https://www.jstage.jst.go.jp/article/prm/3/0/3_20180011/_html/-char/ja
3 巻 (2018)
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ABSTRACT
Objective: The aim of our study was to investigate how systemic inflammation relates to sarcopenia and its impact on functional outcomes in the recovery stages of stroke. Methods: A retrospective cohort study was performed in consecutive patients admitted to convalescent rehabilitation wards following stroke. Patients with acute or chronic high-grade inflammatory diseases were excluded. Systemic inflammation was evaluated using the modified Glasgow Prognostic Score (mGPS). Sarcopenia was defined as a loss of skeletal muscle mass and decreased muscle strength, with the cut-off values set by the Asian Working Group for Sarcopenia. The primary outcome was the motor domain of the Functional Independence Measure (FIM-motor). Univariate and multivariate analyses were used to determine whether mGPS was associated with sarcopenia and FIM-motor at discharge. Results: The study included 204 patients (mean age 74.1 years, 109 men). mGPS scores of 0, 1, and 2 were assigned to 149 (73.0%), 40 (19.6%), and 13 (6.4%) patients, respectively. Sarcopenia was diagnosed in 81 (39.7%) patients and was independently associated with stroke history (odds ratio [OR] 1.890, P=0.027), premorbid modified Rankin scale (OR 1.520, P=0.040), body mass index (OR 0.858, P=0.022), and mGPS score (OR 1.380, P=0.021). Furthermore, the mGPS score was independently associated with sarcopenia (OR 1.380, P=0.021) and FIM-motor at discharge (β=−0.131, P=0.031). Conclusion: Systemic inflammation is closely associated with sarcopenia and poor functional outcomes in the recovery stage of stroke. Early detection of systemic inflammation and sarcopenia can help promote both adequate exercise and nutritional support to restore muscle mass and improve post-stroke functional recovery.
INTRODUCTION
Sarcopenia is the loss of muscle mass, strength, and physical function and largely accounts for physical frailty. It also increases the risk of adverse outcomes such as physical disability, poor quality of life, and death.1) Furthermore, sarcopenia with disability is becoming an important concept in rehabilitation2) because its prevalence is approximately 50% in hospital-based rehabilitation centers worldwide3) and 53% in convalescent rehabilitation wards in Japan.4) Sarcopenia is associated with conditions that are major causes of disability, such as stroke, hip fractures, and hospital-associated deconditioning.2) Moreover, sarcopenia can lead to poor outcomes in hospital rehabilitation settings.5) Therefore, in rehabilitation settings, early detection and appropriate management of sarcopenia, i.e., prevention and treatment, are very important.
Stroke is one of the leading causes of morbidity and mortality worldwide,6) and more than two-thirds of stroke survivors undergo rehabilitation after hospitalization.7) In geriatric medicine, stroke-related sarcopenia is an emerging concept that has garnered much interest.8,9,10) Although it has recently been reported that up to 50% of older post-stroke patients are diagnosed with sarcopenia as defined by the Asian Working Group for Sarcopenia,11,12) there is little information about the pathology and clinical impact of stroke-related sarcopenia.
Systemic inflammation plays an important role in sarcopenia. Chronic low-grade inflammation and changes in body composition are interconnected phenomena that characterize the aging process, leading to sarcopenia.13,14,15) The association between inflammation and muscle wasting as well as impairment of physical function has been known for many years.16,17,18) Nevertheless, few studies have attempted to evaluate the relationship between systemic inflammation and sarcopenia or to evaluate the adverse effects of sarcopenia on health-related outcomes in rehabilitation settings. Furthermore, to the best of our knowledge, no studies have reported the associations between systemic inflammation and functional rehabilitation outcomes in the recovery stages of stroke.
Therefore, the aim of this study was to determine how systemic inflammation relates to sarcopenia and its impact on functional outcomes in the recovery stages in post-stroke patients.
MATERIALS AND METHODS
This was a retrospective cohort study conducted at a 225-bed hospital that provides convalescent rehabilitation in Kumamoto, Japan, and where 28% of the residents are more than 65 years old. Because of the retrospective nature of the study, an opt-out procedure for recruitment was instituted allowing the patients to withdraw from the study at any time. The study was approved by the Institutional Review Board of Kumamoto Rehabilitation Hospital and adhered to the tenets of the Declaration of Helsinki.
Participants
The present study examined data from 262 consecutive stroke patients admitted to the convalescent rehabilitation wards at the Kumamoto Rehabilitation Hospital between June 2015 and December 2017. The following patients were excluded: (1) those with disturbance of consciousness, (2) those for whom bioelectrical impedance analysis (BIA) was not applicable because of restlessness, implanted metallic devices, or use of other medical equipment, (3) those with acute or chronic high-grade inflammatory diseases, and (4) those who were medically unstable.
Participant characteristics including age, sex, stroke type, body mass index (BMI), nutritional status (the Mini Nutritional Assessment-Short Form [MNA-SF]),19,20) dysphagia using the Food Intake Level Scale (FILS),21) comorbidity severity (the Charlson Comorbidity Index [CCI]),22) premorbid activities of daily living (ADL) (the modified Rankin scale [mRS]),23) time from stroke onset, the presence of paralysis (if present, Brunnstrom stage (BRS) of the paralyzed lower limb),24) and stroke history were all recorded at the time of admission. Within 3 days of admission, the skeletal muscle mass was assessed using BIA, the patient’s physical and cognitive functions were assessed using the Functional Independence Measure (FIM),25) and the handgrip strength was measured. Trained nurses evaluated the BMI, and trained physical and occupational therapists assessed BIA, handgrip strength, and FIM. Handgrip strength was measured using a Smedley hand-dynamometer (TTM, Tokyo, Japan) in the non-dominant hand (or in case of hemiparesis, in the non-paralyzed hand), with the patient in a standing or seated position, depending on their ability, and with arms straight at their side; the higher value from two measurements was recorded.
