Abstract
Background
Muscle mass and phase angle (PhA) can be measured using multi-frequency bioelectrical impedance analysis (BIA). Osteoarthritis of the hip (OAhip) causes decreased muscle mass and PhA in the deformed lower limb. However, previous studies have not accounted for the influence of sex, and thus, the relationship between muscle mass, PhA, and motor function remains unclear. This study aimed to elucidate the relationship between PhA, an index of muscle mass and quality measured using BIA, and motor function during gait and standing in female patients with OAhip.
Methods
Muscle mass and PhA of patients with OAhip were measured using BIA. Motor function was evaluated using the Timed Up and Go test, ground reaction/weight, rate of force development/weight, and load ratio between the osteoarthritic (OA) and contralateral sides when standing up. The difference between the OA side and the contralateral lower limb was tested to clarify the characteristics of the deformed lower limb. The relationship between each motor function was determined using a partial correlation coefficient with age as a control variable and multiple regression analysis with each motor function as the dependent variable and age, OA-side muscle mass/body weight ratio, and PhA as independent variables.
Results
This study involved 60 patients with OAhip (age 65.6 ± 7.6 years, height 154.2 ± 6.0 cm, weight 56.8 ± 10.5 kg) scheduled for unilateral total hip arthroplasty. Muscle mass, PhA, and lower limb load ratio were significantly decreased in the lower limbs on the OA side. Furthermore, using a partial correlation coefficient with age as a control variable, PhA showed significant correlations with motor functions related to standing up and walking, and multiple regression analysis revealed that PhA was independently related to each motor function.
Conclusions
Evaluation and interventions that consider muscle quality rather than muscle mass are important.
Keywords: Bioelectrical impedance analysis, Muscle mass, Hip osteoarthritis, Phase angle
Background
Osteoarthritis of the hip (OAhip) is a chronic progressive disease that causes hip joint deformities. A study using radiography among community-dwelling people aged 50 years and older was conducted in Framingham, Massachusetts, USA, and reported that the prevalence of OAhip in their cohort was 19.6% [1]. Additionally, a survey conducted in North Carolina, USA, including participants with an average age of 63 years (range, 45–93 years) reported that the lifetime risk of symptomatic OAhip was 25.3% [2]. The main pathological condition of OAhip is muscle weakness and limited range of motion due to hip joint deformity, which causes pain when bearing weight [3, 4], leading to a decline in important daily life functions, such as standing up and walking; consequently, reducing the quality of life [5]. The global aging rate continues to rise, and a United Nations report predicts that the number of people aged 65 years and older will increase to one billion by 2050, making the global aging rate as high as 16% [6]. As the population ages, basic movements, including self-care, independent living, and walking, are predicted to become impaired and there are concerns that the burden on the medical system will increase [7]. Furthermore, aging is associated with the prevalence of chronic degenerative diseases, including OAhip, and the incidence of symptomatic OAhip increases significantly after the age of 50 years [8]. There is a high possibility of independent living becoming more difficult in patients with OAhip. Therefore, collecting knowledge and taking countermeasures for patients with OAhip will contribute to healthy aging.
Previous studies have focused on the muscles around the hip joint of patients with OAhip because the associated deformity in such patients leads to degeneration of these muscles. Multiple studies have used magnetic resonance imaging [9–12] and needle electromyography [13] to study the muscle quantity and quality. However, measurements using these highly specialized devices require invasive procedures, large-scale equipment, long hours of restraint, and highly skilled technicians [14], making simple and objective evaluation difficult. Therefore, a simple and objective muscle evaluation can be performed using multi-frequency bioelectrical impedance analysis (BIA) method, wherein a weak current is passed through the body, and the phase angle (PhA), which reflects muscle mass and cell health status, can be evaluated through electrical resistance. Although muscle mass is a generally interpretable index, PhA is calculated using reactance and resistance values and is regarded as an index reflecting the physiological function of cell membranes [15, 16]. PhA is also considered an indicator of muscle quality and is related to muscle strength and physical function [17–19]; therefore, individuals with good PhA may exhibit good muscle quality and high motor function.
Notably, few reports have employed the BIA method to evaluate muscle mass and PhA in patients with OAhip. Previous studies have indicated that using the BIA method for evaluating patients with OAhip may be an effective method with good reproducibility before and after total hip arthroplasty [20]. It has been observed that the PhA is decreased in the affected leg compared to the contralateral leg [21, 22], and this decrease in PhA is related to the quadriceps muscle [23]. Among these previous studies, reports using the BIA method on the OAhip included both male and female participants. Although, there has only been one report on Japanese participants, and the relationship with motor function was unclear. However, a recent cohort study found that the incidence of OAhip was 5.6 per 1000 person-years in males and 8.4 per 1000 person-years in females, as assessed using radiography [24]. In other words, there is a sex difference in the incidence of OAhip, with women having a higher incidence. Furthermore, it has been reported that there are sex differences in PhA values that can be measured using the BIA method, with females having lower values than males [25]. For these reasons, when analyzing OAhip using the BIA method, it is necessary to perform sex-standardized analyses. Additionally, most previous studies using PhA used systemic values as an indicator [15–19]. However, a report published in 2023 suggested that PhA levels may differ between the upper and lower limbs, and related motor functions may also differ [26, 27]. Therefore, when evaluating OAhip patients using the BIA method, it is necessary to exclude the influence of sex and evaluate the PhA of each body part. We believe that these studies will allow us to obtain detailed knowledge about PhA in OAhip patients, excluding the influence of sex, and will contribute to reconsidering treatment strategies. However, previous studies [20, 21, 23] often included mixed groups of males and females, and the influence of sex could not be completely excluded.
