Relations Between 6 Minute Walking Distance and 10 Meter Walking Speed in Patients With Multiple Sclerosis and Stroke

ORIGINAL ARTICLE Relations Between 6 Minute Walking Distance and 10 Meter Walking Speed in Patients With Multiple Sclerosis and Stroke Ulrik Dalgas, PhD, Kaare Severinsen, PhD, Kristian Overgaard, PhD 1167 ABSTRACT. Dalgas U, Severinsen K, Overgaard K. Relations between 6 minute walking distance and 10 meter walking speed in patients with multiple sclerosis and stroke. Arch Phys Med Rehabil 2012;93:1167-72. Objective: To investigate the relationship between a short walking test and a long walking test in patients with walking disability due to multiple sclerosis (MS) or stroke. Design: Cross-sectional observational study. Setting: University hospital and sport science department. Participants: Patients with MS (n 38), patients with stroke (n 48), and healthy subjects (n 46). Patients were participants in other clinical trials. Interventions: Not applicable. Main Outcome Measure: Walking speed in a 10m walk test and a 6 minute walk test was compared. Results: Despite differences in absolute walking speed between long and short tests, strong correlations were found between both the tests in patients with MS (r.95) and in patients with stroke (r.94), whereas a more moderate correlation was found in healthy controls (r.69.70). Conclusions: Our findings show that walking speeds of a short walking test and a long walking test are strongly correlated in both patients with MS and patients with stroke, whereas correlations in healthy subjects are weaker. Key Words: Gait; Muscle strength; Rehabilitation. 2012 by the American Congress of Rehabilitation Medicine From the Department of Sport Science, Aarhus University, Aarhus (Dalgas, Overgaard); and the Department of Neurology, Aarhus University Hospital, Aarhus (Severinsen), Denmark. Supported by the National Multiple Sclerosis Society, the Research Foundation of the MS Clinic of Southern Denmark (Vejle, Esbjerg, and Soenderborg), Director Werner Richter and Wife s Grant, the Augustinus Foundation, Engineer Bent Boegh and Wife Inge Boegh s Foundation, Vilhelm Bangs Foundation, Manufacturer Mads Clausen s Foundation, the Toyota Foundation, Mrs Benthine Lund s Foundation, AP Moeller s Foundation, Velux Foundation, and Tryg Foundation. Dalgas has received travel grants and/or teaching honorary from Biogen Idec, Merck Serono, and Sanofi Aventis. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit on the authors or on any organization with which the authors are associated. Clinical Trial Registration No. NCT00381576 Correspondence to Ulrik Dalgas, PhD, Dept of Sport Science, Aarhus University, Dalgas Ave 4, 8000 Aarhus C, Denmark, e-mail: dalgas@sport.au.dk. Reprints are not available from the author. In-press corrected proof published online on Apr 21, 2012, at www.archives-pmr.org. 0003-9993/12/9307-00596$36.00/0 doi:10.1016/j.apmr.2012.02.026 WALKING SPEED AND ENDURANCE are 2 important aspects of walking capacity, and in many groups of patients walking capacity is impaired. Consequently, in clinical intervention trials and in daily clinical settings, walking capacity is a frequently used outcome measure for evaluation of disability. Neurologic patients are the most frequently studied group of patients in studies applying walking tests as an outcome measure. 1 In general, tests of walking capacity are divided into short and long walking tests evaluating walking speed and walking endurance, respectively. The short 10 meter walk test (10mWT) is used to test either comfortable or maximal walking speed, 1 whereas the long 6 minute walk test (6MWT) is used for testing the walking endurance. 