
The study was conducted from September 2022 to December 2022.
Data collection
Study procedure
Study participants were given an activity monitor 7–10 days before the physical measurements and they were asked to wear it from waking up until bedtime for three consecutive days until the day before the physical measurements, to measure the step count, exercise level in daily life, and walking exercise level. On the day of the study, the participants were administered a questionnaire that asked about their age and number of falls they had experienced in the past month. A diagnostic ultrasound system was used to measure the muscle thickness, fascial thickness, and muscle echo intensity. Finally, the walking test was conducted.
Reliability and validity of the diagnostic ultrasound system measurements
Ultrasound measurements were performed by a researcher who had received one month of specialized training under the supervision of a physical therapist with expertise in musculoskeletal ultrasonography. The training emphasized probe placement and proficiency was determined before the start of the study.
All ultrasound measurements were performed by a single examiner to eliminate inter-rater variability. The examiner was a trained researcher who completed one month of specialized instruction under the supervision of a physical therapist with expertise in musculoskeletal ultrasonography. Proficiency in probe handling and image acquisition was confirmed prior to the start of data collection. To minimize tissue deformation and ensure reproducibility, a generous amount of ultrasound gel was applied, and the probe was gently placed on the skin without exerting pressure. Each measurement was performed twice, and the mean of the two measurements was used for analysis.
Intrarater reliability was assessed using the intraclass correlation coefficient (ICC) [1, k]. All three muscle-related indices (muscle thickness, fascial thickness, and muscle echo intensity) demonstrated excellent reproducibility, with ICC values exceeding 0.9.
Study description
Questionnaire survey
A questionnaire survey was used to obtain information about the participants’ age, physical activity, exercise status in daily life and in a typical week, and the number of falls experienced in the past month.
Physical measurements
The following physical characteristics were measured: weight, skeletal muscle mass, body fat percentage, and skeletal muscle index (SMI). All were assessed using a body composition analyzer (RD-800 InnerScan Dual, Tanita, Tokyo, Japan). This device has been used in previous studies involving healthy adults to provide valid and reliable measurements of body composition including segmental muscle mass17).
Measurement of lower limb skeletal muscle thickness, fascial thickness, and muscle echo intensity using a diagnostic ultrasound system
Ultrasound measurements were performed using a diagnostic ultrasound system (JX3-Exp; MediCare, Yokohama, Japan) equipped with a high-frequency linear probe (4–16 MHz). To ensure consistency, the right leg was used for all measurements. The participants were positioned in a prone position with their feet hanging freely off the edge of the bed, allowing the lower limb to rest in a relaxed and neutral position. The medial head of the gastrocnemius muscle was selected as the representative superficial muscle because of its accessibility, clearly distinguishable fascial layers, and high imaging reproducibility. The measurement site was defined as the region in which the muscle belly appeared most prominently.
All ultrasound procedures were performed following standardized protocols adapted from previous studies18,19,20) with minor modifications appropriate for the gastrocnemius anatomy. Figure 1 illustrates the procedures for measuring the muscle thickness, fascial thickness, and muscle echo intensity at this site.
Figure 1.
Ultrasound imaging assessment of the gastrocnemius muscle: muscle thickness (left), fascial thickness (center), and muscle echo intensity (right)
To measure muscle thickness, the probe was aligned along the short axis of the muscle, and two images were obtained at the thickest point of the muscle belly. The muscle parenchyma was measured, excluding the fascia, using the digital caliper function of the device. The average of these two values was used in the analysis.
To assess the fascial thickness, the probe was rotated by 90° to align it with the long axis of the muscle, and two images were captured at the same site. The thickness of the superficial fascia (from the surface to the deep border of the epimysium) was measured and averaged. Muscle echo intensity was calculated using the ImageJ software (NIH, Bethesda, MD, USA) from the same two short-axis images used for muscle thickness measurements. A standardized region of interest (ROI) was defined (width: four scale marks centered on the image; height: 0.5 scale marks starting just beneath the superficial fascia), and mean grayscale values (8-bit, range: 0–255) were computed.
