Skip to main content
The Journal of Nutrition, Health & Aging logoLink to The Journal of Nutrition, Health & Aging
. 2022 May 21;26(6):590–597. doi: 10.1007/s12603-022-1803-y

Association between BIA-derived Phase Angle and Sarcopenia and Improvement in Activities of Daily Living and Dysphagia in Patients undergoing Post-Stroke Rehabilitation

T Bise 1, Yoshihiro Yoshimura 1, H Wakabayashi 2, F Nagano 1, Y Kido 1, S Shimazu 1, A Shiraishi 1, A Matsumoto 1
PMCID: PMC12878607  PMID: 35718868

Abstract

Objectives

To investigate the predictive value of the BIA-derived phase angle with respect to the functional prognosis and baseline sarcopenia in patients undergoing post-stroke rehabilitation.

Design

Retrospective cohort study.

Setting and Participants

Overall, 577 Japanese patients admitted to a post-acute care hospital from 2016 to 2020 were recruited.

Measurements

Body composition analysis, which included BIA-derived phase angle and skeletal muscle mass, was performed using bioelectrical impedance analysis (BIA). Study outcomes included physical function assessed using the Functional Independence Measure (FIM-motor) and the level of dysphagia assessed using the Food Intake LEVEL Scale (FILS). Sarcopenia was defined as the loss of skeletal muscle mass and decreased muscle strength. Receiver operating characteristic curves were used to calculate the optimal cutoff value of BIA-derived phase angle to diagnose sarcopenia. Multivariate analyses were used to determine whether the BIA-derived phase angle at admission was associated with outcomes at discharge and baseline sarcopenia.

Results

After enrollment, 499 patients (mean age: 74.0 ± 13.1 years; 52.0% men) were examined. The median FIM-motor and FILS scores at admission were 47 (20–69) and 8 (7–10), respectively. Sarcopenia was observed in 43.2% of patients. After adjusting for potential confounders, BIA-derived phase angle was positively associated with FIM-motor scores at discharge (β = 0.134, P < 0.001), FIM-motor score gain (β = 2.504, P < 0.001), and FILS scores at discharge (β = 0.120, P = 0.039). BIA-derived phase angle was negatively associated with the sarcopenia diagnosis at baseline (odds ratio = −0.409, P < 0.001); its cutoff value was 4.76° (sensitivity 0.800, specificity 0.790, P < 0.001) for sarcopenia diagnosis in men and 4.11° (sensitivity 0.735, specificity 0.829, P < 0.001) in women.

Conclusion

BIA-derived phase angle was positively associated with the recovery of physical function and dysphagia level and negatively associated with baseline sarcopenia in patients undergoing post-stroke rehabilitation. The BIA-derived phase angle cutoff for sarcopenia diagnosis was 4.76° for men and 4.11° for women.

Key words: BIA-derived phase angle, sarcopenia, dysphagia, malnutrition, convalescent rehabilitation

Introduction

Malnutrition and sarcopenia are associated with poor outcomes in patients with stroke. The 12-month disability rate was 16.6 % for stroke survivors, ranging from 11.1 % for subarachnoid hemorrhage to 29.2 % for cerebral hemorrhage (1). Almost half of the patients with stroke tend to have malnutrition and sarcopenia (2, 3, 4), which are closely associated with poor rehabilitation outcomes (5, 6). Malnourished patients with stroke tend to have a higher mortality rate, longer duration of hospital stay, and greater healthcare costs than their counterparts (7, 8, 9). Malnutrition after stroke also increases disease severity and incidence of infection and dysphagia and hinders improvement in activities of daily living (ADL) (5). Thus, simple and clinically useful indicators of malnutrition and sarcopenia should be identified.

BIA-derived phase angle, a proxy measure for water distribution and body cell mass (10), has been gaining attention in clinical settings as a means to evaluate nutritional status. A higher BIA-derived phase angle suggests greater cellularity (e.g., more body cell mass relative to free fat mass) and cellular integrity and function (11). Evidence has been reported for BIA-derived phase angle and physical function, nutritional status, and sarcopenia in acute stroke, but it has not been well studied in the recovery phase (12, 13, 14). Biomarkers that may predict functional prognosis after stroke include C-reactive protein (15), amino acids, circulating albumin, and hemoglobin (16, 17). BIA-derived phase angle is proposed to be useful in assessing nutritional status and prognosis in various clinical settings (18). Additionally, a recent systematic review suggested an association between BIA-derived phase angle and sarcopenia; however, these findings were mainly based on community-dwelling older adults and not on patients undergoing rehabilitation. Additionally, a recent systematic review suggested an association between BIA-derived phase angle and sarcopenia (10); however, these findings were mainly based on community-dwelling older adults and not on patients undergoing rehabilitation.

To our knowledge, no study has reported an association of BIA-derived phase angle with sarcopenia, dysphagia, and functional recovery among patients undergoing post-stroke rehabilitation. Furthermore, cutoff values for BIA-derived phase angle regarding sarcopenia diagnosis have been reported in several patient populations (19, 20, 21) but not in patients undergoing convalescent rehabilitation. Therefore, we conducted a retrospective cohort study to investigate this association and the BIA-derived phase angle cutoff values for sarcopenia diagnosis in patients undergoing convalescent post-stroke rehabilitation.

Methods

Participants and setting

We conducted a retrospective cohort study at a post-acute care hospital with convalescent rehabilitation wards with 135 beds (22). The study was conducted between January 2016 and December 2020; it included all newly-admitted patients with stroke. Patients admitted were classified into three main categories: (1) stroke, (2) musculoskeletal disorders, and (3) hospital-related decompensation. All patients with stroke were transferred from stroke care units of other acute care hospitals. More than 90% of patients with musculoskeletal disorders and hospital-related decompensation were also transferred from other hospitals once they were clinically stable. Patients who refused to participate, had incomplete data, had altered consciousness, edema, or fluid imbalance, and those who had undergone pacemaker insertion were excluded from the study. The observation period was from the date of admission to the date of discharge.

The convalescent rehabilitation program was conducted daily, up to 3 h per day, and involved a multidisciplinary team, including medical doctors, nurses, rehabilitation therapists, dietitians, social workers, care workers, dental specialists, and pharmacists. It was tailored to each patient's need to maximize the recovery of ADL capacity and to facilitate timely discharge.

