Archives of Physical Medicine and Rehabilitation
Volume 89, Issue 11 , Pages 2041-2047, November 2008

Does Treadmill Exercise Improve Performance of Cognitive or Upper-Extremity Tasks in People With Chronic Stroke? A Randomized Cross-Over Trial

  • Michelle Ploughman, PhD, PT

      Affiliations

    • Eastern Health, L.A. Miller Centre, St. John's, NL, Canada
    • Division of BioMedical Science, Faculty of Medicine, Memorial University, St. John's, NL, Canada
    • Corresponding Author InformationCorrespondence to Michelle Ploughman, PhD, PT, Eastern Health, L.A. Miller Centre, 100 Forest Rd, St. John's, NL, Canada, A1A 1E5
    • ,
  • Jason McCarthy, MD

      Affiliations

    • Eastern Health, L.A. Miller Centre, St. John's, NL, Canada
    • ,
  • Melissa Bossé, MD

      Affiliations

    • Division of BioMedical Science, Faculty of Medicine, Memorial University, St. John's, NL, Canada
    • ,
  • Heather J. Sullivan, BKin

      Affiliations

    • Eastern Health, L.A. Miller Centre, St. John's, NL, Canada
    • ,
  • Dale Corbett, PhD

      Affiliations

    • Division of BioMedical Science, Faculty of Medicine, Memorial University, St. John's, NL, Canada

Article Outline

Abstract 

Ploughman M, McCarthy J, Bossé M, Sullivan HJ, Corbett D. Does treadmill exercise improve performance of cognitive or upper-extremity tasks in people with chronic stroke? A randomized cross-over trial.

Objective

To determine whether acute exercise, using a body-weight–supported treadmill, improves performance on subsequent cognitive tests or an upper-extremity task in people with stroke.

Design

The study was a within-subject, cross-over design in which 21 subjects received, randomly, 2 different testing sequences separated by an interval of 7 to 10 days.

Setting

Outpatient department of a rehabilitation hospital.

Participants

Of 72 potential participants in the convenience sample, 21 people with chronic stroke completed the study. They were 0.5 to 5 years after only 1 documented stroke, were able to walk with or without a cane, were able to grasp with the affected hand, and scored more than 24 on the Mini-Mental State Examination.

Interventions

One session of body-weight-supported treadmill walking for 20 minutes at 70% of estimated heart rate reserve or level 13 on the Borg rating of perceived exertion scale. The control condition consisted of a 20-minute review of a home exercise program with a physiotherapist.

Main Outcome Measures

Cognitive tests included Trail Making Tests Parts A and B, Symbol Digit Substitution Test, and Paced Auditory Serial Addition Test. The Action Research Arm Test (ARAT) measured hemiplegic upper-extremity motor skill.

Results

Treadmill exercise improved movement of the hemiplegic upper extremity (P=.04) but not cognitive performance. The improvement in the ARAT occurred without a change in strength (measured by grip strength) and was negatively correlated with maximum treadmill speed (R2=.20; P=.04).

Conclusions

These findings suggest that acute treadmill exercise improves subsequent skilled movement of the hemiplegic upper extremity that seems unrelated to attention, visuomotor processing, or strength. The etiology and duration of this enhancing effect are worth further study. The existence of an exercise-cognition relationship in people with stroke is an intriguing area of future research.

Key Words: Cognition, Hemiplegia, Physical therapy techniques, Rehabilitation

List of Abbreviations: ANOVA, analysis of variance, ARAT, Action Research Arm Test, BDNF, brain-derived neurotrophic factor, BWSTT, body-weight-supported treadmill training, CI, confidence interval, MCID, minimal clinically important difference, RPE, rating of perceived exertion, TMT-A, Trail Making Test Part A, TMT-B, Trail Making Test Part B

 

