ABSTRACT
Aim
Recent studies associate computed tomography (CT) measurements of the quadriceps femoris with fall risk. However, no study has examined the relationship between falls and each individual quadriceps component. This study longitudinally investigated the association between CT values and cross‐sectional areas of individual quadriceps components and the occurrence of falls 1 year later.
Methods
Single‐slice CT images of the right mid‐thigh were obtained at the initial visit from 246 patients (Age: 77.4 ± 6.6, Male: 80) who returned for follow‐up after 1 year. The quadriceps femoris was segmented into the whole muscle, rectus femoris, vastus medialis, vastus lateralis, and vastus intermedius. For each compartment, cross‐sectional area and mean CT value (average pixel value within a segmented region, representing muscle quality) were calculated. Participants were categorized into fall and non‐fall groups based on new falls during the one‐year follow‐up. Associations between baseline measurements and subsequent falls were analyzed.
Results
Among females in the fall group, CT values of the whole quadriceps femoris, vastus lateralis, and vastus intermedius were significantly lower (p < 0.01, p < 0.05, and p < 0.01, respectively). Binary logistic regression analysis showed that among all CT values, only that of the vastus intermedius was a predictor of falls (p < 0.01; odds ratio, 0.92; 95% confidence interval, 0.862–0.978). The cutoff value was 49.1 Hounsfield units.
Conclusion
Cross‐sectional area was not associated with falls, whereas the CT value of the vastus intermedius was significantly associated with fall occurrence. These findings suggest that the condition of the vastus intermedius may play an important role in fall risk.
Keywords: falls, muscle quality, older adults, quadriceps femoris, vastus intermedius
The CT value of the vastus intermedius, but not its cross‐sectional area, is significantly associated with falls, highlighting muscle quality's role in fall risk. This indicates that muscle condition is crucial for understanding fall risk.
1. Introduction
Rosenberg proposed the term sarcopenia to describe the condition in which muscle mass and physical function decline with aging [1]. In 2018, the European Working Group on Sarcopenia [2] emphasized the importance of muscle quality in addition to muscle strength, muscle mass, and physical capacity in older adults with sarcopenia. McGregor et al. identified muscle structure, myofiber type, metabolism, fibrosis, neural activation, and fat infiltration as determinants of muscle quality [3]. Indicators associated with muscle strength include muscle composition assessed by phase angle and ultrasound luminance, intramuscular fat infiltration, pennation angle, and muscle oxidative capacity [4]. Aging‐related deterioration in muscle quality includes reductions in the size and number of rapidly contracting type II muscle fibers [5] and increased intramuscular fat infiltration [6, 7].
One method of evaluating muscle quality is computed tomography (CT). CT produces muscle cross‐sections that allow for the measurement of fat and non‐fat masses, and the attenuation (CT value [CTV]) in Hounsfield Units (HU), which represents the signal intensity of CT, can be calculated from CT images of skeletal muscle. This value is related to lipid content in the muscle [8]. Therefore, CT is the gold standard for assessing muscle quality, which is influenced by various factors, including fat infiltration into the muscle [3, 9].
In a previous study using CT to examine muscle quality, Mizuno et al. investigated the relationship between quadriceps and knee extension strength using single‐slice CT of the thigh. They showed that the CT area (CTA) and CTV of the entire quadriceps were associated with knee extension strength in men and women. They also found that the CTVs of the rectus femoris (RF) area, vastus lateralis (VL) area, and vastus intermedius (VI) were associated with knee extension strength in women, whereas the VI area was associated with knee extension strength in men [10].
The relationship between knee extension strength and falls has been demonstrated in numerous studies [11, 12, 13], and Asakawa et al. reported that older adults with bilateral knee extension strength below 35% of body weight are at increased risk of falling. Age‐related declines in skeletal muscle mass generally begin after 50 years of age and are greater in the lower limbs than in the upper limbs regardless of sex [14]. Ultrasound studies further showed that, among lower limb muscles, those in the anterior thigh are more susceptible to aging than those in the posterior thigh [15]. In addition, sex‐related differences have been reported in age‐related changes in thigh composition: decreases in thigh cross‐sectional area are mainly attributed to reduced muscle mass in men and reduced fat mass in women, whereas quadriceps cross‐sectional area also decreases with age in women [16].
