Abstract
BACKGROUND:
Impaired motor control, balance, muscle strength, and respiratory function may affect the exercise capacity related to motor performance and activities in individuals with stroke.
OBJECTIVE:
To identify a physical parameter that the exercise capacity has the most significant relationship among physical parameters related to motor function, trunk control, balance, and motor performance and activities in individuals with ischemic stroke.
METHODS:
In total, 241 ischemic stroke patients were recruited in this retrospective study. The clinical measurements included the 6-minute walk test (6 MWT), Montreal cognitive assessment (MoCA), Fugl-Meyer assessment-lower extremity motor function (FMA-LE), trunk impairment scale (TIS), Berg balance scale (BBS), timed up and go test (TUG), 10-meter walk test (10 MWT), functional ambulation category (FAC), and functional independence measure (FIM).
RESULTS:
The 6 MWT was significantly correlated with the FMA-LE, BBS, TUG, 10 MWT, FAC, and FIM, indicating negative or positive moderate correlations. Additionally, the FMA-LE, TIS, BBS, TUG, 10 MWT, FAC, and FIM, excluding the 6 MWT, showed moderate to strong correlations with all of the other outcome measures, whereas the MoCA showed significant correlations only with the BBS and FIM.
CONCLUSIONS:
In this study, the exercise capacity has the most significant relationship with the TUG parameter in stroke patients. Additionally, we suggest that significant relationships between 6 MWT and other comprehensive physical functions measurements are closely related to walking ability in individuals with stroke.
Introduction
Exercise capacity is diminished in patients with stroke who have impaired motor control, balance,and motor performance and activities. Stroke patients show a reduction of up to 50%of respiratory function compared with age- and gender-matched healthy adults. After stroke, impaired motor control, balance, muscle strength, and respiratory function may affect the exercise capacity related to motor performance and activities. MacKay-Lyons & Makrides (2002) reported that the mean exercise capacity of patients with acute stroke was 60%of normative values (MacKay-Lyons & Makrides, 2002). After a stroke, patients may experience limited physical activity, leading to progressive deconditioning and deteriorating cardiovascular fitness (Arsura, 2005). Walking in patients with hemiplegic stroke usually requires extra energy expenditure of 1.5–2.0 times that of age-matched healthy adults. The extent and duration of the changes in exercise capacity during stroke rehabilitation are important due to the cardiorespiratory adaptation to the course of stroke rehabilitation and the requirement for cardiorespiratory exercise prescription. Although the gold standard for assessing exercise capacity is the maximal oxygen consumption (VO2max), its measurement requires specialized knowledge and a testing environment which has limited feasibility in most rehabilitation facilities. Moreover, the rigorous criteria for measuring the VO2max often cannot be met in most patients with stroke. For instance, progressive cardiopulmonary exercise testing is limited when disease-related complaints, including cardiovascular health risks or anxiety, are present in patients with hemorrhagic stroke (Visser-Meily et al., 2013). Several researchers suggested that the 6-minute walk test (6 MWT) can be selected to predict cardiorespiratory fitness or VO2max level in individuals with aneurysmal subarachnoid hemorrhage and healthy adults (Harmsen et al., 2017; Mänttäri et al., 2018). Additionally, Zhang et al. (2017) reported that the VO2max showed a strong correlation (correlation coefficient, r = 0.549) with 6 MWT in home-dwelling individuals aged between 45 and 90 years old (Zhang et al., 2017).