Walking function evaluation
A 10-meter normal walking test was performed outdoors. During the test, participants were asked to walk normally in a straight line in a 16-meter section that included a preliminary pathway, and the measurements were performed over a 10-meter section that excluded the preliminary pathway. A walking analysis system (AYUMIEYE: Waseda Elderly Health Association, Tokyo, Japan) was used to measure walking speed and stride length. The measurements were performed twice, and the better of the two results was used for the analysis of both walking speed and stride length.
Evaluation of physical activity in daily life
Step count, level of exercise in daily life, and walking exercise level (Ex) were measured for three days using an activity monitor (HJA-750 activity monitor, OMRON, Kyoto, Japan), and the mean values for the 3 days were used for analysis. The participants were asked to wear a monitor on the waist of their pants from waking up to bedtime.
Risk of Sarcopenia
In this study, sarcopenia-related traits were evaluated based on the criteria proposed by the AWGS 2019, using the skeletal muscle mass index (SMI) as an indicator of muscle mass and gait speed as an indicator of physical performance. We recruited community-dwelling older women who were independent in their activities of daily living (ADL); thus, we did not target a clinical or frail population. Therefore, we assessed sarcopenia-related traits based on gait speed and SMI and did not include handgrip strength. While we acknowledge that handgrip strength is a key component of formal diagnostic criteria, such as the AWGS or the European Working Group on Sarcopenia in Older People (EWGSOP), we believe that evaluating gait speed and SMI remains meaningful in identifying early muscle decline in a healthy population7).
Because handgrip strength was not assessed, a formal diagnosis of sarcopenia was not made according to the full AWGS 2019 criteria. Instead, to explore the potential early signs of sarcopenia in this population, we calculated the number and percentage of participants who met the cutoff value for either low gait speed (<1.0 m/s) or low SMI (<5.7 kg/m2), as defined by the AWGS 2019. The number and percentage of participants who met these criteria were calculated using descriptive statistics.
Statistical analysis
All data were entered into a personal computer and descriptive statistics were calculated using statistical analysis software (SPSS Ver. 27 for Windows; IBM, Armonk, NY, USA), and the data were analyzed.
Initially, the number and percentage of participants who met the cutoff value for either low gait speed (<1.0 m/s) or low SMI (<5.7 kg/m2) as defined by the AWGS 2019 were calculated to explore the potential risk of sarcopenia in this population.
Next, using univariate analysis, the correlations between the evaluation indices of gastrocnemius muscle mass and quality (muscle thickness, fascial thickness, and muscle echo intensity) and the following variables were assessed: age, height, weight, body fat percentage, skeletal muscle index, walking speed, stride length, step count, walking exercise level, exercise level in daily life, housework time, daily exercise status (exercise types and duration during the week), inactive time, and number of falls in the past month. For multivariate analysis, a regression analysis was performed for explanatory variables identified from survey items with a P-value <0.1 in the correlation analysis and items for which a relationship was found in previous studies, and factors related to gastrocnemius muscle thickness, fascial thickness, and muscle echo intensity were identified. To determine the intra-examiner reliability with respect to the measured values of the gastrocnemius muscle thickness, fascial thickness, and muscle echo intensity, the intraclass correlation coefficient (ICC; 1, k) was calculated. The results for the ICCs for gastrocnemius muscle thickness, fascial thickness, and muscle echo intensity confirmed high reproducibility of ≥0.9 for all indices, indicating that the reliability of the values obtained by using means as analysis data was high. These values were derived by having a single examiner perform two measurements, and the mean of the two was used as the analysis data, indicating high intra-examiner reliability.
Results
Attributes of the participants
The study participants were 54 individuals living in Prefecture A, who provided informed consent. One of the 54 individuals for whom data were collected had severe lower limb edema and was therefore excluded from the study. Consequently, data from 53 individuals were included in the analysis. The attributes of the 53 participants are listed in Table 1.
Table 1. Characteristics of the participants (n=53).
| Variable | Mean ± SD | Median [IQR] | Range (Min–Max) |
|---|---|---|---|
| Age (years) | 77.1 ± 5.5 | 77 [73.0–80.5] | 66–89 |
| Height (cm) | 151.2 ± 5.6 | 150.3 [147.6–154.8] | 142.0–164.4 |
| Weight (kg) | 52.2 ± 8.6 | 51.0 [46.5–53.9] | 36.9–79.1 |
| BMI (kg/m2) | 22.8 ± 3.5 | 22.2 [20.4–24.5] | 16.9–35.2 |
| Body fat percentage (%) | 31.3 ± 6.8 | 30.6 [26.3–35.7] | 18.2–51.4 |
| SMI (kg/m2) | 6.5 ± 0.7 | 6.5 [6.0–7.1] | 5.0–7.8 |
Values are presented as means ± standard deviations (SD), medians with interquartile ranges [IQR], and minimum–maximum ranges. BMI: body mass index; SMI: skeletal muscle index.
