Objectives: Upon completion of this article, the reader should be able to: (1) understand the role of muscle weakness in the pathophysiology of stroke; (2) understand that progressive resistance training is effective in increasing muscle strength after stroke; (3) evaluate the implications of resistance training in rehabilitation after stroke.
Accreditation: The Association of Academic Physiatrists is accredited by the Accreditation Council for Continuing Medical Education to sponsor continuing medical education for physicians.
The Association of Academic Physiatrists designates this continuing medical education activity for a maximum of one credit hour in Category 1 of Physician's Recognition Award of the American Medical Association. Each physician should claim only those hours of credit that he/she actually spent in the education activity.
Disclosure: Disclosure statements have been obtained regarding the authors' relationships with financial supporters of this activity. There is no apparent conflict of interest related to the context of participation of the authors of this article.
Stroke is the leading cause of physical disability in older men and women in the United States.1 Motor impairments including muscle weakness, decreased velocity and control of movement, and abnormal patterns of movement affect 60% to 78% of persons suffering a stroke and often result in decreased functional ability.2 The observed muscle weakness in the post-stroke population has been attributed to reduced muscle fiber size, decreased firing rate, atrophy of type II muscle fibers, increased fatigue, decreased motor unit numbers, and altered motor unit recruitment.3 In cross-sectional studies of stroke outcomes, voluntary muscle strength, particularly of the knee extensors, has been shown to be closely correlated with measures of gait quality,4-6 an important determinant of functional independence in this population.
Older stroke survivors, who number nearly 3 million, may have a continuing decline in mobility after stroke.7 Impairments in self care and mobility in all older adults during tasks such as walking, rising from a chair, and ascending stairs have been associated with a 2-fold greater risk for institutionalization and death.8, 9
Progressive resistance strength training exercise has been shown to increase muscle strength and size in healthy and frail older individuals (for review, see Fielding10). After stroke, few studies have addressed the effects of any type of strength or resistance training on changes in muscle strength.11-13 However, interpretation of these reports is complicated by several confounding factors including the timing of the intervention relative to stroke onset,12 the outcome measures used,11 and the type and intensity of the strengthening program implemented.11, 13
No studies have assessed the effects of progressive resistance training after stroke on changes in strength and the associated changes in functional outcome measures in community dwelling individuals after stroke. Traditionally, recovery of motor function after stroke has been thought to be nearly complete in the first 3 to 6 mo after onset.14, 15 Therefore, the present study was conducted to evaluate the effects of a high intensity resistance strength training intervention on bilateral lower limb strength, performance, and clinical outcome measures in older individuals at least 1 yr after stroke onset.
A time series clinical trial using progressive resistance training was conducted with baseline and postintervention measures of lower limb strength, functional performance, and functional outcome in a volunteer sample of post-stroke individuals.
Subjects were eligible for enrollment if they were living at home, older than age 60, at least 1 yr after stroke, not presently receiving any rehabilitation services, and unable to perform unilateral stance for more than 15 sec with the affected lower limb.
Participants were recruited from Local Easter Seals stroke support groups, Home Health Agencies, Rehabilitation Clinics, and an outreach letter via the National Stroke Association. Recruitment letters were sent to 75 prospective volunteers. Those who responded were screened on the phone and, if appropriate, began the recruitment process. Of the initial pool of 75 subjects, 12 responded to a mailing. All participants underwent further review with a medical history by their own primary care physician, which required a signed medical consent form. Persons scoring below an 18 on the Folstein Mini Mental examination were excluded. Three individuals were excluded who did not meet baseline criteria. Two dropped out after 3 wk for personal reasons. Of the original pool, seven participants met eligibility criteria and agreed to participate. A signed informed consent form was obtained. The protocol was approved by the Institutional Review Boards at Sargent College, Mt. Auburn Hospital, and Massachusetts General Hospital.
Exercise Training Protocol
Baseline measures of performance and strength were assessed twice, separated by 5 days to minimize testing effects.16 After the baseline testing, subjects began the exercise intervention.
The exercise training was performed for 12 wk (2× per wk). Subjects performed standing hip flexion, abduction, and extension using a stack weight training machine (California Gym Apollo, Pomona, CA). Sitting knee extension and leg press were performed on Keiser Pneumatic training equipment (Keiser Sports Health Equipment, Fresno, CA). Each of these exercises was performed unilaterally on both the affected and intact side. All participants were able to do knee extension on the hemiparetic side through part of their range of motion. All subjects worked up to three sets of 8 to 10 repetitions at 70% of the 1 repetition maximum (1 RM). All training and testing was supervised by a physical therapist.
