Stroke and Neurodegenerative Disorders: 3. Poststroke Rehabilitation

Stroke and Neurodegenerative Disorders

Stroke and Neurodegenerative Disorders: 3. Poststroke Rehabilitation Henry L. Lew, MD, PhD, Lisa A. Lombard, MD, Cara Camiolo Reddy, MD, Alex Moroz, MD, PhD, Steven R. Edgley, MD, John Chae, MD Objective: This self-directed learning module highlights rehabilitation strategies in poststroke rehabilitation. It is part of the study guide on stroke and neurodegenerative disorders in the Self-Directed Physiatric Education Program for practitioners and trainees in physical medicine and rehabilitation. Using a case vignette format, this article specifically focuses on typical clinical presentations, recovery patterns, and traditional and innovative therapeutic interventions in poststroke rehabilitation such as constraint-induced movement therapy, treadmill training, functional electrical stimulation, robot-aided therapy, virtual reality treatment, cortical stimulation, speech therapy for aphasia, and orthotic management. The goal of this article is to influence the learner’s knowledge on the delivery of poststroke rehabilitation treatment. 3.1 Clinical Activity: A 65-year-old man who sustained a left middle cerebral artery infarct with right hemiparesis is admitted into your acute stroke rehabilitation unit. The family asks, “When will my father recover?” Describe the time course and pattern of motor and functional recovery following stroke. Patients with left middle cerebral artery (MCA) infarct often present with right hemiparesis. The expected initial clinical presentations of motor impairment include weakness and reduced muscle tone, and lack of voluntary control of the right upper and lower limbs. Based on the anatomical distribution of the MCA territory that covers the primary motor area (Figure 1) [1], one would expect the motor function of the upper limb to be more impaired than that in the lower limb. With stabilization of the acute injury and as edema starts to resolve, the course of motor recovery follows a predictable pattern of reflex changes, from an initial phase of diminished proprioceptive reflexes to abnormally increased reflexes [2]. The recovery of voluntary control typically is preceded by synergistic muscle contraction patterns that are somewhat nonfunctional, since they consist of mass contraction of multiple muscle groups (Table 1) [3]. Recovery tends to occur from proximal to distal portions of the limbs, but the evolution of synergistic and isolated muscle movements can halt at any time. These initial observations by Twitchel [2] regarding motor recovery were further defined by Brunnstrom into specific stages [4], as described in Table 2. Signs of neurological recovery include gradual return of muscle strength, muscle tone, and voluntary control. In a landmark article by Jorgensen et al [5], the authors studied the patterns of recovery for more than 1000 patients, and showed that the majority of neurological and functional recovery occurred within the first 6 months. Using the Barthel Index as the outcome measure, they found that functional recovery was “completed” within 12.5 weeks for 95% of patients. Moreover, 80% of the patients reached their maximum functional recovery level within 6 weeks, suggesting that most of the recovery occurs in the early phase. As expected, the initial severity of the stroke was correlated with the time course of recovery. They reported that for patients with mild, moderate, severe, and very severe strokes, recovery plateaus were reached at 8.5 weeks, 13 weeks, 17 weeks, and 20 weeks, respectively. Echoing this finding, Hendricks et al [6] indicated that the initial grade of paresis is a key prognosticator of motor recovery. PM&R 1934-1482/09/$36.00 Printed in U.S.A.

H.L.L. Harvard Medical School, VA Boston Healthcare System, Physical Medicine and Rehabilitation Service, 150 South Huntington Ave, Boston, MA 02130. Address correspondence to: H.L.L.; e-mail: [email protected] Disclosure: nothing to disclose L.A.L. Santa Clara Valley Medical Center, San Jose, CA Disclosure: nothing to disclose C.C.R. Department of Physical Medicine and Rehabilitation, University Health Center of Pittsburgh, Pittsburgh, PA Disclosure: nothing to disclose A.M. NYU School of Medicine, Rusk Institute of Rehabilitation Medicine, New York, NY Disclosure: 2, IPRO S.R.E. University of Utah, Salt Lake City, UT Disclosure: 2, Northstar Neuroscience J.C. Case Western Reserve University, Department of Physical Medicine and Rehabilitation, MetroHealth Medical Center, Cleveland, OH Disclosure: nothing to disclose Disclosure Key can be found on the Table of Contents and at www.pmrjournal.org