The 6 MWT is a simple and affordable test that is increasingly used to measure impaired exercise capacity resulting from respiratory, cardiovascular, and neurologic diseases (Laboratories, 2002; Salzman, 2009). The safety and feasibility of the 6 MWT were demonstrated in patients with stroke, and this tool has excellent test-retest reliability (intraclass correlation coefficient, ICC = 0.98) (Liu et al., 2008). In a systematic review with meta-analysis, stroke patients walked on average 284±107 m during the 6 MWT, and had large variations in the distance of the 6 MWT in accordance with the stroke severity (Dunn et al., 2015). In 6 MWT-related correlation studies, the 6 MWT showed moderate correlation (r = 0.80) with the Montreal cognitive assessment (MoCA) in patients with chronic stroke (Woo & Hwang, 2012). Carvalho, Willén, and Sunnerhagen (2008) demonstrated that the Fugl-Meyer assessment (FMA) for the lower extremity (r = 0.72) and Berg balance scale (BBS) (r = 0.68) were moderately to highly correlated with the 6 MWT (Carvalho, Willén, & Sunnerhagen, 2008). Kubo et al. (2020) determined that the reference distance value of 6 MWT depending on walking ability (functional ambulation category, FAC) in patients with subacute stroke, and suggested a positive relationship between the walking distance of the 6 MWT and the walking ability score of the FAC (Kubo et al., 2020). According to Dalgas, Severinsen, and Overgaard (2012), the 6 MWT showed a strong correlation (r = 0.94) with the 10-meter walk test (10 MWT) in patients with stroke (Dalgas, Severinsen, & Overgaard, 2012). The 6 MWT showed moderate to strong correlations (r = 0.52 to 0.89) with gait speed, locomotion of functional independence measure (FIM), and motor of FIM in patients with stroke (Fulk, Echternach, Nof, & O’Sullivan, 2008). Researchers have suggested that impaired cognition, motor function, balance, and motor performance and activities are closely related to diminished exercise capacity in patients with stroke.
Despite the clinical significance of the relationship between exercise capacity and cognition, motor function, balance, and motor performance and activities in patients with stroke, the relationships between comprehensive physical functions within the same subjects in a large sample remain poorly investigated. Furthermore, the relationships of exercise capacity with the trunk impairment scale (TIS; trunk control) and the timed up and go test (TUG; functional mobility) have not been presented in patients with stroke. Further research is needed to identify a physical parameter that the exercise capacity (physiological parameter) has the most significant relationship among physical parameters related to motor performance and activities because the decline in exercise capacity results from impaired motor performance and abilities and respiratory dysfunction in individuals with stroke. Therefore, this study mainly aimed to examine the relationships between the 6 MWT and other comprehensive physical function measurements (MoCA, FMA, TIS, BBS, TUG, 10 MWT, FAC, and FIM); that is, to identify a physical parameter that the exercise capacity has the most significant relationship among physical parameters related to motor function, trunk control, balance, and motor performance and activities in individuals with ischemic stroke. The second purpose of this study was to understand the relationships between stroke-related comprehensive physical functions through correlation interpretation of all measurements except for the 6 MWT within the same subjects in a large sample size.
Methods
Study design and participants
We conducted a retrospective study of inpatients with ischemic stroke admitted to the rehabilitation center at Chungnam National University Hospital from July 2019 to July 2020. In total, 241 patients were enrolled according to the following inclusion criteria: (1) first time stroke, (2) participating in routine rehabilitation programs after stroke, (3) no history of orthopedic or cardiac surgery, and (4) stable clinical status identified by a medical doctor specialized in cardiopulmonary rehabilitation. The details about the demographic and clinical characteristics of the participants are presented in Table 1. This study was approved by the Institutional Review Board (IRB) of Chungnam National University Hospital (IRB No. 2020-08-088-004).
Demographic and clinical characteristics of participants
Demographic and clinical characteristics of participants
Data are mean±standard deviationa and n (%)b.
6-minute walk test
The 6 MWT is a practical, valid, and reliable test that measures the distance (meters) walked in 6 min. The measurement procedures of the 6 MWT were performed in accordance with the guidelines of the American Thoracic Society (ATS) (Laboratories, 2002). Participants performed the 6 MWT indoors on a straight 30-meter walkway with marks representing intervals every 1 m. Prior to the test, the participants sat at rest in a chair near the starting line for at least 5 min. The participants were instructed to walk as far as possible at their comfortable pace between the starting and ending lines of the 30-meter walkway for 6 min. Simultaneously, the examiner provided standardized verbal encouragement (such as “You are doing well. You have 1–5 min to go.”) at every minute during measurement. The total distance walked for 6 min was recorded.
Montreal cognitive assessment
The MoCA is a rapid screening tool comprising one-page, 30-point tests for detecting mild cognitive impairment which takes approximately 10 min to administer. The MoCA domains contain cognitive items including visuospatial abilities, executive functions, short-term memory recall, attention, concentration, working memory, language, and time and space orientation. The total score ranges from 0 to 30 points, and a score of 26 or above indicates normal cognitive function (Nasreddine et al., 2005). The MoCA showed a high internal consistency coefficient (Cronbach’s α= 0.88), intra-rater and inter-rater reliability (Pearson correlation coefficients, r = 0.93 to 0.97), and validity (r = 0.87) in stroke patients (Tu et al., 2013).