Additionally, OAhip patients have difficulty standing up due to hip joint deformity [28] and exhibit characteristic abnormal gait [13, 29]. Abnormal gait is particularly observed in the swaying of the trunk and pelvis, which is reported to be associated with Timed Up and Go (TUG) [29]. Therefore, we postulated that clarifying the relationship between motor function and TUG during standing and muscle mass and PhA, would provide useful knowledge for the prevention and improvement regarding motor function in OAhip patients. However, no study has investigated the relationship between PhA and muscle mass of the deformed lower limb, measured using the BIA method, and motor functions, including standing up and walking, in patients with OAhip.
By elucidating these points, we will contribute to the construction of basic data regarding muscle mass and PhA measured using the BIA method in patients with OAhip; considering characteristics of the disease and PhA, we will also contribute to understanding muscle mass and PhA as effective evaluation indicators and motor function. We believe that it would be possible to discuss effective intervention points from the perspective of muscle quantity and quality to improve muscle strength. Therefore, this study aimed to elucidate the relationship between PhA, an index of muscle mass and quality measured using BIA, and motor function during gait and standing in female patients with OAhip. Our hypothesis is that the decrease in PhA in the deformed lower limb will be more than the decrease in the muscle mass. Furthermore, lower limb PhA is related to walking and standing up, and patients with good lower limb PhA are considered to have good motor function.
Methods
Study design and measurement items
This was a cross-sectional, observational study conducted at a single institution. Joint function was evaluated using the Japanese Orthopedic Association (JOA) hip score [30], a widely used specific evaluation tool for Japanese patients with OAhip. Additionally, JOA criteria [31] were employed to evaluate the degree of deformity in both hips. Measurements of physical and motor functions, including PhA, muscle mass, TUG, ground reaction force/weight when standing up (F/w), rate of force development/weight (RFD8.75/w), and load ratio between the osteoarthritic (OA) and contralateral sides, were evaluated. Each test was conducted randomly, with breaks between each test as needed to prevent fatigue. The researchers in this study were two physical therapists with more than 9 years of clinical experience. Each measurement was performed in a standardized manner.
Participants
All measurements were made from August 2021 to March 2023. Data were collected on the day before surgery for female patients with OAhip scheduled for unilateral total hip arthroplasty. During the study period, data were obtained from 87 participants (Fig. 1). All participants were able to walk independently during the measurements. PhA and muscle mass in the lower limbs were measured using multi-frequency bioelectrical impedance; however, none of the participants had a pacemaker inserted. In this study, to exclude effects other than those on the deformed lower limb, we established the following exclusion criteria: (1) patients who had undergone total hip arthroplasty on the contralateral hip (n = 3); (2) evaluation of the degree of hip deformity using the X-ray images and the JOA criteria for patients with contralateral hip joints in advanced or end OA stages (n = 20); and (3) patients who experienced pain during loading in other joints (n = 3). Based on these exclusion criteria, 26 patients were excluded, and finally, the study comprised 61 participants. Of these, 60 participants were included in the analysis; one participant was excluded because of missing JOA hip score (n = 1).
Fig. 1.
During the measurement period, 93 participants were measured. Exclusion criteria were established, and 60 participants were finally analyzed. All participants were female
PhA and muscle mass measurements
Measurements were taken in the afternoon on the day before surgery. The room temperature at the time of measurement was constant because it was measured within the facility. Muscle mass and PhA were measured using a multi-frequency, 8-electrode body composition analyzer (MC-780 A-N, Tanita, Tokyo). The measurement device and method have been previously used in studies with similar populations [26, 27]. Before measurement, the participant’s skin and electrodes were wiped with alcohol, and measurements were performed under the same conditions. During the measurement process, participants were placed in a standing position with bare feet on the toe and heel electrodes, and the hand grip was held with the arm hanging several centimeters away from the body. This bioelectrical impedance device measures electrical resistance by applying a weak alternating current < 90 µA to the body. Measurement frequencies of 5, 50, and 250 kHz were used to measure the extracellular and intracellular water contents of the participant’s body directly. Because this body composition analyzer can determine individual impedances in each segment using the 8-electrode method, the bone and muscle mass was calculated separately for the upper and lower limbs and for the whole body. Muscle mass was calculated as the weight of the tissue (excluding fat and estimated bone mass) divided by body weight and normalized.
PhA, an indicator of muscle quality, was also measured using the same BIA method and equipment as muscle mass. A weak alternating current of ≤ 90 µA was applied to the body to measure reactance (Xc) and resistance (R). The measurement frequency was set to 50 kHz.
The PhA was calculated using the following formula: PhA (◦) = [arc tangent (Xc/R) × (180/π)]. The participant’s PhA was measured for separately in the affected and contralateral lower limbs, and absolute values were calculated for each lower limb.
TUG
The TUG test is a simple assessment method that reflects gait and balance functions. This evaluation method was developed by Podsiadlo and Richardson [32] and is used to evaluate trunk and pelvic sway related to walking in patients with OAhip [29]. TUG is an assessment method with high inter-examiner reproducibility [33]. The participants in this study were able to walk without a cane and capable of independent daily living. The chairs used in the TUG and chair-stand tests were the same, with no armrests and a seat height of 42 cm. At the start of the test, the participants were asked to sit on a chair. When given a signal to start the task, the participants were asked to stand up from the chair and walk around a pole 3 m away. The time required to sit down again was measured. The participants were instructed to walk as briskly as possible and perform the task to the best of their abilities. TUG measurements were performed for all participants while walking without using a cane. The task was performed twice, and the fastest task completion time was considered the representative value for each participant. The TUG test demonstrated good reliability [34] and a correlation coefficient of r = 0.81 with the Berg Balance Scale and r = 0.78 with the Barthel Index for daily activities [35].