1 RM Muscle Strength
Muscle strength testing was performed on all the muscle groups undergoing training and on the same equipment on which the subjects trained. Strength testing in stroke populations has been shown to be reliable and valid as an outcome measure in clinical trials.5 When support in stance was needed, an assistive device such as a cane or walker was used along with occasional physical contact by the therapist. Subjects were allowed several trials of exercise as warm-up. The weight was then progressively increased with a minimum of 30-sec rest between each trial. The 1 RM was used to measure muscle strength. This is defined as the maximum weight that could be lifted correctly for one repetition within 5% of the full range of motion. In general, three to five progressive weight increases were required before 1 RM was found. The 1 RM test was measured at baseline and every 2 wk during the training period. At baseline, the highest of the two measurements was established as the baseline 1 RM and used to determine the initial training intensity.17
Habitual gait velocity was measured to the nearest 0.01 as the mean of two trials by an ultrasonic gait speed monitor (OCPB Electronics, Glasgow, Scotland). The apparatus was applied around the waist and the subject was asked to begin walking at their comfortable walking speed along a level corridor for approximately 6 m. The use of assistive devices was noted. Reliability estimates for habitual gait velocity at baseline were determined by calculating the single test intraclass correlation coefficient (ICC = 0.924).
Chair Rise Time
Repeated chair rise time included five full sit-to-stand sequences. Subjects were instructed to rise from the standard firm seat and use their arms only if necessary. Chair rise time was measured from initiation to full stance and timed to the nearest 0.1 sec. This test was only performed once at each evaluation session. The reliability of this test determined at baseline is excellent (ICC = 0.933).
Subjects were asked to climb a single flight of stairs (11 steps) with rails on both sides. Subjects were instructed to ascend and descend as quickly as possible. The test was repeated twice with the average time taken for analysis. Time for ascent and descent was recorded as well as use of rails and stepping pattern. Reliability for this test was good (ICC = 0.756).
Unilateral Leg Stance
The time was measured as a participant was asked to stand on each leg without upper limb support. The inability of a subject to stand unilaterally was recorded as 0.00 sec. Three trials were performed for each leg with the average time recorded at each session.
All functional performance measures were assessed at baseline, 4, 8, and 12 wk.
Motor Assessment Scale
All subjects were asked to perform the first five items, which test domains of lower limb function, of the Motor Assessment Scale (MAS) at baseline and 12 wk. The MAS uses a 7-point ordinal scale to rate motor function for eight everyday tasks, including gait12. It has been shown to be a valid and reliable baseline indicator of motor function after stroke.18
Static and dynamic balance were tested by using the Berg Balance scale at baseline and 12 wk. It includes 14 items of functional reach, sitting and standing balance, transfers, turning, and tandem walk.19
Self-Reported Measures of Functional Status and Activity
The physical function subscale of the Medical Outcome Survey (36 item short form) health survey (MOS-36) was administered at baseline and 12 wk.20 Levels of voluntary physical activity were monitored by using the Harvard Alumni Questionnaire,21 which has been validated in postmenopausal women,22 and the Physical Activity Scale for the Elderly.23 The Barthel Index was also determined at baseline because it has been used as a good overall measure of disability in randomized controlled studies.24-26 The Barthel Index has been tested for both validity and reliability in assessing disability in the stroke population.2
The Geriatric Depression Scale was administered with an interviewer to assess a clinical marker of depression.27 This is a 30-question instrument that asks questions related to depressive symptoms. Marked depressive symptoms have been noted in 21% to 22% of the stroke population 1 yr after stroke.25 Previous studies have shown progressive resistance exercise to improve depressive symptoms in depressed elders.28 The test was administered at baseline and 12 wk. The Geriatric Depression Scale represents a reliable and valid self-rating depression screening scale for the older population.27 A score of 14 indicates an 80% sensitivity rate for classifying depression.
All data are reported as mean ± SEM values. Differences before, during, and after training were analyzed by analysis of variance for repeated measures. Measurements determined at 0 and 12 wk were compared by using a paired t test. Relationships between variables of interest were determined by using least-squares linear regression. Significance was established at P < 0.05.
The clinical characteristics of the seven subjects enrolled in the intervention are presented in Table 1. The mean Barthel score at baseline was 96/100, which indicates a high independence level of the group. In five subjects, their stroke occurred in the left hemisphere and, in two, it occurred in the right. In addition, three of seven subjects had some degree of sensory loss.
All seven subjects successfully completed the training protocol. The attendance rate was 90% for the 12-wk program. All participants were able to perform the exercises as planned. Two subjects infrequently experienced minor back discomfort during exercise, and one subject experienced some knee discomfort on her intact side with knee extension. None of the participants required analgesic medication or missed sessions because of discomfort.