This study was approved by the Institutional Review Board of the study site (Approval No. 160-200814) and was conducted in accordance with the Declaration of Helsinki and ethical guidelines for medical and health research involving human subjects. Written informed consent could not be obtained because of the retrospective nature of this study, but participants were allowed to withdraw from the study at any time using an opt-out procedure.

Data collection

At admission, the following data were collected: age, sex, stroke type (cerebral infarction, cerebral hemorrhage, subarachnoid hemorrhage), hospitalization duration, C-reactive protein, nutritional status using the Geriatric Nutritional Risk Index (GNRI) (23), paralysis status using the Brunnstrom stage (BRS) (24), dysphagia or swallowing status using the Food Intake LEVEL Scale (FILS) (25), comorbidities using the Charlson Comorbidity Index (CCI) (26), and premorbid ADL status using the modified Rankin scale (mRS) (27).

Trained physiotherapists and occupational therapists assessed Functional Independence Measure (FIM) within 72 h of admission, along with ADL (FIM-motor) and the cognitive level (FIM-cognitive) scores (28). The handgrip strength (HG) of the non-dominant hand (or the non-paralyzed hand in case of hemiplegia) was measured thrice using a hand dynamometer (Smedley TTM, Tokyo, Japan), and the highest value of the three measurements was recorded (29).

Based on medical records, the total number of rehabilitation therapy units received during hospitalization (units per day, 1 unit = 20 min therapy, based on the national health insurance policy) was also calculated.

Body composition

Body composition analysis, which included BIA-derived phase angle and skeletal muscle mass, was performed by trained physical and occupational therapists using a BIA machine (InBody S10; InBody, Tokyo, Japan). It was conducted within 3 days of admission, if the patient was well-hydrated, on bed-rest 4 h after the last meal and 1 h before evaluation, and had no current fever, tremor, or diagnosis of any illness. Using this device, BIA measurements for all patients were performed in the supine position.

BIA-derived phase angle was calculated using the following equation: BIA-derived phase angle = arctangent (Xc/R) × (180/π), where R is the resistance of the right half of the body and Xc is the reactance measured at 50 kHz (14). The skeletal muscle mass index (SMI) was calculated by dividing the measured skeletal muscle mass by the squared height in meters.

Sarcopenia was diagnosed in case of low SMI (< 7.0 kg/m2 for men and < 5.7 kg/m2 for women) and low HG (< 28 kg for men and < 18 kg for women), based on the 2019 Asian Working Group for Sarcopenia criteria (30).

Outcomes

The primary outcome was the motor domain score of FIM at discharge. FIM includes 13 sub-items, with each item assessed on a 7-point ordinal scale ranging from the complete need of care to complete independence (28). The total FIM score can range from 18 to 126, with FIM-motor and FIM-cognitive subscores ranging from 13 to 91 and 5 to 35 points, respectively. The lower the score, the greater is the patient's need for care. The FIM-motor score gain from baseline was calculated by subtracting the FIM-motor score at admission from that at discharge.

Other outcomes included were the FILS score at discharge and sarcopenia diagnosis at admission. FILS is a 10-point observer-rating scale for assessment of dysphagia (25); it classifies dysphagia severity as follows: “no oral intake” (1–3 points), “oral intake and alternative nutrition” (4–6 points), and “oral intake alone” (7–10 points). FILS was assessed by trained nurses and speech-language-hearing therapists at admission and discharge. Additionally, the association between the BIA-derived phase angle level and sarcopenia at baseline was also assessed.

Sample size calculation

The sample size was calculated using data from our previous study (17); it showed that the FIM-motor scores were normally distributed with a standard deviation of 26.0. If the true difference in means between those with lower and higher BIA-derived phase angle is 17 points, a sample size of at least 107 participants per group is required to reject the null hypothesis with a power of 0.8 and an alpha of 0.05. Therefore, we collected data for more than one year to obtain at least 107 participants per group.

Statistical analysis

All analyses were performed using IBM SPSS version 21 (IBM, Armonk, NY, USA). Results are reported as mean (standard deviation; SD) for parametric data, median and 25th-75th percentiles (interquartile range [IQR]) for nonparametric data, and percentage (%) for categorical data. The median BIA-derived phase angle at admission was used to compare the two groups with high and low BIA-derived phase angle using the t-test and the chi-square test. Between-group comparisons were performed using the t-test, the MannWhitney U test, and the chi-square test.

Using the receiver operating characteristic (ROC) curve, cutoff values of BIA-derived phase angle were calculated for each sex for sarcopenia diagnosis. Groups with BIA-derived phase angle values below and above the cutoff were defined as the low and high BIA-derived phase angle groups, respectively.

Multivariate analyses were used to determine the association between BIA-derived phase angle at admission and the outcomes of interest. Multiple regression analysis was used for the outcomes of FIM-motor and FILS scores at discharge. Multivariate logistic regression analysis was used to analyze the rate of sarcopenia at admission. Covariates used for adjustment of potential confounders for outcomes included baseline values for each outcome (FIM-motor and FILS scores); they also included variables associated with each outcome in previous studies or those considered clinically relevant (31, 32, 33, 34, 35), i.e., age, sex, length of hospital stay, FIM-motor, FIM-cognitive and FILS scores at admission, stroke type, premorbid mRS, CCI, BRS of the lower extremities, C-reactive protein and GNRI. The multicollinearity was assessed using the Variance Inflation Factor (VIF): a VIF value of 1–3 implied the absence of multicollinearity. Statistical significance was set at P < 0.05.

Results

In total, 499 participants were enrolled in the study. Among the 577 patients with stroke newly admitted to the wards during the study, those transferred to other hospitals or wards during rehabilitation (n = 16), with missing data (n = 22), with altered consciousness (n = 35), and who had undergone pacemaker insertion (n = 5) were excluded from the analysis (Figure 1).

Figure 1.

Figure 1

Flowchart of participant screening, inclusion criteria, and follow-up

The baseline characteristics of the enrolled participants are summarized in Table 1. The mean age of the participants was 74.0 (13.1) years, and 48% were women. Most patients (63%) had a cerebral infarction stroke type. Sarcopenia was diagnosed in 43.2% of the patients, and median FIM-motor and FIM-cognitive scores were 47 (20, 69) and 22 (14, 28), respectively, suggesting physical dependence among many patients at baseline. The median FILS score at admission was 8 (7, 10).

Table 1.