Fugl-meyer assessment
The FMA is a stroke-specific performance-based impairment measurement. It is designed to assess motor function, balance, sensation, joint range of motion, and joint pain using a 3-point ordinal scale where 0 = cannot perform, 1 = performs partially, and 2 = performs fully in patients with stroke. In particular, the motor function among these 5 domains contains items including movement, coordination, and reflex of the upper and lower extremities (Fugl-Meyer, 1975). In this study, the motor function of the lower extremity (FMA-LE) was assessed because a previous study found significant relationships between low extremity muscle strength related to motor function and exercise capacity in chronic stroke survivors (Polese et al., 2013). The maximal score of FMA-LE is 34 points. The inter-rater reliability of the FMA in patients with stroke was high (r = 0.89–0.95) for the lower extremity motor function domain (Gladstone, Danells, & Black, 2002). The concurrent validity of the FMA-LE (r = 0.661) was highly correlated with the BBS in hemiplegic patients with stroke (Kim et al., 2012).
Trunk impairment scale
The TIS is a standardized scale used to evaluate trunk control comprising static and dynamic sitting balance and trunk coordination in patients with stroke. This scale consists of 17 items, and each item is scored on a 2-, 3-, or 4-point ordinal scale. The total score ranges from 0 to 23 points, and a higher score indicates better trunk control. The TIS has excellent intra-rater and inter-rater reliability (ICC = 0.96 and 0.99), and it was correlated with the Barthel index (r = 0.86) and trunk control test (r = 0.83) for examining construct and concurrent validity in stroke patients (Verheyden et al., 2004).
Berg balance scale
The BBS is the most widely used standardized balance assessment tool and is based on the performance measurement of various functional movements in individuals with stroke. The functional movements were 14-item, including sitting to standing, standing unsupported, standing to sitting, transfers, turning 360°, and standing on one leg. Each item is scored on a five-point scale from 0 (unable to perform) to 4 (able to perform). The total score is 56; scores of 20 or below represent balance impairment, 21 to 40 indicate acceptable balance, and 41 to 56 show good balance ability. The BBS has excellent inter-rater reliability (ICC = 0.95) and high validity (r = 0.71) for subacute stroke (Chou et al., 2006; Mao, Hsueh, Tang, Sheu, & Hsieh, 2002).
Timed up and go test
The TUG is frequently used to assess functional mobility in patients with impaired mobility due to neurological diseases. For the test, the participant was instructed to rise from a seated position in a chair with an armrest, walk in a straight line for 3 m, walk back to the chair, and sit. Concurrently, a verbal command was given by a well-trained examiner, “walk as fast as possible and safely.” The total time needed to perform this task was recorded. This tool has excellent intra-rater and inter-rater reliability (ICC = 0.944–0.998) and high validity with BBS scores (r = –0.634 to –0.527) in people with chronic stroke (Chan, Tou, Mimi, & Ng, 2017).
10-meter walk test
The 10 MWT is a performance-based assessment tool to evaluate the walking ability and is conducted in a straight 10-meter walkway. Participants were asked to walk at their self-selected walking speed along a walkway. The participant was instructed verbally to “walk as fast as possible without running.” The time needed to cover the middle 6 m of the walkway, excluding the first and last 2 m for the acceleration and deceleration phases of walking, was recorded to acquire a rhythmic phase of walking speed. Then, the time was converted to the walking speed in m/s. The 10 MWT had high test-retest reliability (ICC = 0.83), and correlated with the 6 MWT conducted using 15- and 30-meter walkways (r = 0.80–0.95) in people with post-stroke (Cheng, Nelson, Brooks, & Salbach, 2020).