MOST PEOPLE WHO SURVIVE stroke have enduring motor, cognitive, and language deficits that affect productivity and quality of life.1 A growing body of evidence suggests that exercise influences executive control,2 which could potentiate relearning and recovery from brain injury. In clinical studies, both acute (15–40min)3, 4, 5, 6 and prolonged2, 7, 8, 9, 10, 11, 12 running or cycling exercise increases cognitive performance. Unfortunately, patients with stroke engage in only a few minutes each day of exercise intense enough to induce a training effect.13 For patients with mobility impairments, the BWSTT apparatus permits safe and effective cardiovascular and gait training14 and is increasingly being used in clinical practice.15

Currently there are 4 hypotheses explaining how exercise affects executive control. Exercise increases cerebral blood volume16 and angiogenesis17 in areas crucial for task performance. Pereira et al16 found that 3 months of fitness training increased cerebral blood volume and improved verbal learning and memory in middle-aged participants. The second hypothesis suggests that acute exercise increases brain neurotransmitters such as dopamine and norepinephrine, facilitating information processing, also known as the arousal hypothesis.4, 18 Increased levels of arousal measured by brain-evoked potentials have been measured in persons exercising at 70% of their maximum oxygen capacity for 30 minutes.3, 6 The third hypothesis suggests that exercise upregulates neurotrophins such as BDNF and insulin-like growth factor I19 that support dendritic branching and synaptic plasticity in the adult brain (for review see Schinder and Poo20). A short burst of high-impact running results in sustained increases in serum BDNF that is associated with improved learning.5 Finally, the fourth hypothesis suggests that exercise improves mood and alleviates depression, which may also affect cognitive function.18, 21

We do not know whether exercise influences executive functioning in people with brain injury. We also do not know whether a single episode of exercise or more prolonged training is required to produce cognitive effects. As a starting point, we hypothesize that 1 episode of moderate exercise performed with BWSTT, by improving attention, can also enhance performance in seemingly unrelated cognitive and motor tasks. If this is the case, supported treadmill exercise may be used to optimize performance during rehabilitative training sessions in psychology, speech language pathology, occupational therapy, and physiotherapy.

Our objectives were to determine whether this acute exercise priming phenomenon exists in people with stroke, and to determine whether this phenomenon is specific to cognitive or motor tasks.

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Methods 

Subjects 

Seventy-two subjects who were 6 months to 5 years poststroke were sourced from outpatient records from June 2005 to January 2007. Inclusion criteria were (1) at least grade 2 of 7 levels of motor control on the Chedoke-McMaster Impairment Inventory for Arm and Hand,22 (2) a score of greater than 24 on the Mini-Mental State Examintation,23 (3) older than 16 years of age, (4) only 1 documented stroke event, (5) not receiving active rehabilitation intervention, and (6) able to walk with or without a cane. The attending physician assessed subjects' medical status to determine whether treadmill exercise was contraindicated (eg, heart failure, unstable angina). Twenty-one subjects attended the on-site screening assessment and went on to complete the study (fig 1). These subjects provided written consent and were randomized to testing sequence (A–B or B–A). We oriented subjects to the body-weight–supported treadmill apparatus and upper-extremity task; however, they were not aware of the study's hypothesis or testing sequence. The study was approved by the Memorial University Human Investigations Committee according to Tri-Council Policy Guidelines.

Study Design 

The study was a within-subject design with 21 subjects receiving 2 different testing sequences (session A and B, each divided into 2 parts) separated by an interval of 7 to 10 days (fig 2). Order of participation in the testing sequences was randomly assigned to minimize the effect of order. Evaluators were aware of testing sequence. We aimed to detect a difference of 3 points on the ARAT, knowing ARAT SD is equal to 3.24, 25 Power analysis, with the ARAT as the main outcome measure, indicated 16 subjects were required in each group (32 in total) to achieve .80 power at α equal to .05.26 We added 9 more subjects to allow for attrition.

  • View full-size image.
  • Fig 2. 

