Walking Capacity in Mild to Moderate Parkinson s Disease

ORIGINAL ARTICLE Walking Capacity in Mild to Moderate Parkinson s Disease Colleen G. Canning, PhD, Louise Ada, PhD, Justin J. Johnson, MPhty, Stephanie McWhirter, MPhty ABSTRACT. Canning CG, Ada L, Johnson JJ, McWhirter WHEN PEOPLE WITH Parkinson s disease (PD) walk a S. Walking capacity in mild to moderate Parkinson s disease. short distance, they typically show reduced velocity of Arch Phys Med Rehabil 2006;87:371-5. walking associated with reduced stride length and a compensatory increase in cadence. These abnormalities are thought to Objectives: To examine walking capacity in people with be because of hypokinesia, that is, reduced speed and amplitude of movement, which is a major motor impairment ob- mild to moderate Parkinson s disease (PD), specifically, to determine whether spatiotemporal abnormalities observed when people served in PD. 1 Hypokinesia is also known to affect turning with PD walk over short distances are exacerbated over longer ability, 2 with 360 turns in standing characterized by slowness, distances and whether these and other motor impairments affect walking capacity. and multiple short steps. 3 Walking capacity is determined as the distance a person is capable of walking over a longer period Design: Descriptive study comparing participants with PD of time, typically for 6 minutes, usually back and forth in a and healthy participants. corridor known as the 6-minute walk test (6MWT). Although Setting: University laboratory. reduced walking capacity has been reported in people with Participants: Sixteen participants (mean age, 65y) with PD, 4 it is not known whether reduced walking capacity is mild to moderate PD (stages 1 3 of the Hoehn and Yahr rating caused by specific PD impairments (eg, hypokinesia during scale) were tested on medication. Twenty-two healthy participants (mean age, 66y) formed a control group. walking and/or turning and reduced automaticity of walking) or nonspecific impairments such as reduced muscle strength. Interventions: Not applicable. Walking capacity in people with PD has only been reported Main Outcome Measures: Walking capacity was quantified in 2 previous studies. Garber and Friedman 4 reported a mean as the distance walked in the 6-minute walk test (6MWT), 6-minute walk distance (6MWD) of 395m in a group of mild to hypokinesia during walking was quantified as fast-as-possible velocity over 8m, hypokinesia during turning was quan- moderately affected subjects aged in their sixties. This distance is only 42% of their predicted distance based on normative tified as the time taken to complete a 360 turn in standing, values for age, sex, height, and weight. 5 In contrast, Schenkman et al 3 reported a mean 6MWD of 461m in a group of automaticity was quantified as velocity during dual-task walking expressed as a percentage of velocity during single-task people with mild to moderate PD, which would be considered walking over 8m, and muscle strength was quantified as peak close to normative limits for their average age of 74 years. The isometric knee extensor torque. issue of which impairments determine walking capacity in Results: The PD group covered less distance (P.01) in the people with PD needs to be addressed. Although the contribution of a number of physiologic and psychologic factors to 6MWT than the control group. Although both groups recorded similar fast-as-possible walking velocities, the PD group walking capacity has been studied in the elderly population, 6-9 walked at only 76% of their fast-as-possible velocity during the the contribution of motor impairment(s) to walking capacity in 6MWT compared with 84% for the control group (P.002). In people with PD has not been investigated. It has been shown in the PD group, 94% of the variance in walking capacity was a group of active older people that walking velocity is remarkably stable from minute to minute throughout the 6MWT. 6 accounted for by hypokinesia during walking and turning as well as strength (P.001). Given the instability of motor performance associated with PD, Conclusions: Even when people with PD are capable of it may be that spatiotemporal variables of walking deteriorate walking at velocities comparable to healthy controls, they do when people with PD perform the 6MWT and such deterioration could underlie reduced walking capacity. Determining the not sustain this velocity over longer distances. Training that targets high velocities warrants investigation as a remediation most significant impairments contributing to walking capacity technique. in people with PD has the potential to direct rehabilitation Key Words: Gait; Hypokinesia; Parkinson disease; Rehabilitation; Walking. strategies intended to improve walking capacity at the most appropriate target. 