Risk of sarcopenia
Based on the AWGS 2019 criteria, we explored the potential risk of sarcopenia by identifying participants who met the cut-off values for either low gait speed (<1.0 m/s) or low SMI (<5.7 kg/m2). Six participants (11.3%) met the criteria for low SMI and three participants (5.7%) met the criterion for low gait speed. None of the participants simultaneously met both criteria.
Results for walking function and physical activity in older women
Walking function
Three participants (5.7%) had a walking speed of less than 1.0 m/s, indicating a measurable decline in walking function in a portion of the sample. The walking function measurements showed the following trends:
The average walking speed was 1.3 m/s (standard deviation [SD]=0.2), with a median of 1.3 m/s. The interquartile range (IQR) was 1.2–1.5 m/s, with a minimum of 0.8 m/s and a maximum of 1.7 m/s. The mean stride length was 67.7 cm (SD=7.9 cm), with a median of 67.7 cm. The IQR was 63.8–73.4 cm, with a minimum of 47.1 cm and a maximum of 82.1 cm.
Physical activity status
Large individual differences in physical activity have been observed in daily life, which are influenced by factors such as health status and consciousness. These variations are reflected in the measurement results.
The mean step count over three days was 5,445 steps (SD=2,307.9), with a median of 5,615.3 steps. The interquartile range (IQR) was 4,069.0–6,647.2 steps, and the minimum and maximum values were 433.0 and 12,184.3 steps, respectively. The mean walking exercise level over 3 days was 1.5 (SD=1.1), with a median of 1.3. The IQR was 0.7–2.1, and the range was 0 to 5.7. The mean daily exercise level over 3 days was 3.7 (SD=1.4), with a median of 3.5. The IQR was 2.7–4.4, with a minimum of 1.1 and a maximum of 7.6.
Housework time averaged 210.4 minutes per day (SD=90.5), with a median of 180.0 minutes. The IQR was 135.0–290.0, and the range was 60.0 to 400.0 minutes. The average sitting time was 5.2 hours per day (SD=1.9), with a median of 5.0 hours. The IQR was 4.0–6.0 hours, and the range was 1.0 to 10.0 hours.
Characteristics of the gastrocnemius muscle in older women
On the ultrasound images, differences in muscle quality were more visually prominent than differences in muscle thickness. Notable features associated with decreased muscle quality include fascial thickening and a segmented or discontinuous fascial border between the fascia and muscle parenchyma. In Figure 2, the left image shows the gastrocnemius muscle with a thin and clearly defined fascia, whereas the right image shows fascial thickening with a more segmented and irregular border. These findings suggest that structural changes are associated with reduced mobility and aging. Increased muscle echo intensity, as shown in Figure 3, was associated with the thickening of the endomysium surrounding the muscle fibers, a blurred reticular (network-like) structure, and a higher prevalence of hyperechoic (white) areas. Specifically, the left image shows a low-echo region with a well-defined reticular structure, whereas the right image displays a high echo intensity and a blurred internal network, indicating potential intramuscular fat infiltration or fibrosis. These echoic characteristics may occur even in the absence of visible muscle atrophy. The measurement results showed the following trends: Gastrocnemius muscle thickness averaged 16.0 mm (SD=2.1), with a median of 15.9 mm and an interquartile range (IQR) of 14.4–17.8 mm. Fascial thickness had a mean of 2.0 mm (SD=0.7), the median was 1.9 mm, and the IQR was 1.5–2.3 mm. Muscle echo intensity averaged 114.8 (SD=18.0), with a median of 112.7 and an IQR of 102.9–127.1.
Figure 2.
Differences in the gastrocnemius muscle fascia: normal (left) vs. thickened (right)
Figure 3.