2 The maximal 10mWT requires a brief and maximal effort and would, therefore, be expected to be associated with muscle strength. The 6MWT, on the other hand, would be expected to be associated with aerobic capacity because of the cardiorespiratory strain of completing this test. Consequently, the 10mWT would not be expected to show a strong relationship with the 6MWT, which is supported by the one study in healthy subjects that we identified, showing only moderate correlations (r.65.73) between the 2 tests. 3 Nonetheless, Flansbjer et al 4 reported a strong relationship between the 6MWT and a maximal 10mWT (r.95), while Eng et al 5 found a similar relationship (r.92) between comfortable walking speed and the 6MWT in groups of patients with stroke. Therefore, it is possible that the information obtained from the 2 walking tests equally reflects the walking impairment in patients with stroke. Similarly, Dobkin 6 proposed that when applying comfortable walking speed, short and long walking tests might be redundant clinical measures on the basis of finding similar absolute values for short distance walking speed and speed during a 6MWT in patients with stroke. Contrary to this, Dean et al 7 reported that the distance covered during the 6MWT could not be predicted from the 10mWT (comfortable speed) in a group of 14 patients with stroke. The reason for the discrepancy is not clear, but it may be related to differences either in methodology or in the disability levels of the patients in the studies. In patients with multiple sclerosis (MS), no studies describe the relationship between the 10mWT and the 6MWT, but unpublished data from a study 8 including both walking tests indicated a strong relationship (r.88) (D. Gijbels, written communication, November 2010). Published data confirming this strong relationship are, therefore, needed in patients with MS. In summary, it remains unclear whether the 6MWT and the 10mWT actually measure different aspects of walking in patients with stroke and patients with MS or whether the 10mWT provides sufficient information on walking that would be practical and time saving, at least in the daily clinical setting. Furthermore, the findings from healthy subjects also need to be confirmed because no studies have directly compared the relationship observed in patients with MS and patients with stroke with the relationship found in healthy subjects. To further evaluate the relationship between the 6MWT and the 10mWT in patients with MS and patients with stroke, we MS Vo 2 peak 6MWT 10mWT List of Abbreviations multiple sclerosis peak oxygen consumption 6 minute walk test 10 meter walk test

1168 WALKING IN MULTIPLE SCLEROSIS AND STROKE, Dalgas reanalyzed baseline data from 2 recent exercise studies conducted by our groups 9,10 and collected data from a group of healthy people. We hypothesized that despite different neurologic pathologies, a stronger relationship between the 10mWT and the 6MWT would exist in patients with MS and patients with stroke as compared with healthy controls. METHODS Study Design and Subjects Data from 2 recently conducted exercise studies in patients with MS (n 38) 9 and patients with stroke (n 48) 10 were included in the present study. Details on inclusion and specific neurologic testing (Expanded Disability Status Scale and Fugl- Meyer) of patients with MS 9 and patients with stroke 10 and study designs are reported elsewhere. Only data from the baseline testing (performed before any intervention) were included in the present study. Furthermore, data from 46 healthy subjects were collected between May and October 2009. The included subjects fulfilled the following study criteria: able to transport themselves to testing; age greater than 18 years and signed informed consent; systolic/diastolic blood pressure less than 140/90mmHg; rheumatoid arthritis not restricting maximal performance; no dementia, alcoholism, or pacemaker treatment, or any serious medical comorbidities; and not pregnant. Standard Protocol Approvals, Registrations, and Patient Consents All 3 substudies were approved by the local scientific ethics committee and performed in accordance with the Helsinki Declaration 2. Written informed consent was obtained from all patients participating in the study. Evaluation of Walking Capacity The 6MWT was performed in accordance with the guidelines described in the American Thoracic Society statement. 