These findings suggest that evaluating the muscle quality of the quadriceps, which are located on the front of the thigh and are associated with reduced knee extension strength, is important for preventing falls. However, although each individual quadriceps muscle ultimately functions to extend the knee joint via the patella, the VI muscle differs from other muscles in that it works predominantly in the knee joint flexed position [17]. Therefore, evaluating each individual quadriceps muscle may be more important than evaluating the quadriceps as a whole, but there have been no reports on the relationship between individual muscle quality and falls.
In this study, we aimed to longitudinally clarify the relationship between the muscle quality of each quadriceps muscle and the occurrence of falls in patients examined at the outpatient services of the National Center for Geriatrics and Gerontology (NCGG), using muscle cross‐sectional area and CTVs to indicate muscle quality.
2. Methods
2.1. Participants
Between March 2016 and February 2021, 700 patients who visited the Integrated Healthy Aging Clinic at the NCGG and consented to participate in the Locomo–Frail–Sarcopenia Registry Study were enrolled. Among them, 153 patients scheduled for hip or knee orthopedic surgery and 6 patients who withdrew consent, 24 of missing CT data and 1 of missing Kihon Checklist score [18] were excluded, leaving 516 participants included in the study. Of these, 258 returned for a 1‐year follow‐up visit between June 2017 and December 2021. After excluding 12 participants with unanalyzable CT data, 246 patients were included in the final analysis (sarcopenia group, n = 61; non‐sarcopenia group, n = 185) (Figure 1a). Among these participants, 81 had experienced at least one fall before the initial assessment. The inclusion and exclusion criteria and assessment items of the Locomo–Frail–Sarcopenia Registry Study are shown in Figure 1b.
FIGURE 1.
(a) Participant selection for longitudinal studies. (b) Criteria for participation in Locomo–Frailty–Sarcopenia registry. The participant selection and criteria for participation in Locomo–Frailty–Sarcopenia registry research. (a) The participants were 700 patients who were examined at the outpatient services of the NCGG, Center for Frailty and Locomotive Syndrome, and agreed to participate in the Locomo–Frailty–Sarcopenia Registry Study. Of the 258 patients who returned for a follow‐up visit 1 year later, 12 were excluded due to missing CT data or data analysis difficulties. The presence or absence of an experience of falls was determined using the Kihon Checklist score by a questionnaire completed by the study participants at a 1‐year follow‐up visit. The participants who had new falls during the 1‐year follow‐up from baseline were classified as the fall (F) group, and those without falls as the non‐fall (NF) group. (b) Inclusion and exclusion criteria of Locomo–Frailty–Sarcopenia registry research.
2.2. Assessment Methods
We assessed various measures for all of the participants at the initial visit (baseline).
2.2.1. CT Images
One‐slice CT images of the central right thigh were taken in the supine position. The imaging system was a SOMATOM Sensation 64 (Siemens, Munich, Germany). The scan parameters were as follows: tube voltage, 120 kV; tube current, 120 mA; rotation time, 1 s; and field of view, 233 mm. The center of the thigh was defined as the midpoint of the line segment connecting the superior border of the patella to the center of the inguinal region (Figure 2a). The CT thigh images (Figure 2b) were classified into the quadriceps femoris (QF), RF, vastus medialis (VM), VL, and VI using SliceOmatic ver. 5.0 (Tomovision, Magog, Canada) image analysis software by three experienced image analysts, including an orthopedic surgeon (Figure 2c,d). The CTA and mean CTV of each segment were calculated. To achieve reliability of CTA and CTV classification, imaging data from 21 subjects were measured by three examiners in a previous study by our research group, and the associated intraclass correlations were calculated. The intraclass correlations between examiners for the CTA and CTV were ≥ 0.998, and the intraclass correlation between the three examiners was 0.999 [19]. The preliminary study was conducted under a double‐blind system, following a manual prepared in advance by examiners who did not include any third parties other than the research center. The CTV indicates X‐ray absorbance, which was defined as −1000 HU for air and 0 HU for water, 40–100 HU for muscle, and approximately −50 to −100 HU for fat.