    Study design and subject flow through sessions A and B (both divided into 2 parts separated by 60-minute rest with nutrition). Abbreviations: HRR, heart rate reserve; PLE, perceived level of exertion.

Cognitive Tasks 

Trail Making Tests Parts A and B 

The TMT-A and -B measure speed of visuomotor processing and cognitive flexibility. In TMT-Part A, subjects were requested to draw lines sequentially to ascending digits (1–13) as quickly as possible. In TMT-Part B, subjects must alternate between numbers 1 through 13 and letters A through L while connecting them. The score represented the amount of time required to complete each task including errors.

Symbol digit substitution test 

The symbol digit substitution test matches symbols with numbers to test psychomotor performance and concentration.27 Subjects were presented with an answer key with 9 geometric symbols labeled 1 through 9 and asked to match as many subsequent numbers to symbols as possible within 90 seconds. The numbers of correct matches were recorded.

Paced Auditory Serial Addition Test 

The Paced Auditory Serial Addition Test is an oral test that tests general attentional ability.28 Subjects listened to a series of 30 random single digit numbers spaced 2 seconds apart (eg, 2…7…3…1) and were asked to add the most recent number to the digit immediately preceding it (eg, 9…10…4). They practiced initially with 6 digits until they understood the test.

Action Research Arm Test 

The ARAT measures the ability to grasp and release objects including blocks and cylinders of various sizes. Nineteen activities are subdivided into grip, grasp, pinch, and gross motor categories and scored using a 4-point ordinal scale, for a total possible score of 57 (0=unable to perform; 1=able to partially complete; 2=able to complete slowly; 3=able to complete within the time limit). The ARAT was constructed and scored using time limits determined from performance times of healthy, elderly adults.24 Reliability is reported to be .99, and the MCID for the ARAT has been estimated to be 5.7 points (10% of the total score).24

Grip Strength 

We used the Jamar hydraulic hand dynamometera to measure grip strength of the hemiplegic hand (in kilograms) while the subject was seated, without back support, with the elbow at 90°.29, 30 We recorded the mean value of 3 attempts.31

Intervention 

BWSTT consists of a body harness that supports the subject while walking on a treadmill. All subjects received 20% body weight supportb while walking for 20 minutes (including 5-minute incremental increase, 10-minute steady-state, and 5-minute slow down). Heart rate (distal radial pulse) and perceived level of exertion (Borg scale) measures were gathered while the treadmill was paused at 5-minute intervals. Exercise was based on documented guidelines for people with stroke, which suggested 20 minutes of exercise may be a starting point for those naive to training.15 Subjects did not require manual assistance to walk, and pilot work indicated that 20% of body weight support was optimal. None of the subjects had used BWSTT before or were engaged in community exercise programs. We instructed subjects to hold the treadmill supports with both hands, and we provided assistance to the affected hand if required. Pace was determined by reaching 70% of the subject's estimated target heart rate (220 – age × .70) or level 13 (somewhat hard) on the Borg RPE scale, whichever was reached first. The Borg RPE scale ranges from 6 to 20, with 6 indicating no exertion at all and 20 indicating highest exertion.32 In those subjects taking medications affecting heart rate response, Borg RPE scale became the primary method to measure exercise intensity. All subjects received nutrition and water before each testing session to ensure adequate hydration and energy. We used the identical script for subject instruction. The control condition consisted of review of subject's home mobility and independence and updating of the home exercise program while sitting on a treatment mat with the physical therapist.

Statistical Analysis 

Statview softwarec was used for data analyses. To control for practice effects, the change in scores, rather than pretest and posttest scores, was compared between groups using ANOVA and paired t tests where appropriate. Change in score data was plotted and determined to have normative distribution. Simple regression analysis evaluated the relationship between exercise intensity and outcome measures. Significance was set at P less than .05 for all analyses, and values are expressed as mean ± SD.