Differences in gastrocnemius muscle echo intensity: low intensity with clearly defined endomysial reticular structure (left) vs. high intensity with blurred structure (right)
Relationships of gastrocnemius muscle thickness, fascial thickness, and muscle echo intensity with physical characteristics, walking function, and physical activity
The relationships between gastrocnemius muscle thickness, fascial thickness, and muscle echo intensity and physical characteristics, walking function, and physical activity are shown in Table 2.
Table 2. Relationships between the gastrocnemius muscle and physical characteristics, walking function, and physical activity (overall).
| Variable | Muscle thickness | Fascial thickness | Echo intensity | ||||||
|---|---|---|---|---|---|---|---|---|---|
| Rho | P-value | Rho | P-value | Rho | P-value | ||||
| Age | −0.36 | ** | <0.01 | 0.02 | 0.89 | 0.31 | * | 0.03 | |
| Weight | 0.14 | 0.31 | 0.37 | ** | <0.01 | 0.13 | 0.35 | ||
| Body fat percentage | −0.10 | 0.49 | 0.55 | ** | <0.01 | 0.09 | 0.53 | ||
| SMI | 0.33 | * | 0.02 | 0.22 | 0.11 | −0.27 | * | <0.05 | |
| Walking speed | 0.40 | ** | <0.01 | −0.31 | * | 0.02 | −0.35 | ** | <0.01 |
| Stride length | 0.38 | ** | <0.01 | −0.24 | † | 0.08 | −0.20 | 0.16 | |
| Mean step count /3 days | 0.16 | 0.26 | −0.20 | 0.15 | −0.27 | † | 0.05 | ||
| Walking exercise level /3 days | 0.23 | † | 0.10 | −0.27 | * | <0.05 | −0.19 | 0.16 | |
| Exercise level in daily life /3 days | 0.30 | * | 0.03 | −0.14 | 0.31 | −0.19 | 0.16 | ||
| Walking time | 0.06 | 0.65 | −0.14 | 0.32 | −0.22 | 0.12 | |||
| Calisthenics / stretching time | −0.03 | 0.83 | −0.09 | 0.50 | −0.04 | 0.77 | |||
| Muscle training time | 0.12 | 0.41 | −0.01 | 0.95 | 0.03 | 0.82 | |||
| Total exercise time | −0.32 | * | 0.02 | 0.05 | 0.72 | 0.12 | 0.41 | ||
| Housework time | 0.14 | 0.33 | 0.02 | 0.88 | −0.26 | † | 0.06 | ||
| Sitting time/day | 0.10 | 0.48 | 0.16 | 0.25 | −0.13 | 0.37 | |||
| Number of falls/month | −0.09 | 0.54 | 0.20 | 0.15 | 0.10 | 0.49 | |||
Values represent Spearman’s correlation coefficients (ρ) and corresponding P-values.
Bold values indicate statistically significant correlations.
**P<0.01 (two-sided); *P<0.05 (two-sided); †P<0.1 (two-sided).
BMI: body mass index; SMI: skeletal muscle index.
These observed changes in gastrocnemius muscle mass and quality—specifically, reduced muscle thickness, increased fascial thickness, and elevated muscle echo intensity—were associated with physical characteristics such as aging and increased body fat percentage, which may reflect muscle loss rather than true obesity, as well as with reduced walking function and daily physical activity.
Factors related to gastrocnemius muscle thickness, fascial thickness, and muscle echo intensity
Regression analysis was performed to identify factors related to gastrocnemius muscle thickness, fascial thickness, and muscle echo intensity, which were shown in the correlation analysis to be related to age, physical characteristics, walking function, and physical activity in daily life. First, the variables were narrowed down to 5 variables (age, body fat percentage, exercise level in daily life, walking exercise level, and daily sitting time) from the items for which a relationship was found in previous studies and in the correlation analysis of the present study, and an analysis was performed using the forced-entry method. The results showed that, of the parameters of muscle thickness, fascial thickness, and muscle echo intensity, muscle thickness was related to exercise level in daily life (β=0.28, P=0.05, adjusted R2=0.14), and fascial thickness was related to body fat percentage (β=0.58, P<0.01, adjusted R2=0.31) (Tables 3, 4). Muscle echo intensity was not significantly associated with any of the explanatory variables.