Functional ambulation category
The FAC is a functional walking test designed to categorize the functional ambulation ability. This tool distinguishes six levels (0 to 5) of walking ability according to the amount of physical support required. The categories are as follows: (0) nonfunctional ambulation, (1) ambulator-dependent: physical assistance level II, (2) ambulator-dependent: physical assistance level I, (3) ambulator-dependent: supervision, (4) ambulator-independent: level surfaces only, and (5) ambulator-independent. The FAC showed high intra-rater (Cohen kappa = 0.950) and inter-rater (kappa = 0.905) reliability and good validity (r = 0.686–0.952) in hemiparetic patients after stroke (Mehrholz, Wagner, Rutte, Meiβner, & Pohl, 2007).
Functional independence measure
The FIM is an 18-item measurement tool that measures the physical functional disability of individuals with stroke based on the level of assistance required. The FIM items included self-care (6 items), bowel and bladder control (2 items), transfers (3 items), locomotion (2 items), communication (2 items), and social cognition (3 items). Each item is scored from 1 (total assistance) to 7 (complete independence). The FIM established excellent test-retest reliability (ICC = 0.89) and validity with the Barthel index (r = 0.92) in previous studies related to stroke (Fricke, Unsworth, & Worrell, 1993; Hsueh, Lin, Jeng, & Hsieh, 2002).
Statistical analysis
Descriptive statistics include means and standard deviations. The Pearson product correlation coefficient (r) was used to analyze correlations be-tween comprehensive physical functions measured by the 6 MWT, MoCA, FMA-LE, TIS, BBS, TUG, 10 MWT, FAC, and FIM. An r value ranging from 0.7 to 1 indicates a strong correlation, a value in the range of 0.3–0.7. represents a moderate correlation, and a value range of 0.1–0.3 indicates a weak correlation. Finally, r values less than 0.1 are considered negligible. All statistical analyses were completed using SPSS for Windows version 18.0 (SPSS Inc., Chicago, IL, USA), and a significance level of 0.05 was used.
Results
Results of comprehensive physical function measurements
The results of the comprehensive physical function measurements in individuals with ischemic stroke are presented in Table 2. The means and standard deviations of these comprehensive physical function measurements were 340.9±173.2 m (6 MWT), 15.1±6.6 scores (MoCA), 25.3±9.5 scores (FMA-LE), 14.5±7.8 scores (TIS), 25.3±20.0 scores (BBS), 20.8±17.4 sec (TUG), 0.73±0.36 m/s (10 MWT), 2.4±1.5 grade (FAC), and 62.8±28.1 scores (FIM) (Table 2).
Results of comprehensive physical function measurements
Results of comprehensive physical function measurements
6 MWT: 6-minute walk test, MoCA: Montreal cognitive assessment, FMA-LE: Fugl-Meyer assessment-lower extremity motor function, TIS: Trunk impairment scale, BBS: Berg balance scale, TUG: Timed up and go test, 10 MWT: 10-meter walk test, FAC: Functional ambulation category, FIM: Functional independence measure.
Correlations between the 6 MWT and other physical function measurements are shown in Table 3. The 6 MWT was significantly associated with the FMA-LE (r = 0.387, p = 0.016), BBS (r = 0.642, p = 0.000), TUG (r = –0.674, p = 0.000), 10 MWT (r = –0.663, p = 0.000), FAC (r = 0.610, p = 0.000), and FIM (r = 0.411, p = 0.018), indicating negative or positive moderate correlations. However, there was no significant correlation between the 6 MWT and MoCA (r = –0.089, p = 0.685) or between the 6 MWT and TIS (r = 0.264, p = 0.110) (Table 3).
Correlations between the 6 MWT and other physical function measurements
Correlations between the 6 MWT and other physical function measurements
Data are Pearson correlation coefficient r and p values, *p < 0.05, †p < 0.01. 6 MWT: 6-minute walk test, MoCA: Montreal cognitive assessment, FMA-LE: Fugl-Meyer assessment-lower extremity motor function, TIS: Trunk impairment scale, BBS: Berg balance scale, TUG: Timed up and go test, 10 MWT: 10-meter walk test, FAC: Functional ambulation category, FIM: Functional independence measure.