2006 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and whether spatiotemporal abnormalities typically observed dur- Therefore, the overall aim of this study was to determine Rehabilitation ing walking over short distances in people with PD are exacerbated when walking over longer distances because this could limit walking capacity. Specifically, in a group of people with mild to moderate PD, we aimed to address the following questions: (1) Is walking capacity (measured as distance From the School of Physiotherapy, University of Sydney, Lidcombe, NSW, walked in the 6MWT) reduced compared with normative capacity? (2) Is comfortable walking velocity (measured over a Australia. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the author(s) or upon any short distance) maintained throughout the test of walking capacity? (3) Are abnormalities of velocity, stride length, and organization with which the author(s) is/are associated. Reprint requests to Colleen G. Canning, PhD, School of Physiotherapy, Faculty of cadence exacerbated over time during the test of walking Health Sciences, University of Sydney, PO Box 170, Lidcombe, NSW 1825, Australia, e-mail: C.Canning@fhs.usyd.edu.au. capacity? and (4) Which motor impairments (ie, hypokinesia 0003-9993/06/8703-10307$32.00/0 during walking and turning, reduced automaticity of walking or doi:10.1016/j.apmr.2005.11.021 reduced muscle strength) contribute to walking capacity? 371

372 WALKING CAPACITY IN PARKINSON S DISEASE, Canning METHODS Participants A convenience sample of 16 volunteers with mild to moderate idiopathic PD aged between 52 and 78 years (mean standard deviation [SD], 65 7y) participated in the study. Participants were included in the study if their disease severity on the Hoehn and Yahr rating scale 10 was from stages 1 through 3 inclusive and they were able to walk for 6 minutes unaided. They had been diagnosed with PD, on average 7 years previously, and all but 1 participant was on levodopa medication. Participants were excluded from the study if they had a fluctuating response to levodopa; suffered from disabling dyskinesias; were cognitively impaired (indicated by a score of 24 on the Mini-Mental State Examination 11 ); or had any other significant neurologic, cardiovascular, or musculoskeletal condition that could affect their walking. A convenience sample of 22 healthy participants of a similar age (mean, 66 7y) and without any significant neurologic, cardiovascular, or musculoskeletal problems were recruited from the local community service and sporting organizations to form a comparison group. The demographic characteristics of the participants are presented in table 1. Procedures The experimental procedures were approved by the University of Sydney Human Research Ethics Committee, and all participants gave informed consent before data collection. All PD participants were tested approximately 1 hour after taking their usual PD medication. Four motor impairments likely to contribute to walking capacity were measured: hypokinesia during walking, hypokinesia during turning, automaticity, and muscle strength. Measurements of hypokinesia during turning and muscle strength were conducted first, followed by hypokinesia and automaticity while walking short distances (8m). The final test was measurement of walking capacity over a longer distance using the 6MWT. Hypokinesia during turning was tested while participants made 360 turns in standing. 3 The mean time taken and the number of steps for 6 trials (3 in each direction) were calculated. Because time taken to turn correlated significantly with Table 1: Demographic Details of Participants Variable PD (n 16) Control (n 22) Age (y) 65.0 6.9 66.3 6.6.56 Sex (men/women) 13/3 16/6 NA Height (m) 1.70 0.13 1.73 0.07.44 BMI (kg/m 2 ) 25.3 4.1 24.0 3.1.30 Hoehn and Yahr stage (range, 1 5) 2.4 0.5 NA NA Disease duration (y) 7.2 5.0 NA NA MMSE (range, 0 30) 28.3 1.3 NA NA UPDRS motor exam (range, 0 108) 30.8 8.9 NA NA Physical activity* (h/wk) 5.01 3.46 8.24 4.37.02 NOTE. Values are mean SD unless otherwise indicated. The range of scores possible for each test is shown. Abbreviations: BMI, body mass index; MMSE, Mini-Mental State Examination; NA, not applicable; UPDRS, Unified Parkinson s Disease Rating Scale. 