F/w when standing up, RFD8.75/w, and lower limb load ratio on the OA and contralateral sides
The measurements were conducted using a motor function measurement device (Tanita, ZaRitz) with a sampling rate of 80 Hz and a unit of 0.01 kgf/s・kg− 1. For this task, the participant sat shallowly on a chair with a seat height of 42 cm in a position that made it easy to stand up, with their feet 10 cm apart so that they were on the floor reaction force sensor, with both arms crossed in front of their chest, their gaze facing forward, and they stood up with maximum effort thrice. The chairs used in the tests were similar to those used in the TUG evaluation. The chair rise test is an assessment method with high inter-examiner reproducibility [36]. F/w, RFD8.75/w (Fig. 2) and the lower limb load ratio were measured as ground reaction force coefficients obtained during task movements.
Fig. 2.
The graphs show F/w and RFD8.75/w as floor reaction force indices during standing up. F/w is the maximum floor reaction force divided by body weight, and RFD8.75/w is the increase in ground reaction force over a total of 87.5 milliseconds, including 37.5 milliseconds before and after 12.5 milliseconds when the maximum increase was recorded, was converted to 1.0 s and divided by body weight. The figure was taken from a previous study [46] and partially modified
F/w (kgf•kg− 1) is calculated by dividing the maximum value of the ground reaction force by the body weight and reflects the maximum stepping force in the vertical direction when standing up from a chair [37]. Among the three trials, the F/w at the highest RFD8.75/w (kgf/s•kg− 1), indicating the rate of change when the ground reaction force exhibits maximum increase, was selected.
RFD8.75/w (kgf/s•kg− 1) is an index showing the rate of change when the ground reaction force exhibits the maximum increase [37]. The increase in ground reaction force over a total of 87.5 milliseconds, including 37.5 milliseconds before and after 12.5 milliseconds when the maximum increase was recorded, was converted to 1.0 s and divided by body weight. The maximum value was used after three trials.
The lower limb load during standing up was measured for each of the three attempts, and the lower limb load ratio at which the highest RFD8.75/w measurement was adopted. The lower limb load ratios were measured on the OA and contralateral sides.
Statistical analyses
The distribution of all data was examined using the Kolmogorov–Smirnov test for normality. The data were expressed as mean ± standard deviation for normally distributed data and median value (interquartile range) for non-normally distributed data. To examine the characteristics of the lower limb on the OA side, a paired t-test was used to assess the differences in PhA, muscle mass, and load ratio of the lower limbs during standing. The relationship between PhA and muscle mass of the deformed lower limb and motor function was investigated using a partial correlation coefficient with age as a control variable, as PhA is influenced by age. Multiple regression analysis was used to examine whether PhA or muscle mass was independently associated with TUG and ground reaction force index during standing. The dependent variables were TUG, F/w, and RFD8.75/w, and the independent variables were age, lower limb PhA on the OA side, and muscle mass/w. The Kolmogorov-Smirnov test was employed to determine the distribution of variables. No dummy variables were included in the multiple regression analysis. The significance level for all studies was set at p < 0.05.
Results
Basic information of the participants
Table 1 presents the basic information of the participants. The study included 60 female patients with OAhip (mean age: 65.6 ± 7.6 years; height: 154.2 ± 6.0 cm; weight: 56.8 ± 10.5 kg). All participants chose surgery as treatment for their OAhip. All participants were able to walk on their own and were able to carry out independent daily activities. To the extent possible, exclusion criteria were set to exclude influences other than those on the hip joint to be operated on. The degree of deformity of the participant’s hip joint was determined using the JOA criteria, and most of the participants were in the advanced (n = 18) and end stages (n = 41) of OAhip. The contralateral hip was categorized as normal (n = 18), in the pre-arthritic stage (n = 12), and in the early OA stage (n = 30). The JOA hip score was 44.8 ± 10.2 points on the OA side and 90 (85–90) points on the contralateral side, and lower limb function on the deformed side was significantly decreased.
Table 1.
Basic information of the participants
| Variable | Value | |
|---|---|---|
| Age (years) | 65.6 ± 7.6 | |
| Height (cm) | 154.2 ± 6.0 | |
| Weight (kg) | 56.8 ± 10.5 | |
| TUG (sec) | 7.3 (4.7–8.7) | |
| F/w (kgf•kg− 1) | 1.2 ± 0.0 | |
| RFD8.75/w (kgf/s•kg− 1) | 8.8 ± 2.0 | |
| OA side | Contralateral side | |
| JOA Hip score (point) | 44.8 ± 10.2 | 90 (85–90) |
| JOA radiographic stage | ||
| Normal | 0 | 18 |
| Pre-arthritic stage | 0 | 12 |
| Early stage | 1 | 30 |
| Advanced stage | 18 | 0 |
| End-stage | 41 | 0 |
| Lower limb load when standing up (%) | 42.7 ± 6.6 | 57.2 ± 6.6 |
| Muscle mass (kg) | 6.1 ± 0.8 | 6.5 ± 0.8 |
| Muscle mass/w (%) | 10.9 ± 1.5 | 11.6 ± 1.6 |
| Phase Angle (°) | 4.0 ± 0.6 | 4.5 ± 0.6 |
| PhA | Muscle mass | |
| OA side / contralateral side (%) | 89.8 ± 8.3 | 94.1 ± 4.1 |
Normally distributed data: mean ± standard deviation; Non-normally distributed data: Median value (interquartile range)
TUG, Timed Up and Go; F/w, Ground reaction force/weight; RFD8.75/w, rate of force development/weight; OA, osteoarthritic; JOA hip score, Japanese Orthopaedic Association Hip score; Muscle mass/w, Muscle mass/ weight.
Characteristics of the lower limb on the OA side
In this study, we examined the differences between the OA and contralateral sides in terms of the load during standing, muscle mass/body weight ratio, PhA, muscle mass, and PhA ratio of the contralateral leg (Table 2). The load ratio during standing up was 42.7 ± 6.6% on the OA side and 57.2 ± 6.6% on the contralateral side. The muscle mass/body weight ratio was 10.9 ± 1.5% on the OA side and 11.6 ± 1.6% on the contralateral side. PhA was 4.0 ± 0.6° on the OA side and 4.5 ± 0.6° on the contralateral side. The value of the lower limb on the OA side was significantly lower in all the analyses. Moreover, the ratio of PhA and muscle mass in the contralateral leg was 89.8 ± 8.3% for PhA and 94.1 ± 4.1% for muscle mass, and the rate of decrease in PhA was significantly greater than the rate of decrease in muscle mass.