Table 4 presents the correlations between the MoCA, FMA-LE, TIS, BBS, TUG, 10 MWT, FAC, and FIM measurements. The MoCA was positively correlated with the BBS (r = 0.284, p = 0.005) and FIM (r = 0.466, p = 0.000), while the relationships among the MoCA and other measurements, including the FMA-LE (r = –0.023, p = 0.814), TIS (r = 0.089, p = 0.359), TUG (r = –0.164, p = 0.249), 10 MWT (r = 0.009, p = 0.947), and FAC (r = 0.061, p = 0.604) indicated no statistically significant correlation. The FMA-LE (r = –0.535 to –0.637 and r = 0.599 to 0.779, p = 0.000), TIS (r = –0.316 to –0.347 and r = 0.688 to 0.804, p < 0.01), TUG (r = –0.316 to –0.722 and r = 0.960, p < 0.01), 10 MWT (r = –0.347 to –0.698 and r = 0.960, p < 0.01), and FAC (r = –0.467 to –0.476 and r = 0.682 to 0.865, p = 0.000) showed negative or positive correlations in comparison to all of the other outcome measures, with the exception of the MoCA. Moreover, the BBS (r = –0.698 to –0.722, p = 0.000 and r = 0.284 to 0.865, p < 0.01) and FIM (r = –0.369, p = 0.001 and r = 0.466 to 0.813, p = 0.000) were negatively or positively related to all of the other physical function measurements, indicating moderate to strong correlations (Table 4).
Correlations between comprehensive physical function measurements (except for 6 MWT)
Correlations between comprehensive physical function measurements (except for 6 MWT)
Data are Pearson correlation coefficient r and p values, †p < 0.01. 6 MWT: 6-minute walk test, MoCA: Montreal cognitive assessment, FMA-LE: Fugl-Meyer assessment-lower extremity motor function, TIS: Trunk impairment scale, BBS: Berg balance scale, TUG: Timed up and go test, 10 MWT: 10-meter walk test, FAC: Functional ambulation category, FIM: Functional independence measure.
This retrospective study demonstrated the relationships between 6 MWT and other comprehensive physical function measurements (MoCA, FMA-LE, TIS, BBS, TUG, 10 MWT, FAC, and FIM) as well as between comprehensive physical function measurements except for 6 MWT in 241 individuals with ischemic stroke. In terms of the relationships between the 6 MWT and other physical function measurements, we found that the 6 MWT was significantly related to the FMA-LE, BBS, TUG, 10 MWT, FAC, and FIM, indicating moderate correlations. These correlations revealed that the 6 MWT has the most significant relationship with TUG parameter. Although a study on the relationship between 6 MWT and TUG has not been reported previously, several researchers suggest that stroke survivors may need almost twice as many steps and twice as much time to complete a 180° turn compared with age-matched adults (Danielli Coelho de Morais Faria, Fuscaldi Teixeira-Salmela, & Nadeau, 2009; Lam & Luttmann, 2009). Pohl et al. (2002) demonstrated that the FMA-LE and BBS scores were significant predictors of the 6 MWT distance, with 45%of the variance in the distance walked in a stepwise regression analysis, and suggested that stroke-related impairments contribute to diminished 6 MWT performance in individuals post-stroke (Pohl et al., 2002). Dunn et al. (2015) reported that stroke survivors reached an average 6 MWT distance of 285 m (95%confidence interval, CI = 252, 318), whereas healthy older adults (over 60 years) achieved an average distance of 499 m (95%CI 480, 519) on a straight 30-m walkway (Bohannon, 2007). Several studies investigated the relationship between the 6 MWT speed (m/s) and the comfortable and maximal 10 MWT speed (m/s) in people with chronic stroke, and found strong correlations (comfortable 10 MWT: r = 0.84 to 0.91, maximal 10 MWT: r = 0.94 to 0.95) between both tests (Dalgas et al., 2012; Flansbjer, Holmbäck, Downham, Patten, & Lexell, 2005). Kubo et al. (2020) determined the reference distance value of 6 MWT depending on the walking ability (FAC) and the cutoff value of walking independence in patients with subacute stroke. These investigators suggested that the reference distance value of FAC 2 to 5 were 141.8 m, 224.5 m, 352.6 m, and 448.8 m, respectively, showing the positive correlation between 6 MWT and FAC. They also demonstrated that the cutoff value of the 6 MWT for independent walking ability was 304 m (with a sensitivity of 0.833 and specificity of 0.900), and this value for judging walking independence may support the early return to activities of daily living during stroke rehabilitation (Kubo et al., 2020). Finally, correlations between the 6 MWT and FIM (locomotion, locomotion + stairs, motor, total scores) were r = 0.69 (locomotion and locomotion + stairs FIM), r = 0.52 (motor FIM), and r = 0.45 (total FIM), respectively (Fulk et al., 2008). The walking disability after stroke contributes to the lack of aerobic condition and an increase in the demand of energy, thereby, limiting the locomotion performance in activities of daily living (Bowden, Embry, & Gregory, 2011; Carr & Shepherd, 2011; De Almeida et al., 2012).