FIGURE 2.
Quadriceps muscle sectioning. (a) defines the midpoint of the right thigh. As shown in (a), the midpoint of the line connecting the upper edge of the right patella to the midpoint of the inguinal region was set as the center of the thigh. The original image captured at the midpoint of the thigh level (b) is divided into sections as shown in (c) and (d). (A) represents the rectus femoris muscle, (B) the vastus medialis muscle, (C) the vastus lateralis muscle, and (D) the vastus intermedius muscle. (E) represents the entire quadriceps femoris muscle, combining (A) through (D). RF: rectus femoris, VM: vastus medialis, VL: vastus lateralis, VI: vastus intermedius, QF: quadriceps femoris.
2.2.2. Leg Strength
Isotonic leg strength was measured using a motor function analyzer (zaRitz BM‐220, sampling frequency 80 Hz; Tanita Corporation, Tokyo, Japan) by dividing the vertical ground reaction force peak parameter (F: kgf) by body weight (W: kg) while participants stood up quickly from a chair with their arms crossed in front of their chest (F/W). This value was calculated by dividing the maximum vertical ground reaction force peak parameter among three attempts. Isometric knee extension strength was measured using a strain gauge‐based leg strength measurement device (ZP‐500N, sampling frequency 60 Hz; Imada Co. Ltd., Toyohashi, Aichi, Japan) developed by our center (intraclass correlation coefficient [1, 2] = 0.988) [20]. The participants were seated with their trunks and legs secured to the device with belts. The participants were placed at 90° of knee flexion, and a harness connected to the strain gauge was placed directly above their ankles. The test was conducted under the examiner's encouraging voice. In the analysis, the obtained value (kgf) was divided by body weight (kg).
2.2.3. Fall Experience Survey
The presence or absence of an experience of falls was determined using the Kihon Checklist score by a questionnaire completed by the study participants at a 1‐year follow‐up visit. The participants who had new falls during the 1‐year follow‐up from baseline were classified as the fall (F) group, and those without falls as the non‐fall (NF) group (Figure 1a).
2.3. Analysis Methods
Age, F/W, and the CTA and CTV of the RF, VM, VL, VI, and QF of the participants were compared between the two groups by sex in an analysis of covariance with age as a covariate. A binomial logistic regression analysis (BLRA) was performed using forced‐entry methods, with the presence of falls as the dependent variable, and the CTA and CTV for the RF, VM, VL, and VI as explanatory variables. Age and sex were used as adjustment variables. Odds ratios (ORs) and 95% confidence intervals (95% CIs) were obtained in the BLRA. The BLRA was used to determine the sensitivity, specificity, area under the curve, and cutoff values for factors significantly associated with the occurrence of falls using receiver operating characteristic curves. Baseline characteristics of analyzed and non‐analyzed participants were compared using Student's t‐test or chi‐square test.
A p value < 0.05 was considered significant. We used the statistical software IBM SPSS Statistics for Windows Version 28 (IBM Corp., Armonk, NY, USA) for all statistical analyses.
3. Results
A total of 246 patients (mean age: 77.4 ± 6.6 years, 166 women, 80 men) were included in the analysis. At the 1‐year follow‐up, there were 183 patients in the NF group and 63 in the F group. At the 1‐year follow‐up, there was no significant difference in the mean age of women between the two groups. However, in men, the F group had a significantly older mean age than the NF group (p < 0.05, Table 1). F/W was significantly lower in women in the F group than in the NF group (p < 0.001). No significant differences were observed in the CTA for the whole of the QF or any individual QF muscles in either sex. However, the F group had significantly lower CTVs for the VL, VI, and the entire QF in women (VL: p < 0.05, VI: p < 0.01, entire QF: p < 0.01). No significant differences in any CTVs were observed for any QF muscles in men.
TABLE 1.