Baseline Muscle Function
At baseline, strength of the knee and hip extensors of the affected side was reduced by 53% (P < 0.0002) and 62% (P < 0.01), respectively. Muscle strength for all other muscle groups tested was not different between affected and intact side.
Functional performance measures were also related to the 1 RM of several muscle groups evaluated. Repeated chair stand strongly correlated with affected knee extension 1 RM (r = −0.788; P<0.035) (Fig. 1). In addition, affected leg press (r = −0.827; P < 0.022), affected hip flexion (r = −0.824; P < 0.023), and intact hip extension (r = −0.857; P < 0.014) were also associated with repeated chair stand time. Associations were also found between the Berg Balance Scale and affected side leg press (r = 0.875; P < 0.002). The MAS also was strongly associated with affected side leg press (r = 0.776; P < 0.068).
Gait velocity at baseline was associated with affected hip flexion strength (r = 0.814; P < 0.026). Single leg stance time of the affected side was most strongly correlated with hip abduction strength at baseline (r = 0.879; P < 0.01) and affected side leg press (r = 0.867; P < 0.011).
Strength Training Effects
Absolute improvements in muscle strength gains occurred over the 12-wk period for all muscle groups trained with the exception of the hip extensors using the leg press (Table 2). The time course of strength gains revealed that nearly all of the improvements in strength were accomplished by the eighth wk of training. Relative gains in muscle strength were similar on the intact and affected side and averaged 48% and 68%, respectively (Fig. 2).
Repeated chair stand time decreased 21% (P < 0.02) by week 12 of the training intervention. There also was a trend for stair climb time to decrease 11% (P < 0.07) (Table 3). Although stair climb time did not improve significantly, in the four of seven subjects with a step-to-step stair climb pattern, their stair climb quality improved to a step-over-step pattern. Gait velocity and leg stance (affected and intact) were not affected by the exercise intervention.
Clinically Based Functional Assessments
Evaluation of function by using the lower limb subset of the MAS revealed a 12% (P < 0.02) improvement after the intervention (Table 4). In addition, the walking subscale of the MAS also improved significantly when analyzed separately (P < 0.03). Static and dynamic balance, as measured by the Berg Balance Scale, improved 12% (P < 0.003).
Self-Reported Functional Status
The physical function subscale of the MOS improved 17% (P < 0.03) from baseline to week 12. The Geriatric Depression Scale score, the Physical Activity Scale for the Elderly, and Harvard Alumni Questionnaire were not significantly improved over time (Table 5).
In the present study, measures of muscle strength were associated with several measures of functional performance at baseline. Previous studies have also found strong associations between paretic knee extension torque and locomotion.5, 6, 29 In addition, power generated by the hip flexors and the ankle plantarflexors of the paretic lower limb has been shown to be a strong predictor of walking speed in individuals after stroke.30 Associations between knee extensor strength and gait velocity have also been observed in older frail institutionalized individuals.31 Because of the observed relationship between strength and function in our population, we tested the hypothesis that progressive resistance training would improve muscle strength and subsequently improve measures of functional performance.
The major finding of the present study was that progressive resistance training improved affected and intact side muscle strength in individuals at least 1 yr after stroke onset. Previous studies have attempted to train solely the involved lower limb by using strengthening exercises. Studies have used "step-up" exercise and leg extension weight training on the involved side during acute post-stroke rehabilitation,11, 12 and, more recently, 6 wk of isokinetic training of the affected side knee extensors in long-term stroke survivors improved peak torque at all velocities examined.13 It is interesting that, in the present study, the relative improvements in muscle strength on the intact and affected side were similar and represented a greater relative improvement in strength than has been observed in previous studies after stroke. In addition, examination of changes in the 1 RM in the present study suggests that the gains in strength were achieved progressively through week 8 of the 12-wk training program. This rate of improvement is consistent with previously reported gains in strength in healthy and frail older individuals undergoing similar resistance training interventions.31, 32
Despite the nearly universal improvements in strength for all muscle groups trained, functional performance measures were only improved for the repeated chair stand time and there was a trend for improvement in stair climb time. Gait velocity and leg stance time were unaffected by the intervention. In other studies where the relationships between strength gains and functional performance changes have been evaluated, the results have been conflicting.28, 33-37 Generally, in more frail or disabled individuals, improvements in functional performance have been associated with the observed improvements in muscle strength.28, 33, 35, 37 After stroke, Sharp and Brouwer13 found a significant improvement in gait velocity but not chair stand performance or stair climb with isokinetic training of the hemiparetic knee. Recently, Duncan et al.38 reported improvements in gait velocity in individuals with mild-to-moderate stroke after an 8-wk home-based endurance strength and balance training program. The specific differences in functional performance improvements from the present study and other reports may be related to differences in baseline function of subjects and/or specific differences in the type and length of the exercise training protocol. The present study together with previous reports does suggest some association between restoring strength and enhancing functional performance after stroke.