Baseline characteristics of study participants and between-group comparison of patients with lower- and higher- BIA-derived phase angle

Total N=499 Female N=230 Male N=269
Lower PhA N=127 Higher PhA N=103 P Lower PhA N=112 Higher PhA N=157 P
Age, y, mean (SD) 74.0 (13.1) 74.9 (12.0) 68.5 (12.6) <0.001 75.8 (12.1) 64.4 (12.4) <0.001
Stroke type n (%)
Cerebral infarction 314 (63) 83 (65) 56 (55) <0.001 77 (69) 97 (62) 0.002
Cerebral hemorrhage 146 (29) 33 (25) 31 (31) <0.001 31 (28) 51 (32) <0.001
Subarachnoid hemorrhage 39 (8) 11 (9) 16 (14) <0.001 4 (3) 9 (6) <0.001
Length of stay, days, median [IQR] 91.0[53.0, 142.0] 90 [53, 146] 66 [39, 120] <0.001 119 [70, 150] 77 [47, 121] <0.001
GNRI, median [IQR] 96.8 [88.7, 105.3] 94 [86, 103] 101 [94, 108] <0.001 93 [85, 102] 104 [97, 112] <0.001
Premorbid mRS, median [IQR] 0 [0, 1] 0 [0, 2] 0 [0, 1] <0.001 1 [0, 2] 0 [0, 1] <0.001
Paralysis, n (%)
Right 209 (42) 92 (40) 40 (39) <0.001 53 (46) 63 (41) <0.001
Left 196 (39) 92 (40) 39 (38) <0.001 44 (39) 58 (38) <0.001
Both 21 (4) 7 (3) 1 (1) <0.001 11 (8) 5 (4) <0.001
BRS, median [IQR]
Upper limb 5 [3, 6] 5 [3, 6] 6 [4, 6] <0.001 4 [2, 6] 5 [4, 6] <0.001
Hand-finger 5 [3, 6] 5 [3, 6] 6 [4, 6] <0.001 4 [1, 6] 5 [4, 6] <0.001
Lower limb 5 [3, 6] 5 [3, 6] 6 [5, 6] <0.001 5 [2, 6] 6 [4, 6] <0.001
CCI, median [IQR] 3 [1, 4] 3 [1, 4] 2 [1, 3] <0.001 3 [1, 5] 2 [1, 3] <0.001
Muscle-related variables
HG, kg, median [IQR] 19.0 [11.0, 27.6] 14.0 [7.2, 18.9] 18.2 [14.4, 22.2] <0.001 19.7 [8.6, 24.7] 31.3 [24.0, 36.8] <0.001
SMI, kg/m2, median [IQR] 6.3 [5.2, 7.3] 5.4 [4.7, 6.2] 6.1 [5.5, 6.8] <0.001 6.2 [5.7, 6.9] 7.4 [7.0, 8.0] <0.001
Sarcopenia, n (%) 216 (43.2) 116 (51) 19 (19) 0.792 79 (70) 21 (13) <0.001
FIM, score, median [IQR]
Total 70 [36, 94] 70 [33, 92] 88 [58, 104] <0.001 45 [28, 72] 85 [59, 105] <0.001
Motor 47 [20, 69] 47 [17, 68] 65 [38, 79] <0.001 27 [14, 53] 59 [40, 76] <0.001
Cognitive 22 [14, 28] 22 [13, 28] 24 [18, 30] <0.001 15 [10, 22] 25 [17, 31] <0.001
FILS, median [IQR] 8 [7, 10] 8 [7, 10] 10 [7, 10] <0.001 7 [2, 9] 10 [7, 10] <0.001
C-reactive protein, median [IQR] 0.2 [0.1, 1.0] 0.3 [0.1, 1.5] 0.2 [0.1, 0.7] 0.005 0.4 [0.1, 1.2] 0.2 [0.1, 0.7] 0.004
PhA, median [IQR] 4.4 [3.7, 5.3] 4.0 [3.3, 4.7] 4.8 [4.3, 5.1] <0.001 4.1 [3.6, 4.4] 5.6 [5.1, 6.1] <0.001

Data expressed as mean (standard deviation), median [inter-quartile range], or n (%); BRS, Brunnstrom stage; CCI, Charlson's Comorbidity Index; FILS, Food Intake Level Scale; FIM, Functional Independence Measure; GNRI, geriatric nutritional risk index; HG, handgrip strength; MNA-SF, Mini Nutritional Assessment-Short Form; mRS, modified Rankin scale; PhA, BIA-derived phase angle; SMI, skeletal muscle mass index

The cutoff value of BIA-derived phase angle for sarcopenia diagnosis calculated by ROC analysis was 4.76° for men (sensitivity 0.800, specificity 0.790, P < 0.001) and 4.11° for women (sensitivity 0.735, specificity 0.829, P < 0.001) (Figure 2). Comparing baseline variables between the low and high BIA-derived phase angle groups using these cutoff values showed significant differences in all variables among men and in all variables except for sarcopenia in women (Table 1).

Figure 2.

Figure 2

ROC curves to identify the optimal phase angle cut-off for detecting sarcopenia in male (A) and female (B)

A. The optimal cut-off value is 4.76° in male (sensitivity 0.80, specificity 0.79, AUC 0.85, 95% confidence interval 0.79–0.89, p<0.001). B. The optimal cut-off value is 4.11° in female (sensitivity 0.74, specificity 0.83, AUC 0.85, 95% confidence interval 0.80–0.90, p<0.001).

Table 2 shows the results of the two-group comparison of outcomes. In men, the high BIA-derived phase angle group had higher FIM-motor scores at discharge (89 [80, 91] vs. 61 [36, 83], P < 0.001), higher FILS scores at discharge (10 [10, 10] vs. 9 [8, 10], P < 0.001), and lower rates of sarcopenia at admission (13% vs. 70%, P < 0.001). In women, the high BIA-derived phase angle group had higher FIM-motor scores at discharge (87 [79, 90] vs. 69 [34, 83], P < 0.001), higher FILS scores at discharge (10 [10, 10] vs. 9 [8, 10], P < 0.001), and lower rates of sarcopenia at admission (19% vs. 76%, P < 0.001).

Table 2.