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Table 2. Brunnstrom’s Stages of Recovery After Stroke Stage 1

Stage 2 Stage 3

Stage 4

Stage 5

Stage 6

Flaccidity (initial stage immediately after stroke; no voluntary movement or stretch reflex on the affected side) Minimal voluntary movement, spasticity is developing Increase in spasticity (beginning of voluntary movement control, synergistic movement still predominates) Decrease in spasticity (some movement patterns develop independent of synergy; synergy patterns still predominate) Further decrease in spasticity (more independent; complex movements are relearned; basic synergies lose their dominance) Approaching normalcy (isolated joint movements, gradual normalization of voluntary coordination, spasticity has almost disappeared)

From Brunnstrom [4]. Adapted and reproduced with permission.

ing stroke. What is the prognosis for motor and functional recovery for this patient? Figure 1. Penfield’s motor homunculus along the precentral gyrus, showing proportionate representation of the neuronal population corresponding to various parts of the human body. From Kandel et al [1]. Reprinted with permission.

3.2 Clinical Activity: A 72-year-old man is admitted to your acute rehabilitation floor following a left hemisphere lacunar infarct 3 days prior. He requires minimal assistance for activities of daily living (ADL) and moderate assistance for mobility. In the right upper limb, he exhibits 4/5 strength proximally, but 3/5 strength of the finger extensors. In the right lower limb, he exhibits 4/5 strength proximally, but 1/5 strength of the ankle dorsiflexors. His cognition and sensation are intact. He is continent of bowel and bladder. Identify factors predictive of neurological and functional recovery follow-

Table 1. Synergy Patterns in Poststroke Motor Recovery Synergy Type Flexor

Extensor

Upper Limb

Lower Limb

Shoulder retraction Shoulder abduction Shoulder external rotation Elbow flexion Forearm supination Wrist flexion Finger flexion

Hip flexion Hip abduction Hip external rotation

Shoulder protraction Shoulder adduction Elbow extension Forearm pronation Wrist extension Finger flexion

Knee flexion Ankle eversion Dorsiflexion Toe extension Hip extension Hip adduction Knee extension Ankle inversion Plantar flexion Toe flexion

From Roth and Harvey [3]. Reprinted with permission.

This patient presents with clinical manifestations consistent with a pure motor stroke (see Study Guide Activity 1.4). The factors predictive of unfavorable functional recovery after stroke have been well documented by Jongbloed [7], Dombovy et al [8], and Wade et al [9]. Collectively, these factors include: (1) severity of stroke, such as coma at onset or large size of cerebral lesion, (2) history of previous stroke or medical comorbidities such as cardiovascular disease, (3) poor cognitive function, (4) urinary or bowel incontinence, (5) presence of visuospatial deficit, hemianopsia or hemineglect, (6) poor sitting balance, (7) poor upper extremity motor function or lack of motor recovery after 1 month, and, as expected, (8) low functional score on admission. In the Jongbloed review [7], most studies suggested that older patients have less favorable functional outcomes than younger patients, although this may be confounded by the higher prevalence of medical comorbidities in older patients. Also, in a study by Reding and Potes [10], the researchers used life table analysis to study rehabilitation outcome after initial unilateral hemispheric stroke. In patients with motor deficits only, more than 90% of them achieved the goal of independent ambulation (with or without assistance) by 14 weeks after stroke. Regarding the patient described in this case scenario, despite his relatively advanced age, it is likely that he will still achieve favorable functional recovery because of the following factors: low severity of stroke, intact cognition and sensation, intact bowel and bladder function, and no history of prior stroke. 3.3 Clinical Activity: A 57-year-old woman presents with left internal capsule infarct with right motor hemiparesis, impaired ADLs and impaired mobility. Describe the prevailing and emerging strategies for the treatment of hemiplegia and the associated functional deficits.