Table 2.
Difference between OA and contralateral sides
| Variable | OA side | Contralateral side |
Difference | p-value |
|---|---|---|---|---|
| Lower limb load when standing up (%) | 42.7 ± 6.6 | 57.2 ± 6.6 | OA side < contralateral side | < 0.001* |
| Muscle mass/weight (%) | 10.9 ± 1.5 | 11.6 ± 1.6 | OA side < contralateral side | < 0.001* |
| PhA (°) | 4.0 ± 0.6 | 4.5 ± 0.6 | OA side < contralateral side | < 0.001* |
| PhA | Muscle mass | |||
|
OA side muscle / contralateral side PhA and mass (%) |
89.8 ± 8.3 | 94.1 ± 4.1 | PhA < Mass | < 0.001* |
All differences were tested using paired t-tests
OA, osteoarthritic; PhA, Phase Angle
* indicates p < 0.05
Relationship between muscle mass, PhA, and motor function in the lower limb on the OA side
Since PhA is influenced by age, we used a partial correlation coefficient with age as a control variable to examine the relationship between OA lower limb muscle mass/body weight ratio, PhA, and motor function. No items showed a significant correlation with the lower limb muscle mass/body weight ratio; however, PhA exhibited significant correlations with all items (Table 3). Regarding the relationship between PhA of the OA side and each motor function, TUG had a weak correlation, whereas F/w, RFD8.75/w, and lower limb load of the OA side when standing up had a moderate correlation. These relationships suggested that the group with better PhA had better motor function and was putting more weight on the OA side.
Table 3.
Relationship between PhA, muscle mass/weight, and motor function
| TUG | F/w | RFD8.75/w | Lower limb load of OA side when standing up | ||
|---|---|---|---|---|---|
| OA side PhA | r | -0.265 | 0.509 | 0.439 | 0.431 |
| p | 0.042* | < 0.01* | < 0.01* | < 0.01* | |
| OA side muscle mass/weight | r | -0.244 | 0.194 | 0.096 | -0.064 |
| p | 0.062 | 0.140 | 0.467 | 0.627 |
Partial correlation coefficients with age as a control variable were used to examine the relationships between each item
TUG, Timed Up and Go; F/w, Ground reaction force/weight; RFD8.75/w, rate of force development/weight, OA, osteoarthritic; PhA, Phase Angle
* indicates p < 0.05
To examine whether PhA and muscle mass were independently related to motor function, a multiple regression analysis was performed using a stepwise method. No dummy variables were included. Partial correlation coefficients were observed, and no items with r > 0.9. The dependent variables were TUG, F/w, and RFD8.75/w, and the independent variables were age, lower limb PhA on the OA side, and muscle mass/w.
In the multiple regression analysis with TUG as the dependent variable, the probability level for the significance of the coefficients was p = 0.016, the standardized coefficient was − 0.310, and the unstandardized coefficient was − 0.861.
Regression equation: TUG = 11.302–0.861×PhA.
In the multiple regression analysis with F/w as the dependent variable, the probability level for the significance of the coefficients was p < 0.01, the standardized coefficient was 0.515, and the unstandardized coefficient was 0.068.
Regression equation: F/w = 0.947 + 0.068×PhA.
In the multiple regression analysis with RFD8.75/w as the dependent variable, the probability level for the significance of the coefficients was p < 0.01, the standardized coefficient was 0.458, and the unstandardized coefficient was 1.338.
Regression equation: RFD8.75/w = 3.422 + 1.338×PhA.
From the results of each multiple regression analysis, muscle mass was not selected in any analysis, whereas PhA was selected. Notably, the PhA of the OA lower limb is independently related to each motor function measured in this study.
We performed a post hoc analysis to evaluate statistical power (type II (β) error). We defined the effect size (d) as 0.5 and type I (α) error as 0.05 according to the paired t-test and partial correlation analysis, and the effect size (d) as 0.15 and type I (α) error as 0.05 in the multiple regression analysis.
Regarding the post hoc analysis, power values were 0.968 in the paired t-test, 0.979 in the partial correlation analysis, and 0.677 in the multiple regression analysis.
Discussion
Findings of this study
This study recruited female patients with OAhip and aimed to clarify the relationship between basic data on muscle mass and PhA in the OA lower limb and motor function. The results showed that in the patients with OAhip, the lower limb PhA and muscle mass of the OA side with highly advanced deformities decreased significantly compared with those of the contralateral lower limb, and the PhA of the OA lower limb decreased at a greater rate than the muscle mass in the contralateral lower limb. Furthermore, multiple regression analysis revealed that PhA was independently associated with gait function and ground reaction force index during standing. This study is novel as it is the first to examine the relationship between PhA and motor function in the lower limb on the OA side, specifically enrolling patients with OAhip and excluding the influence of sex. Although walking and standing up are crucial for maintaining an independent life, the results of this study suggest that, in future, it is important to emphasize evaluation and intervention that focus on the quality rather than quantity of muscle.