Univariate analysis for study outcomes between patients with lower- and higher BIA-derived phase angle during hospitalization

Total N=499 Female N=230 Male N=269
Lower PhA N=127 Higher PhA N=103 P Lower PhA N=112 Higher PhA N=157 P
FIM-motor score at discharge, median [IQR] 82 [56, 89] 69 [34, 83] 87 [79, 90] <0.001 61 [36, 83] 89 [80, 91] <0.001
FILS score at discharge, median [IQR] 10 [9, 10] 9 [8, 10] 10 [10, 10] <0.001 9 [8, 10] 10 [10, 10] <0.001
Sarcopenia, n (%) 216 (43.2) 97 (76) 19 (19) <0.001 79 (70) 21 (13) <0.001

Data expressed as median [inter-quartile range] or n (%); FILS, food intake level scale mass index.; FIM, Functional Independence Measure; PhA, BIA-derived phase angle

Table 3 shows the results of multivariate linear regression analyses for FIM-motor scores at discharge, FIM-motor score gain, and FILS scores at discharge. There was no multicollinearity between variables. BIA-derived phase angle was independently and positively associated with FIM-motor scores at discharge (β = 0.134, P < 0.001), FIM-motor score gain (β = 2.504, P < 0.001), and FILS scores at discharge (β = 0.120, P = 0.039).

Table 3.

Multivariate linear regression analysis for improvement in activities of daily living and swallowing stage, including FIM-motor score at discharge and FILS score at discharge

FIM-motor score at discharge, FILS score at discharge
β B (95% CI) P β B (95% CI) P
Age −0.031 −0.058 (−0.180, −0.063) 0.347 −0.031 −0.004 (−0.016, 0.007) 0.459
Sex (male) −0.004 −0.179 (−2.916, 2.558) 0.898 −0.039 −0.146 (−0.410, 0.118) 0.279
Length of stay 0.171 0.088 (0.052, 0.124) <0.001 0.179 0.007 (0.004, 0.010) <0.001
FIM-motor at admission 0.320 0.311 (0.202, 0.420) <0.001 −0.027 −0.002 (−0.012, 0.009) 0.714
FIM-cognitive at admission 0.212 0.583 (0.372, 0.793) <0.001 0.128 0.026 (0.006, 0.047) 0.011
Cerebral infarction 0.057 2.923 (−2.238, 8.084) 0.266 0.083 0.320 (−0.178, 0.819) 0.207
Cerebral hemorrhage 0.102 5.521 (−0.070, 10.973) 0.047 0.095 0.391 (−0.136, 0.917) 0.145
Premorbid mRS −0.160 −3.147 (−4.290, −2.004) <0.001 −0.169 −0.251 (−0.361, −0.141) <0.001
CCI −0.015 −0.220 (−1.042, 0.603) 0.600 −0.067 −0.074 (−0.154, 0.005) 0.066
BRS (lower limb) 0.236 3.084 (2.051, 4.116) <0.001 0.130 0.129 (0.029, 0.229) 0.011
GNRI 0.064 0.125 (−0.006, 0.255) 0.061 0.123 0.018 (0.005, 0.031) 0.005
FILS at admission 0.134 1.139 (0.516, 1.762) <0.001 0.427 0.275 (0.215, 0.335) <0.001
C-reactive protein 0.031 0.341 (−0.248, 0.930) 0.256 −0.044 −0.037 (−0.094, 0.020) 0.202
PhA 0.133 2.472 (1.324, 3.683) <0.001 0.088 0.123 (0.009, 0.237) 0.034

BRS, Brunnstrom stage; CCI, Charlson's Comorbidity Index; FILS, Food Intake Level Scale; FIM, Functional Independence Measure; GNRI, geriatric nutritional risk index; mRS, modified Rankin scale; PhA, BIA-derived phase angle; SMI, skeletal muscle mass index

Table 4 shows the results of multivariate logistic regression analysis for sarcopenia at admission. There was no multicollinearity between variables. BIA-derived phase angle was independently and negatively associated with the sarcopenia diagnosis at baseline (odds ratio = −0.409, P < 0.001).

Table 4.

Multivariate logistic regression analysis for sarcopenia at admission

OR (95% CI) P
Age 1.068 (1.039–1.098) <0.001
Sex (male) 1.693(0.967–2.964) 0.065
FIM-motor at admission 1.002(0.981–1.022) 0.879
FIM-cognitive at admission 0.987(0.947–1.029) 0.537
Cerebral infarction 1.111(0.373–3.307) 0.850
Cerebral hemorrhage 1.096(0.343–3.505) 0.877
Premorbid mRS 1.336(1.063–1.679) 0.013
FILS at admission 0.903(0.797–1.022) 0.107
CCI 0.917(0.780–1.077) 0.289
BRS (lower limb) 0.818(0.661–1.012) 0.064
GNRI 0.960(0.934–0.986) 0.003
C-reactive protein 1.010(0.903–1.130) 0.860
PhA 0.408(0.286–0.583) <0.001

BRS, Brunnstrom stage; CCI, Charlson's Comorbidity Index; FILS, Food Intake Level Scale; FIM, Functional Independence Measure; GNRI, geriatric nutritional risk index; mRS, modified Rankin scale; PhA, BIA-derived phase angle; SMI, skeletal muscle mass index

Discussion

In this study, we examined the association of BIA-derived phase angle with functional outcomes and the sarcopenia diagnosis at baseline in patients undergoing convalescent post-stroke rehabilitation. Our results contribute three novel findings: BIA-derived phase angle was independently associated with (1) ADL recovery, (2) dysphagia recovery, and (3) sarcopenia at baseline.

The role of BIA-derived phase angle as a nutrition and health status indicator is well established, but its predictive value for clinical outcomes has only been investigated in selected patient categories (36, 37, 38, 39, 40, 41). To our knowledge, this is the first study to evaluate the prognostic value of BIA-derived phase angle for functional recovery in patients undergoing convalescent post-stroke rehabilitation. This association could be because a higher BIA-derived phase angle may reflect higher cellularity and cellular integrity and function, i.e., better nutritional status and body function. Therefore, BIA-derived phase angle may be a practical option for the clinical assessment of ADL recovery during post-stroke rehabilitation.

We believe it could be because approximately half of the patients with stroke are usually diagnosed with malnutrition and sarcopenia, and > 60% of them have dysphagia (3, 4). In our study, 44.8% of the participants were sarcopenic at baseline. Dysphagia is closely associated with malnutrition and sarcopenia (3, 42, 43). Therefore, the observed improvements in dysphagia among individuals with higher BIA-derived phase angle levels were related to good nutritional status and muscle mass maintenance. Further research is needed to elucidate the mechanisms underlying this association.