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Traditional rehabilitation programs for hemiplegic stroke include mobilization of the affected limb, range of motion exercises, strengthening, and use of compensatory techniques. It is customary to initiate therapy with an interactive, repetitive training program, with constant modification of tasks to engage the patients by keeping the activities challenging. The Bobath method [11], also known as neurodevelopmental training (NDT) is based on the concept that the motor tasks should be relearned from the simplest movements to the most complex and integrated functional movements. It also encourages the use of reflex-inhibiting activities to minimize undesired postural reactions. Thus, mass synergy contractions are discouraged, with the notion that they might cause abnormally increased tone and poor posture. In the past several decades, improvements of technology in the fields of neurophysiology and neuroimaging have provided new clues to explain the mechanisms behind motor recovery. The findings from clinical reports and animal studies support the concept of neuroplasticity. There is evidence to suggest that behavioral activities induce functional plasticity of the uninjured motor cortex [12]. Specifically, strategies that include repetition of novel, functionally relevant, cognitively engaging tasks are associated with neuroplastic changes in animal models. In parallel with these research results, various therapeutic strategies have been developed to enhance motor recovery. They include constraint-induced movement therapy (CIMT), body weight-supported treadmill training, virtual reality interventions, therapeutic electrical stimulation (TES), robot-aided therapy, and cortical stimulation. Constraint-induced Movement Therapy. Also known as “forced use” of the hemiparetic upper limb, CIMT is conducted by restraining the intact (or less-impaired) upper extremity, thus encouraging the patient to use his/her more impaired limb. This approach, which was initially proposed by Taub et al [13], was recently confirmed in a large multicenter clinical trial by Wolf et al [14]. The trial enrolled 222 participants who were 3 to 9 months since their stroke. Those assigned to the CIMT group wore a restraining mitt on the less-affected hand while engaging in repetitive-task practice and behavioral shaping with the hemiplegic hand. Participants underwent behavioral shaping 6 hours a day with a therapist and were encouraged to wear the mitt for 90% of their waking hours to perform functional tasks. The control group received “usual and customary” care. All participants were treated for 2 weeks and followed for 12 months. The clinical trial demonstrated the superiority of CIMT over the standard therapies used by the control group, as evidenced by measures of upper limb motor impairment (Wolf Motor Function Test) and activities limitation (Motor Activity Log). While this is clearly a landmark clinical trial, translation of these results into clinical practice is uncertain for several reasons. First, some doubt exists that the present medical economic climate can absorb the man-hour cost of CIMT as implemented in the trial. A modified form of CIMT may be a

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solution [15]. Second, it is uncertain whether the observed effect was specific to the intervention or simply due to difference in dose. A randomized clinical trial by van der Lee et al that compared CIMT to an equal dose of NDT showed far less impressive results [16]. It is possible that another doseequivalent intervention, a therapy that is perhaps less intensive and thus less costly, could lead to the same results. Wolf et al [14] clearly demonstrated that CIMT is superior to the present standard of care. Whether the observed effect was specific to CIMT, however, remains to be elucidated. Body Weight-supported Treadmill Training. Since treadmill training is climate-independent and readily available, it is natural for patients and therapists to consider this modality for improving ambulatory function. In order to facilitate a normal gait pattern, the use of a harness to reduce the load on the weak limb has been advocated. A therapist applies the harness and assists the patient with the training throughout the entire session. The safety benefits to both patients and therapists are also apparent. Using stringent guidelines from the recent Cochrane review, no statistically significant advantages were found for treadmill training, with or without body weight support, compared to traditional gait training [17]. The lack of positive results for treadmill training might be due to heterogeneity in the nature and severity of stroke in these patients, their demographic distribution, variations in intensity and frequency of training, methods for assisting patients, and the placebo effect. More studies are required to adequately address these questions. Given the cost of the equipment, the labor-intensive nature of body weight-supported treadmill training and the uncertain clinical efficacy, the clinical viability of body weight-supported treadmill training in enhancing locomotion in patients with stroke-induced hemiplegia remains unclear [18]. Virtual Reality Interventions. With advances in computer technology and its easy accessibility, virtual reality (VR) has received increasing attention as an interactive method for stroke rehabilitation. With VR rehabilitation, the program aims to create an individualized, simulated rehabilitation scenario in a safe and controlled environment. Recent studies have suggested that 45 to 60 minutes of VR rehabilitation, at a frequency of 3 times per week, can enhance motor recovery in hemiplegic stroke patients [19,20]. Neuroimaging findings suggested that VR-induced cortical reorganization is associated with functional motor recovery in stroke patients [21,22]. However, since some patients may experience transient motion sickness due to visual-vestibular mismatch, there are still some technical challenges to overcome before applying VR rehabilitation to all stroke patients. Large randomized clinical trials to confirm these early finding seem warranted. Therapeutic Electrical Stimulation (TES). Many studies have been conducted to evaluate the efficacy of movement therapy mediated by electrical stimulation. A comprehensive literature review that focused on upper extremity applications showed a positive effect of TES on motor control