Improvements in clinical measures of function and balance were consistent with the observed improvements in functional performance. The MAS has been used as a clinical marker of function after stroke and was modestly improved in our subjects after the training intervention.18 Although gait velocity did not change in our intervention, the quality of gait changed enough to significantly improve scores on the gait subscale of the MAS. This improvement in the gait subscale of the MAS is accounted for by changes in the use of assistive devices and/or changes in the ability to pick up an object while walking. The observed improvements in static and dynamic balance were consistent with some reports of improved balance with exercise training in frail or disabled elderly.35, 39, 40 Duncan et al.38 reported no effect of a home-based exercise intervention on balance in individuals with mild-to-moderate stroke. It is possible that the supervised high intensity exercise intervention used in the present study may have been responsible for the reported gains in static and dynamic balance. Improvements in balance in individuals with stroke may be an important outcome specifically in relation to reducing the risk of falls.
Both measures of habitual physical activity remained unchanged and revealed a low level of habitual activity. Measurement of physical function, however, using the MOS SF36 physical function subscale, did improve over the intervention. This is consistent with two other studies of exercise in stroke.13, 38 Improvements using this scale (MOS) may have been more sensitive to changes in performance of activities of daily living compared with the other indices of recreational or habitual activity (Harvard Alumnae, Physical Activity Scale for the Elderly).
The motor impairments coupled with the continuing loss of muscle mass and strength in long-term stroke survivors potently accelerate the progression of disability in this population. The results of the present study challenge the concept that functional recovery after stroke is greatest in the first 3 to 6 mo after stroke onset. Although the limited number of subjects enrolled in the present study may limit the generalizability of these findings, the present results show that strength training can profoundly improve strength and result in modest improvements in function late in the course of stroke recovery. Future studies should address the role of rehabilitation strategies using resistance training to maintain independence and prevent further progression of disability after stroke.
We acknowledge Keiser Sports Health Equipment for use of their strength training equipment.
1. Gresham GE, Fitzpatrick TE, Wolf PA, McNamara PM, Kannel WB, Dawber TR: Residual disability in survivors of stroke-Framingham study. N Engl J Med
2. Good DC: Treatment strategies for enhancing motor recovery in stroke rehabilitation
. J Neurol Rehab
3. Weightman MM: Motor unit behavior following cerebrovascular accident. Neurol Rep
4. Bohannon RW: Strength deficits also predict gait performance in patients with stroke. Percept Mot Skills
5. Bohannon RW, Walsh S: Nature, reliability, and predictive value of muscle performance in patients with hemiparesis following stroke. Arch Phys Med Rehabil
6. Hamrin E, Eklund G, Hillgren A, Borges O, Hall J, Hellstrom O: Muscle strength and balance in post stroke patients. Uppsala J Med Sci
7. Wade DT, Collen FM, Robb GF, Warlow CP: Physiotherapy intervention late after stroke and mobility. BMJ
8. Fried LP, Guralnock JM: Disability in older adults: evidence regarding significance etiology and risk. J Am Geriatr Soc
9. Guralnick JM, Ferrucci K, Simonnick EM, Salive ME, Wallace RB: Lower extremity function
over the age of 70 years as a predictor of subsequent disability. N Engl J Med
10. Fielding RA: The role of progressive resistance training and nutrition in the preservation of lean body mass in the elderly. J Am Coll Nutr
11. Inaba M, Edberg E, Montgomery J, Gillis M: Effectiveness of functional training, active exercise
, and resistance exercise
for patients with hemiplegia. Phys Ther
12. Nugent J, Schurr K, Adams R: A dose response relationship between amount of weight-bearing exercise
and walking outcome following cerebrovascular accident. Arch Phys Med Rehabil
13. Sharp SA, Brouwer BJ: Isokinetic strength training of the hemiparetic knee: effects on function
and spasticity. Arch Phys Med Rehabil
14. Wade DT, Wood VA, Heller A, Maggs J, Langton Hewer R: Walking after stroke. Scand J Rehab Med
15. Duncan PW, Goldstein LB, Matchar D, Divine GW, Feussner J: Measure of motor recovery after stroke. Stroke
16. Tangeman P, Banaitis D, Williams A: Rehabilitation
of chronic stroke patients: changes in functional performance. Arch Phys Med Rehabil
17. Nelson ME, Fiatarone MA, Morganti CM, Trice I, Greenberg RA, Evans WJ: Effects of high intensity strength training on multiple risk factors for osteoporotic fractures. JAMA
18. Poole J, Whitney S: Motor assessment scale for stroke patients: concurrent validity and interrater reliability. Arch Phys Med Rehabil
19. Berg K, Wood-Dauphinee S, Williams JI: The balance scale: reliability assessment with elderly residents and patients with acute stroke. Scand J Rehabil Med