Table 3. Factors related to gastrocnemius muscle thickness.
| Model 1 - Muscle thickness (Adjusted R²=0.14, P=0.03) | ||||
|---|---|---|---|---|
| Explanatory variable | Standardized β | P-value | 95% CI | |
| Age | −0.24 | 0.11 | [−0.21, 0.02] | |
| Body fat percentage | −0.03 | 0.84 | [−0.10, 0.08] | |
| Walking exercise level | 0.09 | 0.53 | [−0.38, 0.73] | |
| Exercise level in daily life | 0.28 | * | 0.05 | [0.00, 0.84] |
| Daily sitting time | 0.17 | 0.23 | [−0.13, 0.52] | |
Regression analysis using the forced-entry method. *P<0.1 was considered statistically significant (two-sided).
Results are based on multiple linear regression using the forced-entry method. Standardized β coefficients, P-values, and 95% confidence intervals (CI) are shown. Adjusted R2=0.14, *P<0.1 was considered statistically significant (two-sided).
Table 4. Factors related to gastrocnemius fascial thickness.
| Model 2 - Fascial thickness (Adjusted R²=0.31, P=<0.01) | ||||
|---|---|---|---|---|
| Explanatory variable | Standardized β | P-value | 95% CI | |
| Age | −0.17 | 0.21 | [−0.05, 0.01] | |
| Body fat percentage | 0.58 | * | <0.01 | [0.03, 0.08] |
| Walking exercise level | −0.20 | 0.12 | [−0.29, 0.04] | |
| Exercise level in daily life | −0.15 | 0.23 | [−0.20, 0.05] | |
| Daily sitting time | −0.20 | 0.13 | [−0.17, 0.02] | |
Regression analysis using the forced-entry method. *P<0.05 was considered statistically significant (two-sided).
Results are based on multiple linear regression using the forced-entry method. Standardized β coefficients, P-values, and 95% confidence intervals (CI) are shown. Adjusted R2=0.31, *P<0.05 was considered statistically significant (two-sided).
In regression analysis using the forced-entry method, muscle thickness, fascial thickness, and muscle echo intensity were used as outcome measures. The regression model was created based on physical activity items quantified using age, physical characteristics, and measurement equipment, based on the findings and correlation analysis results reported in previous studies or those found in the technical literature. However, the factors related to muscle echo intensity and muscle quality index could not be determined based on the five explanatory variables selected. In addition, no relationship was observed between fascial thickness and physical activity, although body fat percentage, a physical characteristic, was related to fascial thickness.
Furthermore, because there were several survey items related to physical activity, including subjective and objective indices on the questionnaire, the stepwise method was used to broadly investigate factors related to muscle thickness, fascial thickness, and muscle echo intensity. To implement the stepwise method, the following variables were added to the explanatory variables selected using the forced-entry method: mean step count, walking time (minutes) per week, calisthenic time (minutes) per week, total exercise time (minutes) per week, and housework time (minutes) per week. The results showed that age (β=−0.38, P<0.01, adjusted R2=0.12) was related to gastrocnemius muscle thickness, and that mean step count (β=−0.31, P=0.02, adjusted R2=0.08) was related to muscle echo intensity.
Discussion
Gastrocnemius muscle characteristics and sarcopenia risk in community-dwelling, older women living independently
Although community-dwelling older women living independently were selected for this study, there was a trend toward a decrease in gastrocnemius muscle thickness with age, and the skeletal muscle index of approximately 10% of the participants was below the AWGS 2019 criteria for sarcopenia.
Furthermore, in terms of physical function, a small number of participants had gait speeds <1.0 m/s. This threshold is often used as a clinical indicator of reduced mobility in older adults and may reflect early signs of lower-limb functional decline in this population.