11 The 6MWT is a feasible, valid, reproducible, and reliable measure in MS 8,12,13 and a feasible and reliable measure in patients with stroke. 5 Some methodologic differences existed between the 10mWT in the 2 clinical substudies as described in the following section. Patients with stroke. The patients with stroke performed the 10mWT 3 times at both comfortable and maximal speed essentially in accordance with the procedure described by Flansbjer et al. 4 A total distance of 14m was marked, and the subjects were timed over the middle distance, resulting in a flying start eliminating the acceleration and deceleration phase of walking. Time was measured by using photo cells. a Comfortable walking speed was represented by the average of 3 attempts at comfortable walking speed, while the maximal speed was represented by the best of the 3 maximal attempts to avoid tentative nonmaximal attempts or attempts influenced by fatigue in this category. Patients with MS. Patients with MS were instructed to perform a 10mWT in a wide corridor with 3 lines marking the distance to be walked (0, 10, and 12m). 14 The participants were instructed to walk (running not allowed) as fast as possible and to keep walking for a further 2 meters after passing the 10 meter marking. A standing start was applied, and time was measured with a handheld stopwatch when the front leg passed the starting and finishing lines. The best of 2 attempts was taken as the maximal walking speed. The 10mWT has shown good reliability in MS. 13 Healthy subjects. The healthy subjects performed the 10mWT with both a standing and a flying start as well as with maximal and comfortable speed to allow direct comparison with data from both patients with stroke and patients with MS. Statistics The main focus of the present study was to examine the relationship between the 10mWT and the 6MWT. In both walking tests, the time (10mWT) or distance (6MWT) was transformed to speed. Pairwise correlation analyses were performed for each of the 3 groups including the following variables: maximal 10mWT, comfortable 10mWT (only patients with stroke and healthy subjects), and 6MWT, and a correlation was considered significant for P.05. Data are presented as mean SD in tables. All statistical analyses were performed by using STATA, version 11.0. b RESULTS Demographic Variables Demographic data on the 3 groups of subjects are shown in table 1. The patients with stroke were significantly older and had a higher body mass index than the 2 other groups. Also, body weight in patients with stroke was higher than that in patients with MS and healthy subjects were taller than patients with MS. Table 1: Demographic Data Parameter Patients With MS Patients With Stroke Healthy Subjects n 38 (25F/13M) 48 (14F/34M) 46 (21F/25M) Weight (kg) 67.7 14.1 82.2 21.1* 75.3 14.2 Height (cm) 169.0 10.6 171.5 9.1 175.6 11.0* Age (y) 48.7 8.8 67.7 8.5 46.9 12.2 Body mass index (kg/m 2 ) 23.6 3.7 27.7 5.6 23.9 2.6 EDSS (MS, arbitrary units) 3.8 0.8 NA NA Fugl-Meyer (stroke, arbitrary units) NA 67.7 25.9 NA Time since diagnose (MS) (y) 7.2 5.5 NA NA Debut of symptoms (stroke) (y) NA 1.5 0.5 NA Working 16 of 22 3 of 45 ND NOTE. Data are given as mean SD. Abbreviations: EDSS, Expanded Disability Status Scale; F, female; M, male; NA, not applicable; ND, no data. *Significantly different from patients with MS, P.05. Significantly different from patients with MS and healthy subjects, P.05.