This finding is consistent with the results of a recent systematic review that showed a decreased BIA-derived phase angle in sarcopenic community-dwelling older adults (10). Greater values of BIA-derived phase angle indicate high cellularity, i.e., a low ratio of extracellular to intracellular fluid volume and high integrity of the cell membrane (11). Furthermore, BIA-derived phase angle is well associated with nutritional status (11), muscle mass, and strength (10), as well as with adverse clinical outcomes including falls (44), incident disability (21), frailty (19), and mortality (11). Our results were similar for patients undergoing post-stroke rehabilitation. Sarcopenia is associated with poor rehabilitation outcomes (31); thus, the clinical relevance of BIA-derived phase angle should be emphasized in this context.

BIA-derived phase angle is a proxy measure of cell integrity and water distribution and is expressed in degrees (°). In a pure cell membrane mass, BIA-derived phase angle is 90°; it is 0° in pure electrolyte water. In healthy subjects, the BIA-derived phase angle typically ranges from 8° to 15° (20). However, in clinical practice, BIA-derived phase angle values are relatively low, varying from 3.6° in community-dwelling older adults to 5.1° in patients with cirrhosis (20). A recently published study showed that a BIA-derived phase angle cutoff value of 4.0° was associated with readmissions, falls during hospitalization, and 9-month mortality among hospitalized patients (36). Further, our findings provided a cutoff value of BIA-derived phase angle for sarcopenia diagnosis in target patients. The value was 4.76° for men and 4.11° for women. Previous studies reported BIA-derived phase angle cutoff values of 4.05° for men and 3.55° for women among community-dwelling older adults (19) and 4.46° for patients with a kidney transplant (21). In the future, high-quality studies in diverse populations are needed to determine cutoff values of BIA-derived phase angle for sarcopenia diagnosis considering specific patient groups. The use of simple, practical, and reliable clinical markers such as BIA-derived phase angle to predict functional outcomes and sarcopenia would be useful in clinical practice.

Frequent and individualized nutritional support is associated with improved nutritional status, physical function, and dysphagia after stroke (45). Our findings suggest that there is an urgent need to identify sarcopenia at an early stage (upon admission) and initiate whole-body resistance exercises such as chair-stand exercises in order to promote improvement in sarcopenia and physical function in hospitalized patients undergoing rehabilitation (46). suggesting that deprescribing and modifying polypharmacy in patients with sarcopenia may promote improvement in nutritional status (47).

To our knowledge, no studies have reported the association between BIA-derived phase angle and sarcopenia, dysphagia, and functional recovery in patients undergoing convalescent rehabilitation after stroke. Furthermore, cut-off values for BIA-derived phase angle with respect to sarcopenia diagnosis have not been reported in this setting. The use of simple, practical, and reliable clinical markers such as BIA-derived phase angle to predict functional outcomes and sarcopenia would be useful in clinical practice. Therefore, it is necessary to measure the BIA-derived phase angle from the time of admission, provide more intensive rehabilitation to patients with low values, and strive for functional improvement and prevention/improvement of sarcopenia.

This study had some limitations. First, this was a singlecenter study, which limits its generalizability. Second, since the study was conducted on Japanese only, there are some limitations to generalization. Third, owing to the retrospective nature of this study, we were unable to fully adjust for the effects of confounding factors on outcomes, including changes in the content and quality of nutrition support and rehabilitation therapy during the study. Despite these limitations of the study, the strengths of this study are the large sample size and the fact that we were able to show the reference values for BIA-derived phase angle for men and women. Future multicenter prospective studies in diverse rehabilitation hospitals are needed to examine the relationship between BIA-derived phase angle and functional prognosis, dysphagia, and sarcopenia, not only in stroke patients but also in patients with hip fractures and other conditions.

Clinical implications

As a simple, practical, and reliable clinical marker, BIA-derived phase angle may be useful in clinical practice in that it can provide a good prediction of functional prognosis and sarcopenia. Measuring the BIA-derived phase angle on admission would allow patients with low scores to receive more intensive combined exercise, nutrition, and drug therapy to improve function and prevent or improve sarcopenia.

Conclusion

BIA-derived phase angle was positively associated with the recovery of ADL and dysphagia and negatively associated with baseline sarcopenia in patients with post-stroke rehabilitation. The BIA-derived phase angle cutoff for sarcopenia diagnosis was 4.76° in men and 4.11° in women.

Acknowledgments

This research did not receive any funding from agencies in the public, commercial or not-for-profit sectors.

Conflict of interest

The authors declare no conflict of interest.