Sarcopenia is a condition in which skeletal muscle mass decreases owing to aging or disease. A decline in skeletal muscle mass, which typically begins in the 40s, contributes to reduced muscle strength and impaired physical function. Subjective symptoms of sarcopenia are often detected together with adverse health events that cause a decrease in ADL, such as falls. This often occurs later in life, when the individual becomes aware of symptoms before a certain level of decrease in skeletal muscle mass, muscle strength, or physical function3). Participants in the present study whose skeletal muscle index was below the criterion, maintained their walking speed above the criterion and had no subjective symptoms at the time of the survey. The values for muscle thickness, fascial thickness, and muscle echo intensity obtained in the lower limb skeletal muscle evaluation, which were considered the outcome measures in this study, were measured using a diagnostic ultrasound system. Relationships to sarcopenia were observed for the skeletal muscle index, gastrocnemius muscle thickness, and muscle echo intensity, which are required for the AWGS 2019 sarcopenia evaluation. However, when the skeletal muscle index was low and little muscle was present, the values for both muscle echo intensity and fascial thickness were low in this study; there were participants with good muscle quality, in whom the network structure of the muscle tissue was distinct, and who did not have decreased walking function, which is also a sarcopenia evaluation item. Conversely, when the skeletal muscle index was above the sarcopenia criterion, adequate muscle with an absence of lower-limb edema, high muscle echo intensity, and fascia segmentation and thickening was observed in participants with increased body fat percentage, which may reflect muscle mass loss rather than true obesity. Decreased walking function was observed when the muscle quality was low. Regarding the skeletal muscle index, no standard method has been established to address cases in which skeletal muscle mass is overestimated or underestimated owing to lower-limb edema or poor compatibility between different types of measuring equipment. Consequently, muscle quality and skeletal muscle mass should be evaluated to detect sarcopenia early.
Lower limb skeletal muscle evaluation using a diagnostic ultrasound system and the feasibility of early sarcopenia detection
To avoid the effects of overestimation of skeletal muscle mass due to equipment differences and body fluid retention in the evaluation of the lower limb skeletal muscle, this study used a diagnostic ultrasound system that can visualize muscle quality, which also affects muscle strength, to investigate strategies for early sarcopenia detection.
In evaluations of lower limb skeletal muscle in previous studies, muscle thickness was used as a quantitative evaluation index, and muscle echo intensity was used as a qualitative evaluation index. However, evaluating muscle echo intensity using grayscale values is a relative assessment, and the increase in muscle echo intensity associated with the decrease in muscle quality that begins in middle age has been found to slow down late in life, with no significant changes observed during this period21). A possible reason why the change in muscle echo intensity slows late in life is that the values remain high when the whiteness of the muscle parenchyma area reaches a certain level, making evaluation difficult. Increased muscle echo intensity refers to a condition in which fascial thickening occurs due to fibrosis and fatty infiltration caused by an increase in denatured collagen in the perimysium and endomysium of the muscle parenchyma13). Consequently, although echo intensity tends to remain at a high level late in life, the thickness of the epimysium surrounding the muscle parenchyma can be measured as an absolute value, similar to muscle thickness, enabling the evaluation of fatty infiltration and fibrosis status. Therefore, fascial thickness (the thickness of the epimysium on the surface) was introduced as a novel evaluation index in this study. The results showed relationships between the gastrocnemius muscle and age, physical characteristics, walking function, and physical activity, indicating that this muscle can be used as the quadriceps femoris muscle, which has been used as the main evaluation in previous studies. Moreover, the results suggested that walking speed was related to gastrocnemius muscle thickness, fascial thickness, and muscle echo intensity, and that decreased muscle thickness, fascial thickness, and muscle echo intensity were associated with decreased walking function. Walking speed was used as a criterion for sarcopenia. Consequently, it may be possible to utilize the gastrocnemius muscle thickness, fascial thickness, and muscle echo intensity, which are related to decreased walking function, as novel evaluation indices for the early detection of sarcopenia.
This study used gastrocnemius muscle thickness, fascial thickness, and muscle echo intensity as outcome measures, and broadly investigated the factors related to these measures based on subjective and objective evaluation items related to physical characteristics and physical activity. The results showed that age was related to muscle thickness, body fat percentage was related to fascial thickness, and step count during daily activities was related to muscle echo intensity. Fukumoto et al.21) found that, similar to age-related degeneration of the quadriceps femoris muscle, gastrocnemius muscle thickness also decreased with age. Moreover, with regard to muscle quality evaluation indices that used fascial thickness and muscle echo intensity, degeneration was found to be largely complete later in life, and no age effect was observed.
Okita13) reported that prolonged immobility due to disuse syndrome resulted in the progression of fascial collagen degeneration and fascial thickening. However, the results of the present study indicated that decreased physical activity and increased body fat percentage were related to fascial thickening in older women and that ectopic fat infiltration into the muscle may have a greater impact than fascial fibrosis.