Systemic Inflammation Assessment
We evaluated low-grade systemic inflammation using the modified Glasgow Prognostic Score (mGPS), which is calculated using serum levels of C-reactive protein (CRP) and albumin (Alb). The mGPS has been validated as an independent prognostic factor in patients with various conditions,26,27) including dependence on parenteral nutrition,28) gastric cancer,29) lung cancer,30) soft tissue sarcoma,31) and chemotherapy.32)
The mGPS was calculated as follows33,34): patients with high CRP levels (>1.0 mg/dL) and low Alb levels (<3.5 g/dL) were assigned a score of 2. Patients with high CRP levels (>1.0 mg/dL) were assigned a score of 1, and patients with CRP levels of ≤1.0 mg/dL were assigned a score of 0; albumin levels do not affect a score of 1 or 0. The mGPS for all patients was determined at the time of their admission to the convalescent rehabilitation wards.
Sarcopenia Definition
Sarcopenia was defined as a low skeletal muscle mass index (SMI), as assessed using BIA, and decreased muscle strength (handgrip strength)1) using cut-off values specific to the elderly Asian population.12) A multi-frequency validated BIA instrument (InBody S10; InBody, Tokyo, Japan) was used for the patients in the present study, many of whom were unable to stand independently. The body composition was measured with patients in the supine position. The measurements were performed by experienced physical therapists in the evenings 1 h before dinner and after more than 1 h of rest following rehabilitation. A correction for dehydration caused by exercise was applied when applicable. The SMI was calculated as the measured skeletal muscle mass divided by the squared body height in meters. The cut-off values for SMI in men and women were <7.0 kg/m2 and <5.7 kg/m2, respectively. The cut-off values for handgrip strength in men and women were <26 kg and <18 kg, respectively.12)
Main Outcomes
The primary outcome was the FIM score25) at discharge. The FIM score is one of the most common measurement tools for assessing ADLs. The FIM is divided into the motor domain (FIM-motor) with 13 sub-items and the cognitive domain (FIM-cognitive) with 5 sub-items. Tasks are rated on a seven-point ordinal scale that ranges from total assistance to complete independence. The total FIM score ranges from 18 to 126 points; FIM-motor ranges from 13 to 91 points; and FIM-cognitive from 5 to 35 points. Lower scores indicate lower abilities regarding ADLs.
The secondary outcomes included SMI, handgrip strength, and Alb level at discharge.
Statistical Analysis
This study was powered to detect an effect size of a score of 15 in FIM-motor.35) Assuming an alpha error of 0.05 and a two-sided effect, a sample size of 23 per group provided 80% power to observe the effect, implying that a minimum of 46 participants with or without sarcopenia were needed. Statistical analyses were performed using IBM SPSS Statistics (version 21, Armonk, New York). Continuous variables were reported as means (standard deviation, SD) for parametric data or medians (25th–75th percentiles, IQR) for non-parametric data. The t-test, chi-squared test, and the Mann-Whitney U test were used to examine differences between groups with and without sarcopenia. One-way ANOVA for parametric data and the Kruskal-Wallis test for non-parametric data were used for comparing the three independent samples based on the mGPS score. Univariate and multivariate logistic analyses were used to examine which variables were associated with sarcopenia after adjusting for confounders while excluding CCI owing to multicollinearity with mGPS. Multiple linear regression analysis was used to examine which variables were independently associated with FIM-motor at discharge as a functional rehabilitation outcome. Covariates selected to adjust for bias included age, sex, length of stay, time from onset, premorbid mRS, BRS, FILS, MNA-SF, sarcopenia, mGPS, FIM-motor, and FIM-cognitive, all of which were considered to be clinically associated with ADL at discharge, while excluding CCI owing to multicollinearity with mGPS. P values <0.05 were considered statistically significant.
Ethics
We conducted the study in accordance with the Declaration of Helsinki, and the study was approved by the ethics committee of Kumamoto Rehabilitation Hospital. We supplied information regarding the study to all patients, and patients were informed that withdrawal from the study was always possible.
RESULTS
The present study included 204 patients (mean age 74.1 years, 109 men, and 95 women) for analysis. Patients with missing data (n=11) and those with disturbed consciousness (n=19), those not able to undergo BIA (n=14), those with other acute disease (s) or chronic high-grade inflammation (n=12), and those in a medically unstable condition (n=2) were all excluded from the study
Participant Characteristics
Table 1 compares the characteristics of study participants with and without sarcopenia. Stroke types included cerebral infarction (n=127, 62.3%), cerebral hemorrhage (n=62, 30.4%), and subarachnoid hemorrhage (n=15, 7.4%). Of the 204 patients included in the current study, 81 (39.7%) were diagnosed with sarcopenia. mGPS scores of 0, 1, and 2 were assigned to 151 (74.0%), 40 (19.6%), and 13 (6.4%) patients, respectively. Sarcopenic patients exhibited significantly lower Alb levels (3.4 [0.6] g/dL vs. 3.6 [0.5] g/dL, P=0.015) and significantly higher CRP levels (1.4 [1.1] mg/dL vs. 1.0 [0.9] mg/dL, P=0.002) compared with those without sarcopenia, leading to significant differences in the mGPS scores between the two groups. Moreover, patients with sarcopenia had a significantly higher CCI score compared to those without sarcopenia (3 [3–5] vs. 3 [2–4], P=0.034). However, there was no difference in the frequency of sarcopenia based on the stroke type.
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