20. Ware J: SF36 Health Survey Manual and Interpretation Guide.
Boston, Nimrod Press, 1993
21. Paffenbarger RS, Wing AL, Hyde RT: Physical activity as an index of heart attack risk in college alumni. Am J Epidemiol
22. Ainsworth B, Leon A, Richardson M, Jacobs D, Paffenbarger R: Accuracy of the college alumnus physical activity questionnaire. J Clin Epidemiol
23. Washburn R, Smith K, Jette A: The physical activity scale for the elderly (PASE): development and evaluation. J Clin Epidemiol
24. Mahoney FI, Barthel DW: Functional evaluation: the Barthel Index. Md State Med J
25. Herman N, Black SE: The Sunny Brook stroke study: a prospective study of depressive symptoms and functional outcomes. Stroke
26. Granger CV, Albrecht GL, Hamilton BB: Outcome of comprehensive medical rehabilitation
: measurement by PULSES profile and the Barthel Index. Arch Phys Med Rehabil
27. Yeasavage JA, Brink TL: Development and validation of a geriatric depression screening scale: a preliminary report. J Psychiatr Res
28. Singh NA, Clements KA, Fiatarone MA: A randomized controlled trial of progressive resistance training in depressed elders. J Gerontol
29. Nakamura R, Hosokawa T, Tsujr I: Relationship of muscle strength for knee extension to walking capacity in patients with spastic hemiparesis. Tohoku J Exp Med
30. Olney SJ, Griffin MP, Monga TN, McBride ID: Work and power in gait of stroke patients. Arch Phys Med Rehabil
31. Fiatarone MA, Marks EC, Ryan ND, Meredith CN, Lipsitz LA, Evans WJ: High-intensity strength training in nonagenarians: effects on skeletal muscle. JAMA
32. Frontera WR, Meredith CN, O'Reilly KP, Knuttgen HG, Evans WJ: Strength conditioning in older men: skeletal muscle hypertrophy and improved function
. J Appl Physiol
33. Fiatarone MA, O'Neill EF, Ryan ND, et al: Exercise
training and nutritional supplementation for physical frailty in very elderly people. N Engl J Med
34. Buchner DM, Cress ME, deLateur BJ, et al: The effect of strength and endurance training on gait, balance, fall risk, and health services use in community-living older adults. J Gerontol
35. Sherrington C, Lord SR: Home exercise
to improve strength and walking velocity after hip fracture: a randomized controlled trial. Arch Phys Med Rehabil
36. Lord SR, Ward JA, Williams P, Strudwick M: The effect of a 12-month exercise
trial on balance, strength, and falls in older women: a randomized controlled trial. J Am Geriatr Soc
37. Chandler JM, Duncan PW, Kochersberger G, Studenski S: Is lower extremity strength gain associated with improvement in physical performance and disability in frail, community-dwelling elders? Arch Phys Med Rehabil
38. Duncan P, Richards L, Wallace D, et al: A randomized, controlled pilot study of a home-based exercise
program for individuals with mild and moderate stroke. Stroke
39. Buchner DM, Cress ME, deLateur BJ, et al: A comparison of the effects of three types of endurance training on balance and fall risk factors in older adults. Aging (Milano)
40. Campbell AJ, Robertson MC, Gardner MM, Norton RN, Tilyard MW, Buchner DM: Randomised controlled trial of a general practice programme of home based exercise
to prevent falls in elderly women. BMJ
How to Obtain CME Category 1 Credits
To obtain CME Category 1 credit, this educational activity must be completed and postmarked by December 31, 2001. Participants may read the articles and take the exams issue by issue or wait to study several issues together. After reading the three CME Articles in this issue, participants may complete the Self-Assessment Exam by answering the questions on the CME Answering Sheet and the Evaluation pages, which appear later in this section. Send the completed forms to: CME Department, Association of Academic Physiatrists, 5987 E. 71st Street, Suite 112, Indianapolis, In 46220. Documentation can be received at the AAP National Office at any time throughout the year, and accurate records will be maintained for each participant. CME certificates are issued only once a year in January for the total number of credits earned during the prior year.