References

  • 1.Tu WJ, Chao BH, Ma L, et al. Case-fatality, disability and recurrence rates after first-ever stroke: A study from bigdata observatory platform for stroke of China. Brain Res Bull. 2021;175:130–135. doi: 10.1016/j.brainresbull.2021.07.020. 10.1016/j.brainresbull.2021.07.020 PubMed PMID: 34329730. [DOI] [PubMed] [Google Scholar]
  • 2.Lieber AC, Hong E, Putrino D, Nistal DA, Pan JS, Kellner CP. Nutrition, energy expenditure, dysphagia, and self-efficacy in stroke rehabilitation: A review of the literature. Brain Sci. 2018;8(12) doi: 10.3390/brainsci8120218. 10.3390/brainsci8120218 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Yoshimura Y, Wakabayashi H, Bise T, Tanoue M. Prevalence of sarcopenia and its association with activities of daily living and dysphagia in convalescent rehabilitation ward inpatients. Clin Nutr. 2018;37(6):2022–2028. doi: 10.1016/j.clnu.2017.09.009. 10.1016/j.clnu.2017.09.009 PubMed PMID: 28987469. [DOI] [PubMed] [Google Scholar]
  • 4.Shiraishi A, Yoshimura Y, Wakabayashi H, Tsuji Y. Prevalence of stroke-related sarcopenia and its association with poor oral status in post-acute stroke patients: Implications for oral sarcopenia. Clin Nutr. 2018;37(1):204–207. doi: 10.1016/j.clnu.2016.12.002. 10.1016/j.clnu.2016.12.002 PubMed PMID: 28017450. [DOI] [PubMed] [Google Scholar]
  • 5.Marshall S, Bauer J, Isenring E. The consequences of malnutrition following discharge from rehabilitation to the community: A systematic review of current evidence in older adults. J Hum Nutr Diet. 2014;27(2):133–141. doi: 10.1111/jhn.12167. 10.1111/jhn.12167 PubMed PMID: 24289811. [DOI] [PubMed] [Google Scholar]
  • 6.Morandi A, Onder G, Fodri L, Sanniti A, Schnelle J, Simmons S, Landi F, Gentile S, Trabucchi M, Bellelli G. The Association Between the Probability of Sarcopenia and Functional Outcomes in Older Patients Undergoing In-Hospital Rehabilitation. J Am Med Dir Assoc. 2015;16(11):951–956. doi: 10.1016/j.jamda.2015.05.010. 10.1016/j.jamda.2015.05.010 PubMed PMID: 26089115. [DOI] [PubMed] [Google Scholar]
  • 7.Dennis M. Poor nutritional status on admission predicts poor outcomes after stroke observational data from the food trial. Stroke. 2003;34(6):1450–1455. doi: 10.1161/01.STR.0000074037.49197.8C. 10.1161/01.STR.0000074037.49197.8C [DOI] [PubMed] [Google Scholar]
  • 8.Nishioka S, Aragane H, Suzuki N, Yoshimura Y, Fujiwara D, Mori T, Kanehisa Y, Iida Y, Higashi K, Yoshimura-Yokoi Y, Sato C, Toyota M, Tanaka M, Ishii Y, Kosaka S, Kumagae N, Fujimoto A, Omura K, Yoshida S, Wakabayashi H, Momosaki R, Committee of Clinical Practice Guideline, Japanese Association of Rehabilitation Nutrition Clinical practice guidelines for rehabilitation nutrition in cerebrovascular disease, hip fracture, cancer, and acute illness: 2020 update. Clin Nutr ESPEN. 2021;43:90–103. doi: 10.1016/j.clnesp.2021.02.018. 10.1016/j.clnesp.2021.02.018 PubMed PMID: 34024570. [DOI] [PubMed] [Google Scholar]
  • 9.Sato Y, Yoshimura Y, Abe T. Nutrition in the First Week after Stroke Is Associated with Discharge to Home. Nutrients. 2021;13(3):943. doi: 10.3390/nu13030943. 10.3390/nu13030943 PubMed PMID: 33804072, PMCID 8001465. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Di Vincenzo O, Marra M, Di Gregorio A, Pasanisi F, Scalfi L. Bioelectrical impedance analysis (BIA) -derived phase angle in sarcopenia: A systematic review. Clin Nutr. 2020;40(5):3052–3061. doi: 10.1016/j.clnu.2020.10.048. 10.1016/j.clnu.2020.10.048 PubMed PMID: 33183880. [DOI] [PubMed] [Google Scholar]
  • 11.Lukaski HC, Kyle UG, Kondrup J. Assessment of adult malnutrition and prognosis with bioelectrical impedance analysis: phase angle and impedance ratio. Curr Opin Clin Nutr Metab Care. 2017;20(5):330–339. doi: 10.1097/MCO.0000000000000387. 10.1097/MCO.0000000000000387 PubMed PMID: 28548972. [DOI] [PubMed] [Google Scholar]
  • 12.Abe T, Yoshimua Y, Imai R, Sato Y. A Combined Assessment Method of Phase Angle and Skeletal Muscle Index to Better Predict Functional Recovery after Acute Sroke. The journal of nutrition, health & aging 2022. Published online April 11, 2022:1–7. doi: 10.1007/S12603-022-1777-9. [DOI] [PubMed]
  • 13.Sato Y, Yoshimura Y, Abe T. Phase Angle as an Indicator of Baseline Nutritional Status and Sarcopenia in Acute Stroke. Journal of Stroke and Cerebrovascular Diseases. 2022;31(1):106220. doi: 10.1016/j.jstrokecerebrovasdis.2021.106220. 10.1016/j.jstrokecerebrovasdis.2021.106220 PubMed PMID: 34826661. [DOI] [PubMed] [Google Scholar]
  • 14.Abe T, Yoshimura Y, Imai R, Yoneoka Y, Tsubaki A, Sato Y. Impact of Phase Angle on Physical Function in Patients with Acute Stroke. J Stroke Cerebrovasc Dis. 2021;30(9):105941. doi: 10.1016/j.jstrokecerebrovasdis.2021.105941. 10.1016/j.jstrokecerebrovasdis.2021.105941 PubMed PMID: 34217068. [DOI] [PubMed] [Google Scholar]
  • 15.Napoli M di, Papa F, Bocola V. C-Reactive Protein in Ischemic Stroke An Independent Prognostic Factor. Published online 2001. Accessed April 13, 2022. http://ahajournals.org. [DOI] [PubMed]
  • 16.Aquilani R, Maestri R, Boselli M, et al. The relationship between plasma amino acids and circulating albumin and haemoglobin in postabsorptive stroke patients. Published online 2019. doi: 10.1371/journal.pone.0219756. [DOI] [PMC free article] [PubMed]