Basic information of the participants and differences between the OA side and the contralateral lower limb
Regarding the measured values, the muscle mass of the OA side lower limb was 10.9 ± 1.5%, and the PhA was 4.0 ± 0.6°, and the muscle mass and PhA of the OA side lower limb were significantly decreased compared to those on the contralateral lower limb. This result is consistent with previous research findings [21, 22]. Furthermore, in this study, the muscle mass and PhA of the OA lower limb were divided by the values of the contralateral lower limb to calculate the contralateral lower limb ratio. The rate of decrease in muscle mass was 94.1 ± 4.1%, whereas the decrease in PhA rate was 89.8 ± 8.3%, and it was revealed that the rate of decrease in PhA was greater on the OA side lower limb and that the decrease in the PhA, which is an index of muscle quality, was more than that in the muscle mass. Moreover, the load on the OA side leg during standing up was 42.7 ± 6.6%, which is lower than the load on the contralateral leg, indicating that the contralateral leg bears more load during daily movements. We believe that pain is a factor in the reduction in weight bearing on the OA-side lower limb. In this study, the participants were OAhip patients before surgery, and many of them had severely advanced hip deformities. Therefore, we believe that the deformity caused pain, which reduced the weight bearing on the deformed lower limb. This decrease in the load on the lower limb on the OA side may have contributed to a decreased activity of the muscles surrounding the hip joint, which is thought to have influenced the decrease in PhA. DeMik et al. [21] reported that the PhA of the deformed lower limb was 4.5 ± 1.2° and that of the contralateral lower limb was 4.8 ± 1.1° in 38 patients with OAhip (60.8 ± 11.7 years). Additionally, Pinheiro et al. [22] reported that the PhA of the deformed lower limb was 5.39 ± 1.14° and that of the contralateral lower limb was 5.94 ± 1.03° in 31 patients with OAhip (54.06 ± 6.10 years). The PhA measured on the OA side in this study was 4.0 ± 0.6°, which was lower than those in previous studies [22, 27]. We believe that the reason for this difference from previous studies is that PhA is influenced by sex and age. The mean age of the participants in this study was 65.6 ± 7.6 years old, and the ages of those in previous studies were 60.8 ± 11.7 years [21] and 54.06 ± 6.10 years [22], thus, the participants in this study were older than those in previous studies. Additionally, although all participants in this study were female, in a previous study [21], the number of females was 39.5% of the total, with approximately 60% of their cohort being male. Similarly, in another report, 87.1% of the participants were male [22]. Considering these relationships between sex and age, we conclude that the PhA values in this study were lower than those in previous studies. Furthermore, in a study of healthy older participants, the mean age of the participants was 71.47 ± 4.50 years, and the lower limb PhA was 4.25 ± 0.75° [26]. The PhA value decreases with age; however, the participants in this study were 65.6 ± 7.6 years old, which was approximately 6 years younger than those in previous studies. Nevertheless, the PhA of the lower limb on the OA side was 4.0 ± 0.6°, which was lower than those in previous studies. This comparison with previous studies suggests that PhA, indicating the health and muscle quality of cells in the lower limb on the OA side, may exhibit age-related changes at approximately 60 years of age.
However, PhA, which was used as an index in this study, is influenced by many factors such as the comorbidity history of the participants; the presence of renal, cardiac, or thyroid diseases; treatment with diuretics or hormone replacement therapy; frailty; nutritional status; the presence of edema and pain; and level of physical activity. These factors cannot be sufficiently excluded in this or the previous studies [22, 26, 27]; hence, caution should be taken when making simple comparisons.
Relationship between PhA, muscle mass, and motor function
In this study, we investigated the relationship between muscle mass and PhA in the OA lower limb measured using BIA and standing and walking functions, which are closely related to maintaining an independent lifestyle. Because PhA is influenced by age, we used a partial correlation coefficient with age as a control variable. However, PhA was correlated with all motor function-related items, whereas muscle mass was not related to any of the items. PhA on the OA side had a weak-to-moderate correlation with each motor function, and participants with good PhA had good motor function and were able to load the lower limb on the OA side. Additionally, multiple regression analysis was performed with each motor function-related item as the dependent variable and age, muscle mass/w, and PhA as the independent variables, revealing that PhA was independently related to each motor function-related item. We hypothesized that this result was due to the physiological characteristic that changes in muscle quality of the lower limbs precede aging. Age-related muscle degeneration occurs earlier in the lower limbs than in the upper limbs [38], and the loss of muscle function is associated with increased nuclear apoptosis [39], stress from participation [40], muscle fiber denervation [41], and reduced satellite cell content and/or regenerative potential [42]. Notably, in a comparison between the Robust and Pre-Frail groups, there was no difference in lower limb muscle mass; however, PhA of the lower limbs decreased in the Pre-Frail group, and items related to balance and walking function showed a significant correlation with PhA rather than muscle mass [26]. Furthermore, in this study, the rate of decrease in PhA was greater in the ratio of PhA and muscle mass of the contralateral leg than that of the OA side.
These results suggest that changes in muscle quality that occur with age precede changes in muscle mass. The decline in lower limb PhA is exacerbated by deformity, and the PhA of patients with OAhip with advanced deformity is thought to have been accelerated, and it was believed to be related to motor function rather than to the muscle mass.
Clinical application
This study revealed that patients with OAhip with advanced deformity have a greater decline in PhA than in muscle mass, which is also related to important motor functions, such as standing up and walking. Muscle mass and PhA can be easily measured using the BIA method employed in this study, and PhA is related to various motor functions; therefore, we believe that it can be an effective evaluation index. Moreover, PhA was more closely related to each motor function item than to muscle mass, indicating the importance of measures to address changes in quality to improve motor function. Regarding the external validity of this study, the participants were female OAhip patients before surgery, and several exclusion criteria were set to conduct an analysis that excluded the influence of anything other than the deformed hip joint as much as possible. Therefore, the study is considered valid for female OAhip patients with severe deformity. In the future, it will be necessary to increase the number of participants and add analyses in males and of the degree of deformity. In addition, the effectiveness of PhA was revealed, and nutritional aspects such as protein intake [43], aerobic exercise [44], and resistance training [45] are recommended to improve muscle quality. Therefore, a comprehensive intervention that considers nutrition and combines multiple exercise modalities is desirable rather than focusing only on muscles around the hip joint. The results of this study demonstrated that the load on the OA leg during standing up was small, predicting that resistance training and aerobic exercise in the weight bearing position would be challenging. A decrease in the PhA may lead to reduced muscle activity, promoting a decline in PhA. Therefore, considering the progression of the patient’s pain and deformity, exercises that mobilize the muscles of the entire lower limb, such as ergometers, pole walking, and pool exercises, may be effective.