Comparison between the NF group and the F group.
| Sex | Item | NF group (n = 183) | F group (n = 63) | p | |
|---|---|---|---|---|---|
| Age | 76.41 ± 6.67 | 78.54 ± 7.15 | 0.08 | ||
| Leg strength (R) | 0.37 ± 0.13 | 0.33 ± 0.01 | 0.10 | ||
| Female (n = 166) | F/W | 1.24 ± 0.09 | 1.17 ± 0.08 | p < 0.001 | |
| NF (n = 120) | CTV (HU) | RF | 49.34 ± 5.92 | 47.72 ± 6.98 | 0.18 |
| F (n = 46) | VM | 47.46 ± 7.66 | 44.76 ± 7.19 | 0.07 | |
| VL | 43.54 ± 6.59 | 40.36 ± 9.42 | p < 0.05 | ||
| VI | 49.85 ± 6.90 | 45.82 ± 7.76 | p < 0.01 | ||
| Whole QF | 45.64 ± 6.69 | 41.65 ± 7.51 | p < 0.01 | ||
| Age | 77.70 ± 6.21 | 80.59 ± 4.66 | p < 0.05 | ||
| Leg strength (R) | 0.46 ± 0.13 | 0.40 ± 0.12 | 0.24 | ||
| Male (n = 80) | F/W | 1.31 ± 0.10 | 1.26 ± 0.11 | 0.07 | |
| NF (n = 63) | CTV (HU) | RF | 50.43 ± 5.26 | 49.75 ± 4.42 | 0.99 |
| F (n = 17) | VM | 52.86 ± 7.97 | 50.69 ± 4.87 | 0.51 | |
| VL | 47.30 ± 5.72 | 47.07 ± 4.95 | 0.72 | ||
| VI | 53.46 ± 7.98 | 48.94 ± 4.46 | 0.06 | ||
| Whole QF | 50.19 ± 7.09 | 47.26 ± 4.35 | 0.23 | ||
| Female | CTA (cm2) | RF | 4.53 ± 1.18 | 4.39 ± 0.94 | 0.86 |
| VM | 6.87 ± 1.66 | 6.78 ± 1.37 | 0.74 | ||
| VL | 12.00 ± 2.92 | 11.79 ± 3.29 | 0.82 | ||
| VI | 12.03 ± 2.92 | 11.75 ± 2.67 | 0.68 | ||
| Whole QF | 37.05 ± 7.04 | 36.43 ± 6.80 | 0.67 | ||
| Male | CTA (cm2) | RF | 5.88 ± 1.37 | 5.55 ± 1.31 | 0.78 |
| VM | 9.88 ± 2.78 | 9.11 ± 2.06 | 0.63 | ||
| VL | 16.83 ± 4.27 | 14.82 ± 3.49 | 0.21 | ||
| VI | 16.62 ± 4.50 | 15.03 ± 3.17 | 0.38 | ||
| Whole QF | 51.00 ± 10.63 | 46.26 ± 7.83 | 0.28 | ||
Note: The results of analysis of covariance with age as a covariate.
Abbreviations: CI: Confidence interval, (Mean ± SD); CTA: CT area; CTV: CT value; F: Falls; NF: Non falls; OR: Odds ratio; QF: RF + VM + VL + VI; RF: rectus femoris; VI: vastus intermedius; VL: vastus lateralis; VM: vastus medialis.
The BLRA of the CTA did not show any significant individual QF factors that contributed to falls (Table 2). However, regarding the CTV, only the VI was a significant (p < 0.01) factor contributing to falls (OR: 0.92, 95% CI: 0.862–0.978).
TABLE 2.
The results of logistic regression analysis with the presence or absence of falls as the dependent variable.
| Item | B | p | OR | 95% CI of OR | ||
|---|---|---|---|---|---|---|
| Lower limit | Upper limit | |||||
| CTV | Age | 0.041 | 0.095 | 1.042 | 0.993 | 1.094 |
| Sex (1) | −0.167 | 0.641 | 0.846 | 0.42 | 1.706 | |
| RF | 0.02 | 0.56 | 1.021 | 0.953 | 1.093 | |
| VM | 0.01 | 0.73 | 1.01 | 0.952 | 1.072 | |
| VL | −0.006 | 0.862 | 0.994 | 0.93 | 1.062 | |
| VI | −0.085 | 0.008 | 0.918 | 0.862 | 0.978 | |
| CTA | Age | 0.053 | 0.049 | 1.054 | 1 | 1.111 |
| Sex (1) | −0.298 | 0.497 | 0.742 | 0.314 | 1.753 | |
| RF | 0.013 | 0.935 | 1.013 | 0.745 | 1.376 | |
| VM | 0.022 | 0.835 | 1.022 | 0.834 | 1.252 | |
| VL | −0.04 | 0.551 | 0.961 | 0.843 | 1.096 | |
| VI | −0.006 | 0.919 | 0.994 | 0.886 | 1.115 | |
Abbreviations: CTA: CT area, CTV: CT value, Sex (1): Female.