WALKING IN MULTIPLE SCLEROSIS AND STROKE, Dalgas 1169 Table 2: Short (10mWT) and Long (6MWT) Walk Tests in Patients With MS and Stroke and in Healthy Subjects 10mWT maximal (s) 10mWT comfortable (s) FS SS FS SS 6MWT (m) Healthy subjects 3.9 0.6 4.4 0.5 5.9 0.6 6.2 0.7 711 71 MS NT 7.3 2.9 NT NT 436 144 Stroke 10.9 7.8 NT 14.4 7.2 NT 292 117 NOTE. Data are given as mean SD. Abbreviations: FS, flying start; NT, not tested; SS, standing start. Correlations Between Walking Tests Data for walking tests for the 3 groups are presented in table 2. Both patients with MS and particularly patients with stroke had impaired walking function compared with healthy controls. As seen in figure 1, strong correlations were found between the performance during the 10mWT (maximal speed) and the 6MWT in patients with MS (r.95) and in patients with stroke (r.94), whereas only moderate correlations were found in healthy controls (r.69.70). To determine whether the correlations can be regarded as representing the same linear relationship in all groups, the values for walking speed in the 2 tests were depicted graphically (see fig 1). From figure 1, it is evident that patients with MS and patients with stroke show nearly the same linear relation between the 6MWT and the 10mWT, whereas the relation in healthy subjects deviates considerably from that in both these groups. The relationship between comfortable 10mWT and 6MWT was at a similar level in patients with stroke (r.91) (table 3), while the relationship was weak in healthy subjects (r.26, P.05) (see table 3). Comfortable walking speed was not measured in the patients with MS. DISCUSSION The main findings of this study are (1) strong correlations between walking speed in a 10mWT and a 6MWT in patients 6MWT velocity / m/s 2,5 2,0 1,5 1,0 0,5 0,0 0 1 2 3 4 10mWT velocity / m/s Stroke patients MS patients Healthy subjects Fig 1. Relation between the 10mWT (maximal speed) and the 6MWT in patients with stroke (r.94, P<.05), patients with MS (r.95, P<.05), and healthy subjects (r.69, P<.05). To allow direct comparison of 10mWT data (maximal speed) in patients with MS (standing start) to data from the patients with stroke (flying start), all individual data from patients with MS were corrected for the influence of the acceleration phase. The correction was based on observations from the healthy subjects in the present study who showed a difference of 11% between the 10mWT with and without flying start. Consequently, the obtained MS data were multiplied by 1.11. with walking disability due to stroke or MS; (2) strikingly similar best fit regression lines (10mWT vs 6MWT) of the 2 groups of patients despite differences in age, disease, and absolute level of walking ability; and (3) a notably weaker correlation between short and long walking tests in a group of healthy subjects as compared with patients with stroke and patients with MS. Relationship Between Walking Speed From Long and Short Walking Tests Table 3 summarizes results from previous studies that have reported correlation coefficients between walking speed obtained from long and short walking tests in patients with neurologic disorders and in healthy subjects. In general, the correlation coefficients between walking tests are very high in patients with MS and patients with stroke regardless of whether comfortable or maximal speed is measured in the short walk test. This indicates that the speed during the 6MWT and the 10mWT reflects the same aspects of walking capacity in these patients, probably because the neural impairments are the most significant determinant of walking speed regardless of the length of the test. In healthy controls, the correlations between the speed of the walking tests were less pronounced, perhaps indicating that various other factors (cardiovascular and muscular) played a larger role in the different tests. In agreement with our interpretation, Dobkin 6 suggested that the long and short walking tests could be considered redundant measures because the absolute values for average speed were nearly identical in the 2 tests when performed on patients with stroke. Similarly, very high correlations between 10mWT (both comfortable and maximal speed) and 6MWT have been found in patients with spinal cord injury. On the basis of this, van Hedel et al 18 concluded that the 6MWT does not provide additional information about the walking capacity compared with the 10mWT in this group of patients. Our data (see table 2) and most other studies (see table 3) have shown that the absolute values for walking speed during short walking tests performed at comfortable speed were different from the speed during the 6MWT. The 6MWT speed is usually within the range between comfortable and maximal speed measured with short walking tests. This indicates that patients with MS and patients with stroke, as well as healthy subjects, employ a pacing strategy during the 6MWT to minimize the occurrence of fatigue, corresponding to earlier findings. 