25 *Physical activity score is the time engaged in physical activities over and above everyday functional activities. Significant difference at P.05 (t test for independent samples). P the number of steps (r.85, P.001), time taken was used to quantify hypokinesia during turning. Isometric quadriceps muscle strength was measured with a Cybex Orthotron dynamometer a by using the protocol described by Amundsen. 12 Participants sat with the knee fixed at 60 of flexion. They performed 3 maximum isometric contractions on each leg, with a 1-minute rest period between each contraction. The peak measurement was recorded for each leg and averaged to give a mean peak isometric knee extensor torque (in Nm). The 8-meter walk test (8MWT) and 6MWT were conducted by using a GAITRite mat b to measure spatiotemporal gait variables. The 8MWTs were performed over a 14-m walkway with the 8-m GAITRite mat in the middle to avoid collecting data during acceleration and deceleration. Participants were required to perform the 8MWT under 3 conditions: (1) walking at their comfortable speed (single comfortable), (2) walking at their comfortable speed while performing a color classification task (dual comfortable), and (3) walking as fast as possible (fast as possible). The color classification task 13 involved participants listening to a prerecorded audiotape and answering yes when they heard the word red and no when they heard the word blue. The audiotape presented the words red and blue in random order at 3-second intervals. Two practice trials were performed for each condition of walking before collecting 1 trial for analysis. Hypokinesia during walking was quantified as the walking velocity recorded under the fast-as-possible condition. To quantify automaticity, the walking velocity under the dual-comfortable condition was expressed as a percentage of the walking velocity under the single-comfortable condition, known as the automaticity index. 14 The 6MWT 15 was used to determine walking capacity as well as to measure spatiotemporal variables of walking over a longer distance. The 8-m GAITRite mat was placed in the middle of a 30-m walkway, and participants were required to walk back and forth along the 30-m walkway for 6 minutes. Participants were instructed to walk as far as possible in the 6 minutes and were provided with standardized encouragement every minute, for example, You are doing well, you have 5 minutes to go. Total distance walked during the test was recorded to the nearest tenth of a meter and the 6-minute average walking velocity was calculated by dividing the total distance walked by the total number of seconds in the test. Walking velocity, stride length, and cadence were collected the first time the subject walked over the GAITRite mat in each of the 6 minutes of the test. To reflect the intensity of exercise performed, heart rate, breathlessness, and leg muscle fatigue were recorded on immediate completion of the test. Heart rate was recorded by using a Polar heart rate monitor. c Breathlessness and leg muscle fatigue were evaluated by using the Borg 10-point Rating of Perceived Exertion scale. 16 Data Analysis Data are reported as means and SDs. Determination of significant differences between groups was conducted with t tests for independent samples. Repeated-measures analysis of variance with trend analysis was used to analyze the minuteby-minute data for velocity, stride length, and cadence throughout the 6MWT. To determine the contribution of hypokinesia, automaticity of walking, and muscle strength to walking capacity, standard multiple linear regression analysis was performed. This analysis returns the proportion of the variance in walking capacity attributable to the variables entered in total as well as the proportion of variance attributable to each of the variables separately (as squared semipartial correlations) and also tests these to determine if they are significantly different