Limitations
This study has some limitations. First, we measured muscle mass and PhA in patients with OAhip using BIA. BIA values are influenced by the amount of water in the body. However, because the participants were OAhip patients and the measurements were taken the day before surgery, it was difficult to regulate the fluid intake or output, or the food consumed. Additionally, it was difficult to obtain detailed background information such as the degree of edema or history of heart disease. Evaluation and comprehension of this information may affect the results measured by the BIA method; hence, this should be taken into consideration in future research. Second, multiple exclusion criteria were established to exclude effects other than hip joint deformation. However, the hip joint often exhibits bilateral deformity, and the analysis included the pre-arthritic and early stages of deformity of the contralateral hip joint. In addition, the number of participants was small, and in the future, the number of participants should be increased to perform more powerful statistical analysis. Additionally, although the same chair was used to evaluate the orthostatic function and TUG in this study, it was not possible to customize the chair according to the individual height of the participant. Both the orthostatic function and TUG are actions of standing up from a chair, and the chair height may affect each action. Moreover, because the participants of this study were preoperative OAhip patients, the reproducibility of the measurement method could not be confirmed. Given these limitations, to obtain more detailed findings, future studies should enroll more participants; confirm the reproducibility of fluid intake, measurement time, chair height relative to height and measurement method; and analyze the effect on the contralateral hip joint. In addition, clear background information, such as a history of cardiac disease and the degree of edema that may be related to PhA, should be obtained and analyzed.
Conclusions
Lower limb PhA in female patients with OAhip decreased more than their lower limb muscle mass and was also associated with motor functions such as standing up and gait. Based on these findings, the BIA method can be used to evaluate PhA, which is related to motor function and is considered a useful evaluation tool for patients with OAhip in clinical settings. Furthermore, because PhA is often associated with motor functions necessary for independent daily life, evaluation and intervention modalities that consider muscle quality rather than muscle mass may be important in the future.
Acknowledgements
This study was supported in part by a grant from the France Bed Home Care Foundation.
Abbreviations
- OA
Osteoarthritic
- OAhip
Osteoarthritis of the hip
- PhA
Phase angle
- BIA
Bioelectrical impedance analysis
- TUG
Timed Up and Go test
- F/w
Ground reaction force/weight
- RFD8.75/w
Rate of force development/weight
- JOA
Japanese Orthopedic Association
Author contributions
DH: Conducting research and writing the paper NI: Research supervision, construction of research design DM: Recruiting people to be measured MY: Measurement aid TS: Measurement aid YH: Construction of research design HS: Construction of research design YD: Recruiting people to be measured NE: Research supervision, construction of research design IM: Research supervision, construction of research design HK: Research supervision.
Funding
This research was supported in part by the France Bed Medical Home Care Research Subsidy Public Interest Incorporated Foundation.
Data availability
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
Declarations
Ethics approval and consent to participate
This study was conducted in accordance with the principles of the Declaration of Helsinki and was approved by the Ethics Committee of Niigata Bandai Hospital (approval number: 2303-115). All the participants provided written informed consent to participate in this study.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Footnotes
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
References
- 1.Kim C, Linsenmeyer KD, Vlad SC, Guermazi A, Clancy MM, Niu J, et al. Prevalence of radiographic and symptomatic hip osteoarthritis in an urban United States community: the Framingham osteoarthritis study. Arthritis Rheumatol. 2014;66:3013–7. 10.1002/art.38795 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Murphy LB, Helmick CG, Schwartz TA, Renner JB, Tudor G, Koch GG, et al. One in four people may develop symptomatic hip osteoarthritis in his or her lifetime. Osteoarthritis Cartilage. 2010;18:1372–9. 10.1016/j.joca.2010.08.005 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Dibonaventura MD, Gupta S, McDonald M, Sadosky A. Evaluating the health and economic impact of osteoarthritis pain in the workforce: results from the National Health and Wellness Survey. BMC Musculoskelet Disord. 2011;12:83. 10.1186/1471-2474-12-83 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Eitzen I, Fernandes L, Kallerud H, Nordsletten L, Knarr B, Risberg MA. Gait characteristics, symptoms, and function in persons with hip osteoarthritis: a longitudinal study with 6 to 7 years of follow-up. J Orthop Sports Phys Ther. 2015;45:539–49. 10.2519/jospt.2015.5441 [DOI] [PubMed] [Google Scholar]