12 In light of the strong correlation coefficients, it should be possible to obtain a good prediction of the 6MWT performance from the short walking tests. However, the finding of similar high correlation coefficients between long and short walking tests in many studies does not ensure that the correlations follow the same general equation in all studies. Because no consensus exists regarding the short walking test methodology (standing vs flying start, different distances, maximal vs comfortable speed, etc), it is probably not possible to generate 1 unique prediction equation. Consensus on walking test meth-

1170 WALKING IN MULTIPLE SCLEROSIS AND STROKE, Dalgas Table 3: Walking Speed and Correlations Between Short and Long Walking Tests in Neurologic Patients and in Healthy Subjects Study Population 6MWT Speed (m/s) Short Walk Test Speed (m/s) Correlation (r) 6MWT vs Short Walk Test Speed Comfortable Maximal Comfortable Maximal Stroke Kelly et al 15 Recent stroke (n 17) 0.84 0.71 1.03 0.91 0.89 Flansbjer et al 4 Chronic stroke (n 50) 1.07 1.11 0.89 0.94 1.3 1.4 0.84 0.89 0.94 0.95 Tang et al 16 Chronic stroke (n 30 33) 0.95 0.84 (5mPP) 1.15 (5mPP) 0.79 0.82 Patterson et al 17 Chronic stroke (n 74) 0.60 0.51 (9mSS) ND 0.88 ND Eng et al 5 Chronic stroke (n 25) 0.74 0.8 (4mFS) ND 0.92 ND Present study Chronic stroke (n 48) 0.81 0.69 0.92 0.91 0.94 MS Gjibels et al 8 MS (all, n 50) 1.14 1.03 (7.6mSS) 0.88 Gjibels et al 8 MS (mild, n 29) 1.40 1.39 (7.6mSS) 0.65 Gjibels et al 8 MS (moderate, n 21) 0.79 0.75 (7.6mSS) 0.89 Present study MS (n 38) 1.21 1.36 (10mSS) 0.95 Other neurologic diseases van Hedel et al 18 Incomplete SCI (n 18) 1.11 0.79 1.10 0.93 0.93 Kim et al 19 Incomplete SCI (n 20) 0.53 0.55 (4mFS) ND 0.98 ND Healthy subjects Simonsick et al 3 Healthy, aged (n 50) 1.26 ND 1.64 (20mSS) ND 0.65 0.73 Present study Healthy (n 46) 1.98 1.72 2.78 0.26 (NS) 0.69 NOTE. 6MWT speed converted from reported 6MWT distance. Short test walking speed is from 10mWT with flying start unless otherwise noted. Abbreviations: 4mFS, 4 meter walk test with flying start; 5mPP, 5 meter walk test on a power plate; 9mSS, 9 meter walk test with standing start; 7.6mSS, 7.6 meter walk test with standing start; 10mSS, 10 meter walk test with standing start; 20mSS, 20 meter walk test with standing start; ND, no data; NS, nonsignificant; SCI, spinal cord injury. odology when evaluating neurologic (and other) patients is therefore warranted. Furthermore, it is likely that some differences in the relation between short and long walking tests exist because of differences in disease type or disability level as suggested by Gijbels et al, 8 who found a weaker correlation between the 10mWT (maximal speed) and the 6MWT in patients mildly affected with MS as compared with those moderately affected (r.65 vs r.89, data obtained through written communication with D. Gijbels, November 2010), indicating that disability level may influence the relation. Altogether, the findings suggest that a short walking test may be sufficient in clinical or research settings, when the objective is to assess the relative degree of impairment on walking speed in patients with neurologic dysfunction and that adding a 6MWT will provide only little additional information on walking speed. In other studies, the 6MWT has been used to examine variables in addition to the covered distance (or average speed). In a group of patients with stroke, Sibley et al 20,21 found that walking speed was gradually reduced over time when the 6MWT results were examined in intervals of 2 minutes or less. Furthermore, changes in walking symmetry and rest periods over the course of the tests were observed, which may reflect the development of fatigue. Therefore, the 6MWT may still be a relevant test to consider when evaluating walking capacity in neurologic patients, but additional data on speed changes over time, rests, and walking pattern should be gathered to extract a more complete evaluation. In our study, however, we recorded data only on total distance and average speed over the 6MWT. Influence of Short Test Methodology Based on the studies summarized in table 3, it seems that correlations are very similar between the 6MWT and short tests performed at either maximal or comfortable speed in patients with stroke. 