WALKING CAPACITY IN PARKINSON S DISEASE, Canning 373 Table 2: Results of Tests of Motor Impairments and Walking Tests PD Control t P 8MWT Velocity: single comfortable (m/s) 1.31 0.18 1.50 0.22 2.82.008* Velocity: dual comfortable (m/s) 1.26 0.19 1.50 0.23 3.40.002* Motor impairments Hypokinesia: walking (velocity fast as possible) (m/s) 2.01 0.43 2.05 0.24 0.38.70 Hypokinesia: turning (s) 2.9 1.3 2.1 0.5 2.63.01* Automaticity (% velocity-single/velocity-dual) 96 6 100 5 2.31.03* Strength (Nm) 162 40 158 44 0.28.78 6MWT Distance (m) 546 103 619 69 2.63.01* Velocity (m/s) 1.52 0.28 1.72 0.19 2.63.01* Heart rate (beats/min) 117 27 117 22 0.02.98 Shortness of breath (range, 0 10) 2.5 1.4 2.0 0.9 1.33.19 Leg fatigue (range, 0 10) 2.8 2.1 1.2 1.1 3.06.004* NOTE. Values are mean SD. Two PD participants were on ß-blocker medication and therefore were removed from the analysis of heart rate. *Significant difference at P.05 (t test for independent samples). from zero. Significance was set at equal to.05 for all statistical tests. RESULTS Is Walking Capacity Reduced Compared With Normative Capacity? The PD group covered significantly less distance in the 6MWT than the control group (table 2). The walking performed during the test produced heart rates that were on average 75% of predicted maximum heart rate, and this did not differ between groups. Although both groups reported only light to moderate levels of breathlessness, the PD group reported moderate leg fatigue at the end of the test that was significantly greater than the very slight leg fatigue reported by the control group. Is Comfortable Walking Velocity (Over a Short Distance) Maintained Throughout the Test of Walking Capacity? Comfortable walking velocity over a short distance for the PD group was significantly slower than for the control group (see table 2). Nevertheless, both groups were able to exceed their comfortable walking velocity during the 6MWT. The PD group produced an average walking velocity during the test of 115% 15% of their comfortable velocity compared with 116% 15% for the control group (t 36.13, P.90). In contrast, fast-as-possible walking velocity over a short distance for the PD group was comparable to the control group. However, the PD group walked at only 76% 5% of their fast-as-possible velocity during the 6MWT compared with 84% 7% for the control group (t 36 4.08, P.001). Are Abnormalities of Velocity, Stride Length, and Cadence Exacerbated Over Time During the Test of Walking Capacity? The results for velocity, stride length, and cadence recorded within each minute of the 6MWT are shown in figure 1. The PD group maintained a lower velocity (F 1,36 4.59, P.04) and stride length (F 1,36 7.45, P.01) than the control group throughout the test, but there was no difference between groups in cadence (F 1,36.04, P.84). Examination of the spatiotemporal variables over time shows that the pattern of results for both groups is similar. With respect to velocity, the velocity drops over the first 2 to 4 minutes and then increases again toward the end of the test. For example, velocity for the PD group varied from a maximum of 1.74m/s in the first minute, reducing to 1.61m/s in the fourth minute and increasing to 1.68m/s in the last minute. For the control group, the maximum velocity of 1.87m/s was recorded in both the first and the last minute, and the minimum velocity of 1.81m/s was recorded in the fourth minute. This pattern of results was reflected by a significant quadratic trend component in velocity measures over time (F 1,36 37.38, P.001), with both groups following the same trend (ie, no significant groupby-time interaction was observed [F 1,36 1.72, P.20]). The same pattern of results was observed for stride length, with both groups showing a significant quadratic trend in their data (F 1,36 34.59, P.001), with no significant group-by-time interaction (F 1,36 2.29, P.14). Similarly, for cadence, a significant quadratic trend (F 1,36 15.41, P.001) was observed, with no significant group-by-time interaction (F 1,36 0.38, P.54). Which Motor Impairments Contribute to Walking Capacity in PD? Simple linear regression analysis showed that for the PD group, hypokinesia walking (r.96, R 2.92, P.001), hypokinesia turning (r.61, R 2.38, P.01), and strength (r.55, R 2.30, P.03) correlated significantly with 6MWD, whereas automaticity of walking did not (r.07, R 2.01, P.79). Therefore, hypokinesia walking, hypokinesia turning, and strength were entered into the standard multiple linear regression analysis. Hypokinesia walking, hypokinesia turning, and strength combined accounted for 94% of the variance seen in the 6MWD (R 2.94, P.001), with hypokinesia walking making a significant independent contribution to the variance in 6MWD (R 2.48, P.001). The independent contributions of hypokinesia turning (R 2.001, P.63) and strength (R 2.007, P.28) were not significant. DISCUSSION The people with mild to moderate PD in this study did not sustain sufficiently high velocities of walking during the 6MWT to cover the same distance achieved by the control group. Despite this, they did walk considerably further in the 6MWT than has been previously reported for people with PD.