- 5.Kubota M, Shimada S, Kobayashi S, Sasaki S, Kitade I, Matsumura M, et al. Quantitative gait analysis of patients with bilateral hip osteoarthritis excluding the influence of walking speed. J Orthop Sci. 2007;12:451–7. 10.1007/s00776-007-1160-z [DOI] [PubMed] [Google Scholar]
- 6.Morley JE, Vellas B, van Kan GA, Anker SD, Bauer JM, Bernabei R, et al. Frailty consensus: a call to action. J Am Med Dir Assoc. 2013;14:392–7. 10.1016/j.jamda.2013.03.022 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Delbaere K, Crombez G, Vanderstraeten G, Willems T, Cambier D. Fear-related avoidance of activities, falls and physical frailty. A prospective community-based cohort study. Age Ageing. 2004;33:368–73. 10.1093/ageing/afh106 [DOI] [PubMed] [Google Scholar]
- 8.Oliveria SA, Felson DT, Reed JI, Cirillo PA, Walker AM. Incidence of symptomatic hand, hip, and knee osteoarthritis among patients in a health maintenance organization. Arthritis Rheum. 1995;38:1134–41. 10.1002/art.1780380817 [DOI] [PubMed] [Google Scholar]
- 9.Grimaldi A, Richardson C, Stanton W, Durbridge G, Donnelly W, Hides J. The association between degenerative hip joint pathology and size of the gluteus medius, gluteus minimus and piriformis muscles. Man Ther. 2009;14:605–10. 10.1016/j.math.2009.07.004 [DOI] [PubMed] [Google Scholar]
- 10.Zacharias A, Pizzari T, English DJ, Kapakoulakis T, Green RA. Hip abductor muscle volume in hip osteoarthritis and matched controls. Osteoarthritis Cartilage. 2016;24:1727–35. 10.1016/j.joca.2016.05.002 [DOI] [PubMed] [Google Scholar]
- 11.Homma D, Minato I, Imai N, Miyasaka D, Sakai Y, Horigome Y, et al. Appropriate sites for the measurement of the cross-sectional area of the gluteus maximus and the gluteus medius muscles in patients with hip osteoarthritis. Surg Radiol Anat. 2021;43:45–52. 10.1007/s00276-020-02535-2 [DOI] [PubMed] [Google Scholar]
- 12.Homma D, Minato I, Imai N, Miyasaka D, Sakai Y, Horigome Y, et al. Relationship between the hip abductor muscles and abduction strength in patients with hip osteoarthritis. Acta Med Okayama. 2023;77:461–9. [DOI] [PubMed] [Google Scholar]
- 13.Zacharias A, Pizzari T, Semciw AI, English DJ, Kapakoulakis T, Green RA. Comparison of gluteus medius and minimus activity during gait in people with hip osteoarthritis and matched controls. Scand J Med Sci Sports. 2019;29:696–705. 10.1111/sms.13379 [DOI] [PubMed] [Google Scholar]
- 14.Akamatsu Y, Kusakabe T, Arai H, Yamamoto Y, Nakao K, Ikeue K, et al. Phase angle from bioelectrical impedance analysis is a useful indicator of muscle quality. J Cachexia Sarcopenia Muscle. 2022;13:180–9. 10.1002/jcsm.12860 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Beberashvili I, Azar A, Sinuani I, Kadoshi H, Shapiro G, Feldman L, et al. Longitudinal changes in bioimpedance phase angle reflect inverse changes in serum IL-6 levels in maintenance hemodialysis patients. Nutrition. 2014;30:297–304. 10.1016/j.nut.2013.08.017 [DOI] [PubMed] [Google Scholar]
- 16.Rimsevicius L, Gincaite A, Vicka V, Sukackiene D, Pavinic J, Miglinas M. Malnutrition assessment in hemodialysis patients: role of bioelectrical impedance analysis phase angle. J Ren Nutr. 2016;26:391–5. 10.1053/j.jrn.2016.05.004 [DOI] [PubMed] [Google Scholar]
- 17.Yamada Y, Buehring B, Krueger D, Anderson RM, Schoeller DA, Binkley N. Electrical properties assessed by bioelectrical impedance spectroscopy as biomarkers of age-related loss of skeletal muscle quantity and quality. J Gerontol Biol Sci Med Sci. 2017;72:1180–6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Basile C, Della-Morte D, Cacciatore F, Gargiulo G, Galizia G, Roselli M, et al. Phase angle as bioelectrical marker to identify elderly patients at risk of Sarcopenia. Exp Gerontol. 2014;58:43–6. 10.1016/j.exger.2014.07.009 [DOI] [PubMed] [Google Scholar]
- 19.Yamada M, Kimura Y, Ishiyama D, Nishio N, Otobe Y, Tanaka T, et al. Phase angle is a useful indicator for muscle function in older adults. J Nutr Health Aging. 2019;23:251–5. 10.1007/s12603-018-1151-0 [DOI] [PubMed] [Google Scholar]
- 20.Ukai T, Watanabe M. Do metal implants for total hip arthroplasty affect bioelectrical impedance analysis? A retrospective study. BMC Musculoskelet Disord. 2023;24:763. 10.1186/s12891-023-06893-x [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.DeMik DE, Marinier MC, Gulbrandsen TR, Glass NA, Elkins JM. Does isolated unilateral hip or knee osteoarthritis lead to adverse changes in extremity composition? Iowa Orthop J. 2022;42:163–7. [PMC free article] [PubMed] [Google Scholar]
- 22.Pinheiro JS, Carlos FR, Caseiro-Filho LC, Ferraz Picado CH, Garcia FL, de Oliveira Guirro EC, et al. Segmental bioelectrical impedance analysis can detect differences between the affected and non-affected limbs in individuals with hip osteoarthritis. BMC Musculoskelet Disord. 2023;24:420. 10.1186/s12891-023-06541-4 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Wada O, Yamada M, Kamitani T, Mizuno K, Kurita N. The associations of phase angle with the structural severity and quadriceps strength among patients with hip osteoarthritis: the SPSS-OK study. Clin Rheumatol. 2021;40:1539–46. 10.1007/s10067-020-05419-3 [DOI] [PubMed] [Google Scholar]
- 24.Iidaka T, Muraki S, Oka H, Horii C, Kawaguchi H, Nakamura K, et al. Incidence rate and risk factors for radiographic hip osteoarthritis in Japanese men and women: a 10-year follow-up of the ROAD study. Osteoarthritis Cartilage. 2020;28:182–8. 10.1016/j.joca.2019.09.006 [DOI] [PubMed] [Google Scholar]