5,16 Data from our patients with stroke support this (r.94 vs r.91), and both a maximal and a comfortable speed short test would, therefore, be expected to give a good prediction of the 6MWT performance. Also, the starting procedure in short walk tests seems to have a minor influence on the predictive value of the short walk test on 6MWT performance. Furthermore, short test distances vary from 4 to 20 meters, but no clear influence on the correlations between short and long test walking function is evident. Walking Tests and Physical Capacity Because of the nature of the maximal 10mWT (a brief and maximal effort), this test would be expected to be more strongly associated with lower body muscle strength than the 6MWT, which, on the other hand, would be expected to be more strongly associated with the aerobic capacity because of the cardiorespiratory strain of completing this test. However, data from our patients with stroke (published elsewhere 10 ) show only a weak correlation (r.31, P.05) between isometric paretic knee extensor strength and maximal walking speed, suggesting that other factors, such as the level of neuromotor control, also limit walking function. On the other hand, a number of other studies have shown moderate to strong correlations between lower body muscle strength and maximal walking speed. Nadeau et al 22 reported a strong correlation (r.88) between dynamic hip flexor strength in the paretic leg and maximal walking speed, whereas Hsu et al 23 found a weak correlation between dynamic paretic hip flexor strength and maximal walking speed (r.59) and a moderate correlation between dynamic paretic knee extensor strength and maximal walking speed (r.68). Bohannon 24 reported strong correlations for isometric muscle strength of both hip flexors and knee extensors in the paretic leg (r.81 and.82, respectively). However, the relation between strength and maximal walking speed is probably not linear. In most healthy subjects, only a fraction of the maximal force-generating capacity is used in the muscles during walking, and it is possible that strength will become a limiting factor for walking only when below a certain

WALKING IN MULTIPLE SCLEROSIS AND STROKE, Dalgas 1171 limit, as indicated by the findings in healthy elderly subjects. 25,26 Regarding the relationship between the 6MWT and the peak oxygen consumption (VO 2 peak), studies have generally found a moderate relationship in patients with cardiorespiratory diseases (for review, see Solway et al 2 ). Data from our patients with stroke (published elsewhere 10 ) support this by showing a weak correlation (r.58, P.05) between VO 2 peak and 6MWT distance, again suggesting that there are other factors in addition to aerobic capacity that limit walking function. Correlations between the 6MWT and VO 2 peak from other studies evaluating patients with stroke are inconsistent with studies showing no, 27 weak (r.4.56), 16,28 moderate (r.6.64), 17,29 or strong (r.84) 15 correlations. A number of factors could explain the lack of a strong correlation between VO 2 peak and 6MWT in neurologic patients. First, the neurologically induced impairment may dominate over the cardiovascular deficit even though many patients with stroke have a low cardiovascular fitness level, which is also the case in the present group of patients with stroke. Second, the neurologic impairment affects the economy of walking to a varying degree in patients with stroke, 30 which introduces considerable variation in the relation between VO 2 peak and walking distance even if it is assumed that all patients were able to achieve the same relative level of cardiovascular stress during a long walking test. Third, the relationship between walking speed and oxygen uptake is curvilinear, 31 which would tend to lower the correlation between VO 2 peak and walking distance in both healthy subjects and groups with impaired walking capacity when employing a linear correlation model. Study Limitations There are a number of limitations of the present study. First, both patients with MS and patients with stroke are selected groups not necessarily representing patients with MS and patients with stroke in general. Therefore, the relationships between long and short walking tests might look different in both more and less disabled patients. Second, the healthy subjects in this study were not matched with both groups of patients, and, consequently, the healthy subjects and the patients with MS were significantly younger than the group of patients with stroke. Third, this study did not examine the responsiveness of the 2 tests, and the 6MWT, therefore, might be more responsive than the 10mWT to certain interventions and in certain groups of neurologic patients. This aspect should be evaluated in future studies. Finally, some minor methodologic differences existed between the applied short walking test in patients with MS and patients with stroke that may have a small impact on the results. 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