The cutoff value of the receiver operating characteristic curve for the VI, which was a significant factor related to the occurrence of falls, was 49.1 HU (sensitivity: 0.65, specificity: 0.62, area under the curve: 0.66) (Figure 3).
FIGURE 3.
Cutoff CT value of VI for falls. Vertical axis in the figure is sensitivity, horizontal axis is 1—specificity. Cutoff CT value of VI for fall is 49.1 HU, sensitivity is 0.65, specificity is 0.62, area under the curve (AUC) is 0.66.
Height and sex differed significantly between analyzed and non‐analyzed participants, whereas age, weight, and BMI did not.
4. Discussion
This paper presents the relationship between CT information and falls occurring 1 year later.
The main findings of this study are as follows. (i) There was no significant difference in the sex ratio of falls 1 year later between the F and NF groups. The F group had a significantly older age than the NF group, only in men. (ii) The F group showed significantly lower F/W values than the NF group only in women. (iii) No significant difference in CTA was found between the F and NF groups in men or women. However, the F group showed significantly lower CTVs only for VL, VI, and QF overall than the NF group in women. (iv) The BLRA indicated that VI was a significant factor for falls at 1 year.
The fall rate by sex in the community is higher in women than in men in Japan and other countries [21, 22]; however, this study did not find a significant difference in the incidence of falls between the sexes. This finding is thought to be partly due to the small number of men who had falls in this study. Regarding leg strength, in the relationship between knee extensor muscle strength and falls in older people, a study reported that falls were more likely to occur when knee joint extensor muscle strength was < 35% of body weight in each leg [11]. In the present study, female fallers had an isometric knee extension muscle strength relative to body weight of 0.33, which is consistent with the report of Asakawa et al. [11]. These results suggest that extensor muscle strength is related to falls in women, despite their younger age of falling than men. Knee extensor strength is strongly related to stair climbing and balance function [23] and is an independent factor in falls [24].
There were no significant differences in the CTAs of individual QFs between the two groups, regardless of sex. In contrast, only women who had falls showed significantly lower CTVs for the VL, VI, and whole QF than those without falls, suggesting poorer muscle quality. BLRA identified the VI as a significant factor associated with falls. A CT study of the whole QF reported that CTA was strongly associated with knee extension strength, whereas CTV was more strongly associated with motor function, including gait speed and chair rise time [18]. The association between lower VI CTV and falls suggests that VI function contributes to fall risk because balance, leg strength, and flexibility are important determinants of falls in community‐dwelling older adults [25]. Receiver operating characteristic analysis identified a VI CTV cutoff of 49.1 HU, a relatively low value within the general muscle CTV range of 40–100 HU. These findings suggest that CT assessment of muscle quality may be useful for predicting fall risk.
Aerobic exercise has been shown to reduce intramuscular lipids and improve glucose tolerance [26], whereas reduced physical activity increases intramuscular lipids even in healthy young adults [27]. Magnetic resonance imaging studies have also shown that physical activity suppresses increases in muscle fat and water content regardless of sex [7]. Together, these findings suggest that reduced physical activity impairs muscle quality, whereas exercise may improve muscle quality in older adults.
Declines in muscle fiber characteristics, structure, aerobic capacity, fibrosis, and neuromuscular activity impair intramuscular function [3]. Muscle quality deterioration may also precede skeletal muscle mass loss [3, 28]. Although muscle quality is generally higher in men younger than 80 years than in women, it declines with age in both sexes [16]. Therefore, evaluating muscle quality before skeletal muscle mass loss occurs may help prevent and correct age‐related declines in intramuscular function.