In terms of the relationships between comprehensive physical functions (except for 6 MWT), the FMA-LE, TIS, TUG, 10 MWT, and FAC showed moderate to strong correlations with all of the other outcome measures, except for the MoCA. The BBS and FIM showed moderate to strong correlations with all of the other comprehensive physical function measurements in individuals with ischemic stroke. A previous study found that the FMA-LE scores were closely correlated with the TIS at one, three, and six months after stroke onset. This shows the relationship between trunk impairment and lower limb weakness, indicating that truncal and limb motor controls have similar recovery trajectories (Verheyden et al., 2008). Correlations between the TIS, BBS, TUG, and 10 MWT were studied in individuals with a single stroke, and found that the TIS was positively or negatively correlated with the BBS (r = 0.529), TUG (r = –0.426), and 10 MWT (r = –0.516). Additionally, there were significantly moderate to strong correlations between the BBS and TUG (r = –0.567), BBS and 10 MWT (r = –0.838), and TUG and 10 MWT (r = 0.674) (J.-H. Kim, Lee, & Jeon, 2015). Numerous studies have investigated the relationships between FAC and gait parameters such as walking velocity, cadence, and step and stride length in neurologically impaired patients, indicating that improvement in FAC scores is related to improvements in walking ability (Holden, Gill, & Magliozzi, 1986; Mehrholz et al., 2007). This suggestion supported our results, in which the FAC was significantly correlated with walking ability-related FMA-LE, BBS, TUG, 10 MWT, and FIM measurements. Jung, Kim, and Park (2005) reported a moderate correlation between BBS and FIM (r = 0.529) in 92 patients with the first attack of stroke, suggesting that balance function could affect functional motor ability during the stroke rehabilitation process (Jung, Kim, & Park, 2005). Significant correlations between the BBS and MoCA (r = 0.46), as well as FIM motor score and MoCA (total: r s = 0.40, visuoexecutive: r s = 0.51, delayed recall: r s = 0.27, orientation: r s = 0.38, naming: r s = 0.25) for stroke patients were revealed in previous studies (Kang, Jeong, Kim, & Ha, 2018; Toglia, Fitzgerald, O’Dell, Mastrogiovanni, & Lin, 2011). Lower visuoexecutive subscores may support the recognition of persons at risk for impaired balance control and functional motor ability (e.g., self-care and mobility) during stroke rehabilitation programs.
This study proposes significant relationships between the 6 MWT and the FMA-LE, BBS, TUG, 10 MWT, FAC, and FIM, since all measurements were closely related to walking ability in individuals with stroke. Importantly, these results showed that the exercise capacity has the most significant relationship with the TUG parameter. These relationships could be interpreted because the walking ability to perform 6 MWT is an important factor in the overall functional ability related to post-stroke. An intensive gait training proposed during stroke rehabilitation program is probably expected to affect the level of exercise capacity and related motor performance and activities.
Conclusion
Impaired motor control, balance, muscle strength, and respiratory function are associated with diminished exercise capacity in individuals with stroke. Our findings demonstrated that a short 6 MWT distance may assist in identifying stroke patients at risk together with decreased FMA, BBS, FAC, and FIM scores as well as the increased TUG and 10 MWT time during the stroke rehabilitation program. Importantly, the exercise capacity has the most significant relationship with the TUG parameter. We suggest that significant relationships between 6 MWT and other comprehensive physical function measurements are closely associated with walking ability in individuals with stroke.
Conflict of interest
None to report.
Funding
This research was supported by the Bio & Medical Technology Development Program through the National Research Foundation (NRF) funded by the Korean government (No. NRF-2019M3E5D1A02068569).