  • 17.Yoshimura Y, Wakabayashi H, Nagano F, Bise T, Shimazu S, Shiraishi A. Low Hemoglobin Levels are Associated with Sarcopenia, Dysphagia, and Adverse Rehabilitation Outcomes After Stroke. J Stroke Cerebrovasc Dis. 2020;29(12):105405. doi: 10.1016/j.jstrokecerebrovasdis.2020.105405. 10.1016/j.jstrokecerebrovasdis.2020.105405 PubMed PMID: 33254381. [DOI] [PubMed] [Google Scholar]
  • 18.Garlini LM, Alves FD, Ceretta LB, Perry IS, Souza GC, Clausell NO. Phase angle and mortality: a systematic review. Eur J Clin Nutr. 2019;73(4):495–508. doi: 10.1038/s41430-018-0159-1. 10.1038/s41430-018-0159-1 PubMed PMID: 29695763. [DOI] [PubMed] [Google Scholar]
  • 19.Kilic MK, Kizilarslanoglu MC, Arik G, Bolayir B, Kara O, Dogan Varan H, Sumer F, Kuyumcu ME, Halil M, Ulger Z. Association of Bioelectrical Impedance Analysis-Derived Phase Angle and Sarcopenia in Older Adults. Nutr Clinical Pract. 2017;32(1):103–109. doi: 10.1177/0884533616664503. 10.1177/0884533616664503 [DOI] [PubMed] [Google Scholar]
  • 20.Barbosa-Silva MC, Barros AJ, Wang J, Heymsfield SB, Pierson RN., Jr Bioelectrical impedance analysis: population reference values for phase angle by age and sex. Am J Clin Nutr. 2005;82(1):49–52. doi: 10.1093/ajcn.82.1.49. 10.1093/ajcn/82.1.49 PubMed PMID: 16002799. [DOI] [PubMed] [Google Scholar]
  • 21.Uemura K, Doi T, Tsutsumimoto K, Nakakubo S, Kim MJ, Kurita S, Ishii H, Shimada H. Predictivity of bioimpedance phase angle for incident disability in older adults. J Cachexia Sarcopenia Muscle. 2019;11(1):46–54. doi: 10.1002/jcsm.12492. 10.1002/jcsm.12492 PubMed PMID: 31436391, PMCID 7015240. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Yoshimura Y, Wakabayashi H, Nagano F, Bise T, Shimazu S, Shiraishi A. Elevated Creatinine-Based Estimated Glomerular Filtration Rate is Associated with Increased Risk of Sarcopenia, Dysphagia, and Reduced Functional Recovery after Stroke. J Stroke Cerebrovasc Dis. 2021;30(2):105491. doi: 10.1016/j.jstrokecerebrovasdis.2020.105491. 10.1016/j.jstrokecerebrovasdis.2020.105491 PubMed PMID: 33253988. [DOI] [PubMed] [Google Scholar]
  • 23.Bouillanne O, Morineau G, Dupont C, Coulombel I, Vincent JP, Nicolis I, Benazeth S, Cynober L, Aussel C. Geriatric Nutritional Risk Index: a new index for evaluating at-risk elderly medical patients. Am J Clin Nutr. 2005;82(4):777–783. doi: 10.1093/ajcn/82.4.777. 10.1093/ajcn/82.4.777 PubMed PMID: 16210706. [DOI] [PubMed] [Google Scholar]
  • 24.Huang CY, Lin GH, Huang YJ, Song CY, Lee YC, How MJ, Chen YM, Hsueh IP, Chen MH, Hsieh CL. Improving the utility of the Brunnstrom recovery stages in patients with stroke: Validation and quantification. Medicine (Baltimore) 2016;95(31):e4508. doi: 10.1097/MD.0000000000004508. 10.1097/MD.0000000000004508 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Kunieda K, Ohno T, Fujishima I, Hojo K, Morita T. Reliability and validity of a tool to measure the severity of dysphagia: the Food Intake LEVEL Scale. J Pain Symp Manag. 2013;46(2):201–206. doi: 10.1016/j.jpainsymman.2012.07.020. 10.1016/j.jpainsymman.2012.07.020 [DOI] [PubMed] [Google Scholar]
  • 26.Charlson ME, Pompei P, Ales KL, MacKenzie CR. A new method of classifying prognostic comorbidity in longitudinal studies: Development and validation. J Chronic Dis. 1987;40(5):373–383. doi: 10.1016/0021-9681(87)90171-8. 10.1016/0021-9681(87)90171-8 PubMed PMID: 3558716. [DOI] [PubMed] [Google Scholar]
  • 27.Banks JL, Marotta CA. Outcomes validity and reliability of the modified Rankin scale: implications for stroke clinical trials: a literature review and synthesis. Stroke. 2007;38(3):1091–1096. doi: 10.1161/01.STR.0000258355.23810.c6. 10.1161/01.STR.0000258355.23810.c6 PubMed PMID: 17272767. [DOI] [PubMed] [Google Scholar]
  • 28.Ottenbacher KJ, Hsu Y, Granger CV, Fiedler RC. The reliability of the functional independence measure: A quantitative review. Arch Phys Med Rehabil. 1996;77(12):1226–1232. doi: 10.1016/s0003-9993(96)90184-7. 10.1016/S0003-9993(96)90184-7 PubMed PMID: 8976303. [DOI] [PubMed] [Google Scholar]
  • 29.Kido Y, Yoshimura Y, Wakabayashi H, Momosaki R, Nagano F, Bise T, Shimazu S, Shiraishi A. Sarcopenia is associated with incontinence and recovery of independence in urination and defecation in post-acute rehabilitation patients. Nutrition. 2021;91–92:111397. doi: 10.1016/j.nut.2021.111397. 10.1016/j.nut.2021.111397 PubMed PMID: 34364264. [DOI] [PubMed] [Google Scholar]
  • 30.Chen LK, Woo J, Assantachai P, Auyeung TW, Chou MY, Iijima K, Jang HC, Kang L, Kim M, Kim S, Kojima T, Kuzuya M, Lee JSW, Lee SY, Lee WJ, Lee Y, Liang CK, Lim JY, Lim WS, Peng LN, Sugimoto K, Tanaka T, Won CW, Yamada M, Zhang T, Akishita M, Arai H. Asian Working Group for Sarcopenia: 2019 Consensus Update on Sarcopenia Diagnosis and Treatment. J Am Med Dir Assoc. 2020;21(3):300–307.e2. doi: 10.1016/j.jamda.2019.12.012. 10.1016/j.jamda.2019.12.012 PubMed PMID: 32033882. [DOI] [PubMed] [Google Scholar]
  • 31.Yoshimura Y, Wakabayashi H, Bise T, Nagano F, Shimazu S, Shiraishi A, Yamaga M, Koga H. Sarcopenia is associated with worse recovery of physical function and dysphagia and a lower rate of home discharge in Japanese hospitalized adults undergoing convalescent rehabilitation. Nutrition. 2019;61:111–118. doi: 10.1016/j.nut.2018.11.005. 10.1016/j.nut.2018.11.005 PubMed PMID: 30710883. [DOI] [PubMed] [Google Scholar]