- 25.Barbosa-Silva MCG, Barros AJD, Wang J, Heymsfield SB, Pierson RN. Bioelectrical impedance analysis: population reference values for phase angle by age and sex. Am J Clin Nutr. 2005;82:49–52. 10.1093/ajcn/82.1.49 [DOI] [PubMed] [Google Scholar]
- 26.Homma D, Minato I, Imai N, Miyasaka D, Sakai Y, Horigome Y, et al. Analysis of phase angle and balance and gait functions in pre-frail individuals: a cross-sectional observational study. Acta Med Okayama. 2023;77:21–7. [DOI] [PubMed] [Google Scholar]
- 27.Homma D, Minato I, Imai N, Miyasaka D, Horigome Y, Suzuki H, et al. Associations of lower-limb phase angle with locomotion and motor function in Japanese community-dwelling older adults. Geriatr (Basel). 2023;8:121. 10.3390/geriatrics8060121 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Eitzen I, Fernandes L, Nordsletten L, Snyder-Mackler L, Risberg MA. Weight-bearing asymmetries during Sit-To-Stand in patients with mild-to-moderate hip osteoarthritis. Gait Posture. 2014;39:683–8. 10.1016/j.gaitpost.2013.09.010 [DOI] [PubMed] [Google Scholar]
- 29.Homma D, Minato I, Imai N, Miyasaka D, Sakai Y, Horigome Y, et al. Three-dimensional evaluation of abnormal gait in patients with hip osteoarthritis. Acta Med Okayama. 2020;74:391–9. [DOI] [PubMed] [Google Scholar]
- 30.Imura S. The Japanese Orthopaedic Association: evaluation chart of hip joint functions. J Jpn Orthop Assoc. 1995;69:864–7. [Google Scholar]
- 31.Ueno R. Staging of osteoarthritis of the hip joint according to the roentgenographic findings. J Jpn Orthop Assoc. 1971;45:826–8. [Google Scholar]
- 32.Podsiadlo D, Richardson S. The timed UP & go: a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc. 1991;39:142–8. 10.1111/j.1532-5415.1991.tb01616.x [DOI] [PubMed] [Google Scholar]
- 33.Wright AA, Cook CE, Baxter GD, Dockerty JD, Abbott JH. A comparison of 3 methodological approaches to defining major clinically important improvement of 4 performance measures in patients with hip osteoarthritis. J Orthop Sports Phys Ther. 2011;41:319–27. 10.2519/jospt.2011.3515 [DOI] [PubMed] [Google Scholar]
- 34.Bischoff HA, Stähelin HB, Monsch AU, Iversen MD, Weyh A, von Dechend M, et al. Identifying a cut-off point for normal mobility: a comparison of the timed ‘up and go’ test in community-dwelling and institutionalised elderly women. Age Ageing. 2003;32:315–20. 10.1093/ageing/32.3.315 [DOI] [PubMed] [Google Scholar]
- 35.Rikli RE, Jones CJ. Development and validation of criterion-referenced clinically relevant fitness standards for maintaining physical independence in later years. Gerontologist. 2013;53:255–67. 10.1093/geront/gns071 [DOI] [PubMed] [Google Scholar]
- 36.Gill S, McBurney H. Reliability of performance-based measures in people awaiting joint replacement surgery of the hip or knee. Physiother Res Int. 2008;13:141–52. 10.1002/pri.411 [DOI] [PubMed] [Google Scholar]
- 37.Kera T, Kawai H, Takahashi J, Hirano H, Watanabe Y, Fujiwara Y, et al. Association between ground reaction force in sit-to-stand motion and falls in community-dwelling older Japanese individuals. Arch Gerontol Geriatr. 2020;91:104221. 10.1016/j.archger.2020.104221 [DOI] [PubMed] [Google Scholar]
- 38.Hughes VA, Frontera WR, Wood M, Evans WJ, Dallal GE, Roubenoff R, et al. Longitudinal muscle strength changes in older adults: influence of muscle mass, physical activity, and health. J Gerontol Biol Sci Med Sci. 2001;56:B209–17. 10.1093/gerona/56.5.B209 [DOI] [PubMed] [Google Scholar]
- 39.Marzetti E, Calvani R, Bernabei R, Leeuwenburgh C. Apoptosis in skeletal myocytes: a potential target for interventions against Sarcopenia and physical frailty—A mini-review. Gerontology. 2012;58:99–106. 10.1159/000330064 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40.Johnston APW, De Lisio M, Parise G. Resistance training, Sarcopenia, and the mitochondrial theory of aging. Appl Physiol Nutr Metab. 2008;33:191–9. 10.1139/H07-141 [DOI] [PubMed] [Google Scholar]
- 41.Degens H, Alway SE. Control of muscle size during disuse, disease, and aging. Int J Sports Med. 2006;27:94–9. 10.1055/s-2005-837571 [DOI] [PubMed] [Google Scholar]
- 42.Buford TW, Anton SD, Judge AR, Marzetti E, Wohlgemuth SE, Carter CS, et al. Models of accelerated Sarcopenia: critical pieces for solving the puzzle of age-related muscle atrophy. Ageing Res Rev. 2010;9:369–83. 10.1016/j.arr.2010.04.004 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 43.Yamada M, Kimura Y, Ishiyama D, Nishio N, Otobe Y, Tanaka T, et al. Synergistic effect of bodyweight resistance exercise and protein supplementation on skeletal muscle in sarcopenic or dynapenic older adults. Geriatr Gerontol Int. 2019;19:429–37. 10.1111/ggi.13643 [DOI] [PubMed] [Google Scholar]
- 44.Ryan AS, Harduarsingh-Permaul AS. Effects of weight loss and exercise on trunk muscle composition in older women. Clin Interv Aging. 2014;9:395–402. 10.2147/CIA.S56662 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 45.Taaffe DR, Henwood TR, Nalls MA, Walker DG, Lang TF, Harris TB. Alterations in muscle attenuation following detraining and retraining in resistance-trained older adults. Gerontology. 2009;55:217–23. 10.1159/000182084 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 46.Tsuji T, Tsunoda K, Mitsuishi Y, Okura T. Ground reaction force in sit-to-stand movement reflects lower limb muscle strength and power in community-dwelling older adults. Int J Gerontol. 2015;9:111–8. 10.1016/j.ijge.2015.05.009 [DOI] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.