374 WALKING CAPACITY IN PARKINSON S DISEASE, Canning A Velocity (m/s) B Stride Length (m) C Cadence (steps/min) 2.2 2.0 1.8 1.6 1.4 1.2 1.0 0.8 0.6 0.4 0.2 0.0 2.0 1.8 1.6 1.4 1.2 1.0 0.8 0.6 0.4 0.2 0.0 140 120 100 80 60 40 20 0 1 2 3 4 5 6 Minutes Fig 1. Mean (SD) for (A) velocity, (B) stride length, and (C) cadence for PD ( ) and control ( ) participants during each minute of the 6MWT. Their mean distance of 546m is more than 150m further than that recorded by Garber and Friedman 4 and 75m further than the older participants in the study by Schenkman et al. 3 Although all studies tested participants with similar disease severity, some of the discrepancy in findings is likely to be because of the testing protocols used. Schenkman 3 instructed participants to walk at comfortable pace for 6 minutes over a track of unspecified distance, whereas Garber and Friedman 4 instructed participants to walk as fast as possible over a short 12-m track, necessitating a large number of turns. The Parkinson s group participants had no difficulty in exceeding their comfortable walking velocity throughout the 6MWT, but despite being able to walk as fast as the control group over a short distance, they did not match the velocities of the control participants over the longer test. It is interesting to speculate on what factors might explain this difficulty in sustaining high velocities of walking over time. If more attentional resources are required for people with PD to sustain high velocities, then it would be expected that abnormalities of velocity, stride length, and cadence would be exacerbated as 6MWT continues. However, the results of the trend analysis showed that although the Parkinson s group walked slower than controls throughout the test, they showed no deterioration in spatiotemporal walking parameters during the test. Nevertheless, throughout the test, the Parkinson s group walked with lower velocity and stride length but a similar cadence to the control group, showing the typical spatiotemporal abnormalities of walking associated with PD. Another way to consider the demand for attentional resources contributing to difficulty in sustaining high velocities is to analyze the contribution of automaticity to walking capacity. Although the Parkinson s group showed some loss of automaticity of walking in agreement with other studies, 17-19 there was no significant correlation between automaticity index and walking capacity in this group. This finding would suggest that reduced automaticity of walking determined at comfortable speed is not the major contributor to reduced walking capacity in people with mild to moderate PD. It may be the case, however, that the attentional demands required to sustain faster walking speeds are considerably greater for people with PD than for healthy participants. However, because we did not test automaticity of walking at fast-as-possible speed, this is a question that needs to be addressed in future research. It is possible that people with PD default to a velocity of walking that can be maintained relatively automatically (ie, with little attentional resources), and this could explain why they do not use the higher speeds of which they are capable. The results of the simple and multiple linear regression analyses shed further light on the impairments that might contribute to reduced walking capacity in people with PD. Overwhelmingly, more than 90% of the variance in walking capacity is explained by hypokinesia during walking in the Parkinson s group. This finding highlights the impact that slowness of movement has on walking capacity. Although slowness in turning also contributes in these mild to moderately affected people, the velocity of walking is the largest and only independent contributor to walking capacity. Although this finding is not altogether unexpected, it is surprising that none of the other variables tested made an independent contribution to walking capacity. If people with PD routinely use lower walking velocities to walk longer distances, this is likely to result in deconditioning over time. The Parkinson s group recorded similar heart rate and breathlessness scores to the controls along with greater fatigue while covering less distance in the 6MWT. This suggests that reduced walking capacity in PD is, at least in part, attributable to deconditioning and raises the question of whether the walking capacity of the participants was related to the amount of regular physical activity they performed. From the demographic variables investigated, the only variable on which the control group differed from the Parkinson s group was level of physical activity. Compared with the Parkinson s group, the control group spent an extra 3 hours a week engaged in physical activity over and above everyday functional activ-

WALKING CAPACITY IN PARKINSON S DISEASE, Canning 375 ities. Furthermore, post hoc Pearson product moment correlation analysis showed that the amount of regular physical activity correlated significantly with 6MWD in the PD group (r.56, R 2.32, P.02). These findings suggest that the reduced walking capacity in the Parkinson s group is associated with reduced physical activity. Furthermore, this finding is consistent with previous work showing greater regular physical activity is associated with greater exercise capacity measured on a bicycle ergometer in people with mild to moderate PD. 20 The people with PD in this study represent a convenience sample of mild to moderately affected subjects. Therefore, the results cannot be generalized to people more severely affected. A further limitation of the study is that because we did not test participants off medication, we cannot draw conclusions about the contribution of impairments to walking capacity in the unmedicated state. CONCLUSIONS Overall, the results of this study show that the major impairment limiting walking capacity in people with mild to moderate PD is hypokinesia. This is despite a demonstrated ability to walk as fast as control subjects over short distances. In addition, consistently walking at lower velocities is likely to result in deconditioning and further reduce walking capacity. Therefore, interventions aimed at improving walking capacity in this group should logically target sustaining walking at fast speeds. Such interventions could simultaneously address the primary motor control impairment of hypokinesia while improving exercise capacity. This may be achieved by incorporating visual or attentional cueing strategies to maintain stride length 1,21 and/or the use of a treadmill to cue speed. 22-24 Future research is planned to address the effectiveness of strategies designed to sustain walking at fast speeds in randomized controlled trials. 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