  • 32.Yoshimura Y, Bise T, Nagano F, Shimazu S, Shiraishi A, Yamaga M, Koga H. Systemic Inflammation in the Recovery Stage of Stroke: Its Association with Sarcopenia and Poor Functional Rehabilitation Outcomes. Prog Rehabil Med. 2018;3:1–10. doi: 10.2490/prm.20180011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33.Shimazu S, Yoshimura Y, Kudo M, Nagano F, Bise T, Shiraishi A, Sunahara T. Frequent and personalized nutritional support leads to improved nutritional status, activities of daily living, and dysphagia after stroke. Nutrition. 2021;83:111091. doi: 10.1016/j.nut.2020.111091. 10.1016/j.nut.2020.111091 PubMed PMID: 33388653. [DOI] [PubMed] [Google Scholar]
  • 34.Abe T, Iwata K, Yoshimura Y, Shinoda T, Inagaki Y, Ohya S, Yamada K, Oyanagi K, Maekawa Y, Honda A, Kohara N, Tsubaki A. Low Muscle Mass is Associated with Walking Function in Patients with Acute Ischemic Stroke. J Stroke Cerebrovasc Dis. 2020;29:105259. doi: 10.1016/j.jstrokecerebrovasdis.2020.105259. 10.1016/j.jstrokecerebrovasdis.2020.105259 PubMed PMID: 33066891. [DOI] [PubMed] [Google Scholar]
  • 35.Yoshimura Y, Wakabayashi H, Momosaki R, Nagano F, Shimazu S, Shiraishi A. Shorter Interval between Onset and Admission to Convalescent Rehabilitation Wards Is Associated with Improved Outcomes in Ischemic Stroke Patients. Tohoku J Exp Med. 2020;252(1):15–22. doi: 10.1620/tjem.252.15. 10.1620/tjem.252.15 PubMed PMID: 32848123. [DOI] [PubMed] [Google Scholar]
  • 36.Del Giorno R, Quarenghi M, Stefanelli K, Rigamonti A, Stanglini C, De Vecchi V, Gabutti L. Phase angle is associated with length of hospital stay, readmissions, mortality, and falls in patients hospitalized in internal-medicine wards: A retrospective cohort study. Nutrition. 2021;85:111068. doi: 10.1016/j.nut.2020.111068. 10.1016/j.nut.2020.111068 PubMed PMID: 33545536. [DOI] [PubMed] [Google Scholar]
  • 37.Player EL, Morris P, Thomas T, Chan WY, Vyas R, Dutton J, Tang J, Alexandre L, Forbes A. Bioelectrical impedance analysis (BIA)-derived phase angle (PA) is a practical aid to nutritional assessment in hospital in-patients. Clin Nutr. 2019;38(4):1700–1706. doi: 10.1016/j.clnu.2018.08.003. 10.1016/j.clnu.2018.08.003 PubMed PMID: 30170780. [DOI] [PubMed] [Google Scholar]
  • 38.Shin J, Kim CR, Park KH, Hwang JH, Kim SH. Predicting clinical outcomes using phase angle as assessed by bioelectrical impedance analysis in maintenance hemodialysis patients. Nutrition. 2017;41:7–13. doi: 10.1016/j.nut.2017.02.013. 10.1016/j.nut.2017.02.013 PubMed PMID: 28760431. [DOI] [PubMed] [Google Scholar]
  • 39.Pena NF, Mauricio SF, Rodrigues AMS, Carmo AS, Coury NC, Correia MITD, Generoso SV. Association Between Standardized Phase Angle, Nutrition Status, and Clinical Outcomes in Surgical Cancer Patients. Nutr Clin Pract. 2019;34(3):381–386. doi: 10.1002/ncp.10110. 10.1002/ncp.10110 PubMed PMID: 29870080. [DOI] [PubMed] [Google Scholar]
  • 40.Lim SK, Lim JY. Phase angle as a predictor of functional outcomes in patients undergoing in-hospital rehabilitation after hip fracture surgery. Arch Gerontol Geriatr. 2020;89:104060. doi: 10.1016/j.archger.2020.104060. 10.1016/j.archger.2020.104060 PubMed PMID: 32304889. [DOI] [PubMed] [Google Scholar]
  • 41.Morisawa T, Saitoh M, Takahashi T, Watanabe H, Mochizuki M, Kitahara E, Fujiwara T, Fujiwara K, Nishitani-Yokoyama M, Minamino T, Shimada K, Honzawa A, Shimada A, Yamamoto T, Asai T, Amano A, Daida H. Association of phase angle with hospital-acquired functional decline in older patients undergoing cardiovascular surgery. Nutrition. 2021;91–92:111402. doi: 10.1016/j.nut.2021.111402. 10.1016/j.nut.2021.111402 PubMed PMID: 34364266. [DOI] [PubMed] [Google Scholar]
  • 42.Fujishima I, Fujiu-Kurachi M, Arai H, Hyodo M, Kagaya H, Maeda K, Mori T, Nishioka S, Oshima F, Ogawa S, Ueda K, Umezaki T, Wakabayashi H, Yamawaki M, Yoshimura Y. Sarcopenia and dysphagia: Position paper by four professional organizations. Geriatr Gerontol Int. 2019;19(2):91–97. doi: 10.1111/ggi.13591. 10.1111/ggi.13591 PubMed PMID: 30628181. [DOI] [PubMed] [Google Scholar]
  • 43.Cohen DL, Roffe C, Beavan J, Blackett B, Fairfield CA, Hamdy S, Havard D, McFarlane M, McLauglin C, Randall M, Robson K, Scutt P, Smith C, Smithard D, Sprigg N, Warusevitane A, Watkins C, Woodhouse L, Bath PM. Post-stroke dysphagia: A review and design considerations for future trials. Int J Stroke. 2016;11(4):399–411. doi: 10.1177/1747493016639057. 10.1177/1747493016639057 PubMed PMID: 27006423. [DOI] [PubMed] [Google Scholar]
  • 44.Uemura K, Yamada M, Okamoto H. Association of bioimpedance phase angle and prospective falls in older adults. Geriatr Gerontol Int. 2019;19(6):503–507. doi: 10.1111/ggi.13651. 10.1111/ggi.13651 PubMed PMID: 30957354. [DOI] [PubMed] [Google Scholar]
  • 45.Shimazu S, Yoshimura Y, Kudo M, et al. Frequent and personalized nutritional support leads to improved nutritional status, activities of daily living, and dysphagia after stroke. Nutrition. 2021;83:111091. doi: 10.1016/j.nut.2020.111091. 10.1016/j.nut.2020.111091 PubMed PMID: 33388653. [DOI] [PubMed] [Google Scholar]
  • 46.Yoshimura Y, Wakabayashi H, Nagano F, et al. Chair-Stand Exercise Improves Sarcopenia in Rehabilitation Patients after Stroke. Nutrients. 2022;14(3) doi: 10.3390/nu14030461. 10.3390/NU14030461 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 47.Matsumoto A, Yoshimura Y, Wakabayashi H, et al. Deprescribing Leads to Improved Energy Intake among Hospitalized Older Sarcopenic Adults with Polypharmacy after Stroke. Nutrients. 2022;14(3) doi: 10.3390/nu14030443. 10.3390/NU14030443 [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Nutrition, Health & Aging are provided here courtesy of Elsevier

RESOURCES