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Results 

All subjects completed both sessions, and there were no complaints or adverse events (table 1). Mean maximum Borg RPE scale was near the target value, although subject measures ranged from 8 to 17, likely because the Borg RPE scale and heart rate were measured at 5-minute intervals rather than continuously. There was no effect of session order (A–B or B–A; ANOVA, P>.05, data not shown), suggesting that the order in which subjects were randomized to receive the cognitive or arm motor tests did not affect change in performance.

Table 1. Subject Characteristics
CharacteristicsMean ± SDRange
Age (y)61.4±10.232–78
Months poststroke20.1±14.66–60
MMSE score28.6±1.425–30
CMII arm5.6±1.62–7
CMII hand5.0±1.92–7
Initial ARAT41.7±16.34–56
Initial grip strength (kg)22.2±15.91.8–54
Sex (women/men)8/13
Stroke type2 hemorrhagic, 19 ischemic
Stroke location6 cortical, 11 subcortical,
3 both, 1 brainstem
Maximum Borg rating of perceived exertion scale13.3±2.248–17
Maximum treadmill speed (m/s)1.9±0.730.7–3.5

Abbreviations: CMII, Chedoke-McMaster Impairment Inventory; MMSE, Mini-mental State Examination.

Treadmill Exercise Did Not Affect Cognitive Performance 

Performance in most of the cognitive tests significantly improved between pretesting and posttesting under both control and treadmill conditions (table 2), likely a result of practice. However, treadmill exercise did not further enhance change in performance of any of the cognitive tests compared with control condition (paired t test, range P=.36–.75). Because intensity of exercise varied among subjects, we examined whether intensity of exercise (maximum Borg RPE scale and maximum treadmill speed) influenced change in cognitive scores. There was no relationship between maximum treadmill speed or Borg RPE scale on change in performance in any of the cognitive tests (P>.05, data not shown).

Table 2. Results of Primary Outcome Measures
TestTreadmillControl
Pre ± SDPost ± SDChange ± SDPre ± SDPost ± SDChange ± SD
TMT-A (s)51.2±21.146.9±28.7−4.35±14.852.1±27.944.9±24.6†−7.3±11.7
TMT-B (s)132.6±87.4109.9±80.7⁎−22.65±18.0131.4±78.3110.9±73.4†−20.45±25.3
SDST (no. correct)31.1±12.935.1±11.6⁎3.9±4.732.8±11.435.3±12.3‡2.5±4.3
PASAT (no. correct)23.1±7.925.9±9.7⁎2.8±3.822.6±6.026.2±8.0‡3.55±6.2
ARAT40.4±17.042.7±16.1⁎2.45±2.841.8±16.341.9±17.10.15±2.7

NOTE. Compared with preintervention scores,

⁎P<.005,

†P<.01,

‡P<.05.

Treadmill Exercise Improved Upper-Extremity Movement 

ARAT performance improved after BWSTT but not control condition (see table 2) (P<.005). When comparing the change in scores under both conditions, subjects experienced significantly larger improvement in ARAT score after treadmill training than after the control condition (fig 3) (paired t test, P=.04). ARAT score increased by 2.5±2.8 (95% CI, 1.27–3.73) points after treadmill exercise, compared with 0.15±2.7 (95% CI, –1.07–1.39) points after control condition. When analyzing subcomponents of the ARAT (grip, grasp, pinch, and gross motor), there was no significant difference in change in performance (P>.05, data not shown) in any of the subtests between the 2 conditions.

To test whether change in ARAT score was caused by faster movement speed during task performance, we analyzed whether more subjects improved from a score of 2 (indicating ability to complete the task slowly) on the ARAT to a score of 3 (indicating ability to do the task within the time limit) after treadmill exercise than with the control condition. In this analysis, there was no significant difference between conditions. Improvement in performance was subject-specific; however, anecdotally, some subjects described that their hemiplegic arm was “easier to move” after treadmill exercise.