Anatomically, the VI is the most centrally located monoarticular muscle among the muscles that make up the QF, and is the most efficient knee extensor muscle, dominating other muscles in the QF during submaximal isometric knee extension [17, 29]. Architecturally, the VI features long muscle fibers and a small pennation angle, enabling high contraction velocity and a large range of motion, which best predicts knee extension force [30, 31]. The pennation angle refers to the anatomical angle between the muscle's axis of action and the course of the muscle fibers.
Based on these anatomical characteristics, the VI plays a crucial role during dynamic knee extension with the knee joint flexed, particularly contributing to the initial concentric phase and the final efferent phase of knee joint movement [17]. Therefore, knee extension muscle strength training focusing on the VI is effective for stabilizing the knee joint in a flexed position. Furthermore, because VI muscle fibers have a higher proportion of slow‐twitch muscle fibers than the VL, which is a synergist of the VI [32], exercise training involving slow muscle contractions is considered more appropriate than strength training focusing on quick movements. Exercise training for older people that takes into account the characteristics of the VI is effective in increasing muscle strength and maintaining balance and motor function, even at low intensities [33], and can have similar effects to high‐intensity training in improving muscle endurance and reducing the time to climb stairs [34].
A limitation of this study is as follows: (i) Not all participants were sarcopenic. As the role of each quadriceps muscle in falls may differ by sarcopenia severity, future studies should account for changes in sarcopenia during follow‐up. (ii) The follow‐up period of this study was only 1 year. (iii) The nature of participants' falls was unclear, and further research on fall‐related recovery is needed. (iv) Because analyzed and non‐analyzed participants differed in height and sex, potential attrition bias cannot be excluded. (v) Simple body weight normalization may cause underestimation in individuals with high body fat because it cannot differentiate muscle from fat mass. (vi) Although additional covariates were not considered in the logistic regression analysis, the results remained unchanged even after including sarcopenia in the exploratory analysis. Despite these limitations, to the best of our knowledge, this study is the first to report a relationship between the occurrence of fall events and the VI using single‐slice CT images of the right mid‐thigh.
5. Conclusions
This study reveals that leg strength is lower in women who have experienced falls compared to those who have not. Additionally, while the CTA is not associated with falls, the CTV of the VI is related to falls. These findings suggest that the VI, one of the muscles that comprise the QF, is involved in falls. We believe that these results will be useful for developing exercise programs that focus on VI function to prevent falls in older people.
Author Contributions
Conceptualization: Y.M., Y.H., Y.S., T.W., N.T., Hiroyasu A., Hidenori A. Methodology: Y.M., Y.H., Hiroyasu A., Hidenori A. Formal analysis: Y.H., Y.S., Y.M. Data curation: Y.S., N.T. Investigation: Y.M., Y.H., Y.S., N.T. Writing – original draft: Y.H. Writing – review and editing: Y.M., M.S., Hiroyasu A., Hidenori A. Supervision: T.W., M.T., S.S., S.M., Hiroyasu A., Hidenori A. All authors read and approved the final manuscript.
Funding
This study was supported in part by Research Funding for Longevity Sciences from the National Center for Geriatrics and Gerontology, Japan (grant numbers: 26‐12, 29‐12, 20‐12, and 22‐24); Co‐research funding for this study was provided by Tanita Corporation (1‐14‐2 Maeno‐cho, Itabashi‐ku, Tokyo, Japan; https://www.tanita.co.jp/). None of the grant providers played a role in the design, analysis, or writing of this manuscript.
Ethics Statement
The study was approved by the Ethics Committee of the National Institute for Longevity Sciences (Locomo, Frailty, and Sarcopenia Registry Study No. 881) and was conducted in accordance with the guidelines of the Declaration of Helsinki.
Consent
Written informed consent was obtained from each participant.
Conflicts of Interest
The authors declare no conflicts of interest other than research funding from Tanita Corporation.
Acknowledgments
The authors express their gratitude to all participants who provided useful data and to the staff involved in data organization. We also thank Ellen Knapp, PhD, from Edanz (https://jp.edanz.com/ac) for editing a draft of this manuscript.
Data Availability Statement
Research data are not shared.
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Data Availability Statement
Research data are not shared.