This interpretation should be made with caution because an increase in body fat percentage may also reflect a reduction in muscle mass rather than true obesity. These findings suggest that promoting regular exercise habits among community-dwelling older women may contribute not only to improvements in skeletal muscle mass but also to enhancements in muscle quality of the lower limbs. Therefore, a longitudinal follow-up study is warranted to examine the changes in fascial thickness and muscle echo intensity in relation to individual exercise patterns or routines. In addition, Tabata et al.22) examined the effects of sarcopenia exercise habits in middle and high school on occurrence in elderly individuals and found that regular exercise, both when young and elderly, reduced the risk of sarcopenia. These findings indicate that identifying individuals at a high risk of sarcopenia and preventing them before they become elderly extends their healthy life expectancy.
Limitations
This study utilized a JX3-Exp ultrasound system and an RD-800 device for bioelectrical impedance analysis (BIA). The JX3-Exp, which is marketed in Japan as a research instrument, is an OEM version of the Sonoscape X3Exp system that is used clinically in international settings and complies with global safety standards. However, as no validation studies for the JX3-Exp were indexed in PubMed, this remains a limitation of the present study. Furthermore, the intra-rater reliability of the ultrasound measurements was confirmed, with intraclass correlation coefficients (ICC 1, k) exceeding 0.9 for all indices. These results indicate a high level of measurement consistency and help mitigate concerns regarding measurement bias.
In contrast, the RD-800 BIA device has been examined in previous studies involving community-dwelling adults, and has been shown to provide valid and reliable measurements of body composition, including segmental muscle mass. These findings support the appropriateness of their use in the present study.
Conclusions
Although community-dwelling older women living independently were selected, there was a trend toward a decrease in gastrocnemius muscle thickness with age, and the skeletal muscle index was below the AWGS 2019 criterion for sarcopenia in 11.3% of participants.
The results indicated that aging, increased body fat percentage, and decreased walking function and physical activity in daily life were associated with reductions in gastrocnemius muscle mass and quality. This interpretation should be made with caution, as an increased body fat percentage may reflect reduced muscle mass rather than true obesity.
Regression analysis (forced entry method) using gastrocnemius muscle thickness, fascial thickness, and muscle echo intensity as dependent variables, and age, body fat percentage, exercise level in daily life, walking exercise level, and daily sitting time as explanatory variables indicated that only fascial thickness was related to an increase in body fat percentage.
To broadly investigate the factors related to gastrocnemius muscle mass and quality evaluation indices, a regression analysis (stepwise method) was performed with mean step count, walking time, calisthenics time, total exercise time, and housework time added to the explanatory variables of age, body fat percentage, exercise level in daily life, walking exercise level, and daily sitting time. The results indicated that age was related to gastrocnemius muscle thickness, and step count was related to muscle echo intensity.
Conflict of interest
The authors declare no conflicts of interest.
Funding information
This study was funded by the University of Shiga Prefecture Special Research Project grant from 2022 to 2024.
Ethics approval and consent to participate
This study was approved in advance by the human subjects research ethics committee of the University of Shiga Prefecture (approved on October 25, 2022; approval number 882-2). Informed consent was obtained from all participants after full disclosure of the aims and procedures of the study.
Consent for publication
All authors have agreed to the publication of this paper in the Journal of Rural Medicine.
Author contributions
K. S. was responsible for developing the research concept, design, analysis, interpretation of the results, original writing, and editing. Y. D. and Y. S. contributed to data analysis, interpretation, and editing of the manuscript.
Author’s note
This reference list is part of a doctoral dissertation submitted to the Graduate School of Nursing, Osaka Prefecture University, in partial fulfillment of the requirements for the Doctor of Nursing Science degree.
Acknowledgments
The authors express their gratitude to the participants for their cooperation. In addition, they are deeply grateful to Prof. Emeritus Kiyoji Tanaka of the University of Tsukuba and Associate Prof. Shinichi Shirahoshi of Bukkyo University for their guidance in evaluating and analyzing the lower limb skeletal muscles using a diagnostic ultrasound system.
Data availability statement
The data used in this study cannot be linked or shared without permission for ethical reasons.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The data used in this study cannot be linked or shared without permission for ethical reasons.