We measured grip strength before and after each intervention, throughout both sessions, to gauge changes in strength of the hemiplegic upper extremity. Subject grip strength did not change significantly in the 7 to 10 days between the beginning of session A (22.2±15.9kg) and session B (21.5±15.4kg, paired t test, P=.26). Furthermore, there was no effect of time on subjects' grip strength throughout either of the sessions (repeated measures ANOVA, session A, F3,60=1.20, P=.32; session B, F3,60=.29, P=.84), suggesting that neither of the interventions altered grip strength. Because change in strength (increased fatigue) could influence ARAT score, we examined whether maximum treadmill speed altered change in grip strength. There was no correlation between change in grip strength (before and after treadmill exercise) and treadmill speed, indicating that treadmill exercise did not make the subjects' hemiplegic upper extremity stronger or weaker (data not shown).

We examined whether intensity of exercise (maximum Borg RPE scale and maximum treadmill speed) influenced change in ARAT score. Change in ARAT score was not correlated with Borg RPE scale (R2=.01; P=.63); however, improvement in ARAT was negatively correlated with maximum treadmill speed (R2=.2; P=.04). Subjects exercising at higher treadmill speeds experienced less improvement in the ARAT (fig 4). The attenuating effect of treadmill speed was less robust at the highest walking speeds (>3m/s), resulting in a U-shaped response. However, individuals with lower-arm functioning did not necessarily have lower walking speed during BWSTT, because level of arm impairment (initial ARAT score) was not related to maximum treadmill speed (R2=.07; P>.27).

  • View full-size image.
  • Fig 4. 

    Change in ARAT score after BWSTT is associated with maximum treadmill speed. Linear regression line indicates R2 equal to 0.2 (P=.04). Polynomial U-shaped curve shows a more robust effect for the very slowest walkers.

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Discussion 

We aimed to determine whether 1 session of BWSTT enhanced cognitive or upper-extremity performance in people with stroke. In contrast with other studies supporting the facilitory effect of acute exercise on tests of executive function in normative populations,4, 5, 6 we found that 20 minutes of walking exercise using BWSTT did not improve cognitive performance in people with chronic stroke. We did, however, find that BWSTT improved performance on a test of upper-extremity performance after stroke, although modestly. This is the first study to examine the cognitive effects of BWSTT in people with stroke and is the first to report an effect on seemingly unrelated upper-extremity function.

Improvement in the ARAT was greater after BWSTT (2.5±2.8; 95% CI, 1.27–3.73) but less than the MCID for the ARAT (5.7 points33). The measured MCID for the ARAT is yet to be reported; however, an improvement of about 3 points (as demonstrated in this study) indicates the subject can perform an entirely new movement, such as picking up a marble, within normalized time limits. The ARAT has very high intrarater reliability (intraclass correlation coefficient=.997) with the difference between scores by the same rater described as negligible,24 which suggests the effect we see in this study is unlikely a result of error. Compared with the benefits of forced-use therapy in people with chronic stroke, van der Lee et al34 report there is a 3-point difference in ARAT score in favor of the forced-use group (95% CI, 1.3–4.8), comparable to the results of treadmill exercise in this study. Although the gain after treadmill is modest, considering it occurred after only 1 session, it could still be important in the arm and hand skilled task training phase during rehabilitation.

How Does Treadmill Exercise Improve Movement of the Hemiplegic Arm? 

We attempted to determine the basis of the treadmill exercise effect on the hemiplegic arm and found, interestingly, that there was less improvement in ARAT score with higher treadmill speeds (>1.5m/s) (see fig 4). Although subjects could experience more arm fatigue with higher speeds (all subjects held the hand rails), this was not evidenced by decreased grip strength. Our data suggest that BWSTT had a more robust effect on upper-extremity movement for the slowest walkers. Improvement in ARAT with treadmill could also occur if there was a lessening of excessive tone in the muscles of the hemiplegic upper extremity. Because all subjects held both hand rails of the treadmill, the rhythmic movement of the trunk on fixed arms while walking could have relaxed tone in the arm and hand. Anecdotally, some subjects did report that their hemiplegic arm was “easier to move” after treadmill exercise. Alternatively, the treadmill exercise could have served as a warm-up, facilitating performance in comparison with the sedentary control condition. Future studies should examine the effect of treadmill exercise with and without arm support in comparison with healthy age-matched controls.

Even though enhanced ARAT performance was not a result of improved attention or visuomotor processing, it is possible that movement time could be faster after exercise without a change in cognitive scores. Subjects have faster movement speed without improved cognitive performance after acute cycling.4 These authors propose that faster movement time could be a result of exercise-induced increases in core temperature and neuronal transmission. Precise reporting of movement time during motor tasks could help determine whether movement speed was enhanced with exercise.

Exercise improves mood and lessens depression in healthy individuals and people with stroke,35, 36 which may have influenced performance on the ARAT. Further examination of the effect of a single bout of exercise on measures of depression and motor performance after stroke would help identify the etiology of this exercise effect.

Why Did Treadmill Exercise Have No Effect on Cognitive Performance? 

Our findings conflict with others that show a facilitory effect of exercise on executive functioning. There could be many reasons for this. We tested a unique population who may respond differently to exercise than people without brain injury. In addition, our paradigm (20 minutes of walking at a moderate intensity level) may not be of adequate intensity or duration to produce a cognitive effect. Others have shown that intense exercise for 40 minutes or more is required to increase neurotransmitters, norepinephrine and dopamine.4, 5 Hillman et al3 have confirmed that increases in P3 amplitude, an indicator of cognitive processing speed, occurs only in people exercising somewhat hard for 30 minutes at the Borg RPE scale level. In contrast, light, moderate, and hard intensities of acute cycling equally improved performance on a flanker task.6 Because the threshold required inducing an exercise-cognition effect in people with brain injury is not known, future studies should examine several clinically relevant exercise paradigms.

The effect of exercise on cognition also depends on cognitive complexity.6, 37 Previous studies have shown that acute6, 38 and prolonged39 exercise enhances complex executive tasks more robustly than simple cognitive tasks. The timed cognitive tests used in this study were relatively simple. Future studies should determine whether exercise, both acute and prolonged, exerts a specific effect on tasks of higher complexity in people with brain injury. There is likely an interaction between exercise intensity and duration and the complexity of the cognitive task.

Study Limitations 

This exploratory, proof-of-principle study demonstrates that exercise may enhance subsequent arm function in people with stroke. The cognitive effects of exercise were inconclusive; however, our findings indicate further refinement of exercise paradigms, and cognitive outcome measures are required. The testers were aware of randomization, and this could have affected the results even though we chose timed, objective outcome measures to limit tester bias. In addition, we do not know whether the exercise effects were long-lasting.

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Conclusions 

Novel approaches in rehabilitation are required to address the debilitating effects of residual physical and cognitive impairment after stroke. This study is the first to identify that a single session of treadmill exercise may potentiate performance on a subsequent arm motor task. Further studies should examine the etiology and longevity of this exercise effect. Furthermore, the cognitive enhancing effect of exercise in people with brain injury, as has been demonstrated in animal models and healthy individuals, is unknown. It is expected that this avenue of rehabilitation research may lead to innovative practice for the benefit of people with stroke.

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  • a Sammons Preston, 1000 Remington Blvd #210, Bolingbrook, IL 60440.
  • b Pneuweight unweighting system; Pneumex, 2605 N Boyer Ave, Sandpoint, ID 83864.
  • c SAS Institute, 100 SAS Campus Dr, Cary, NC 27513.

 Supported by the Newfoundland and Labrador Centre for Applied Health Research.

 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.

 Reprints not available from the author.

PII: S0003-9993(08)00798-3

doi:10.1016/j.apmr.2008.05.017

Archives of Physical Medicine and Rehabilitation
Volume 89, Issue 11 , Pages 2041-2047, November 2008

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