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Table 3. Manifestations and Classification of Vascular Aphasic Syndromes Broca Fluency* Content Comprehension

Wernicke

Conduction

TC Motor

TC Sensory

TC Mixed/ Global

Anomic

Optic

Good Poor Poor

Fair-good Good Intact words, simple sentences

Poor Good Intact words, simple sentences

Good Poor Poor

Poor Poor Poor

Good Good Good

Good Good Good

Poor, fluent jargon Worse for nouns Poor

Poor

Good

Good

Good

Good

Fair-good

Fair-good

Poor

Mixed: good; Global: poor Poor

Spelling

Poor Good Intact words, simple sentences Poor, nonfluent Worse for verbs Poor

Poor

Poor

Poor

Poor

Poor

Poor

Associated signs

Right arm weakness, apraxia of speech

Superior visual field cut

May be spared May be spared Abulia

Poor with visual stimuli Good

Reading

May be spared May be spared Poor working memory

Worse for nouns May be spared May be spared

Right visual field cut

Right hemiplegia

Repetition Naming

Poor Right hemianopia

TC ⫽ transcortical. From Hillis [34]. Adapted and reproduced with permission. *Fluency includes grammaticality, prosody, melody, articulatory agility, and rate of speech, which can be differentially affected.

(impairment); however, its effect on functional abilities was inconclusive [23]. A follow-up review suggested that electromyographically triggered electrical stimulation was superior to cyclic stimulation in facilitating the recovery of the hemiparetic upper extremity [24]. In contrast, a quantitative review concluded that there was strong evidence that TES of the lower limb is associated with significant improvements in walking speed of stroke survivors [25]. Additional studies are needed to determine optimal treatment dose and duration, the most effective type(s) of stimulation and patient characteristics that are predictive of treatment success. Robot-aided Therapy. Engineers and clinicians have worked together to develop various robotic devices, with the goal of improving motor recovery in hemiplegic stroke patients [26]. Theoretically, robotic therapy should provide safe, repetitive, and task-specific treatment to improve the function of the affected limb. In a single-blind, randomized, controlled multicenter trial, Feys et al [27] suggested that repetitive, stereotyped movements effected by means of robotic aids improved hemiplegic upper limb function in the acute phase after stroke. However, a recent review by Prange et al [28] found that, although robot-assisted therapy improved motor control of the paretic elbow and shoulder, there were no consistent improvements in actual functional abilities. Cortical Stimulation. Two major types of noninvasive cortical stimulation are used experimentally in stroke rehabilitation: transcranial magnetic stimulation and transcranial direct current stimulation [29-33]. Findings from early studies suggest improvements in motor impairment. However, additional studies are needed to optimize treatment parameters and approaches. While these techniques appear promis-

ing, the potential risk of seizure induction has presented a challenge to patient recruitment. 3.4 Clinical Activity: A 72-year-old man presents with left cortical infarct and aphasia characterized by nonfluent speech, impaired repetition and intact comprehension. Describe the assessment, anatomical localization, classification, treatment, prognosis and the time course of recovery for aphasia. A recent review by Hillis [34] classified vascular aphasia into the following categories: (1) Broca, (2) Wernicke, (3) conduction, (4) transcortical motor, (5) transcortical sensory, (6) transcortical mixed/global, (7) anomic, and (8) optic. The clinical manifestations of various vascular aphasic syndromes are listed in Table 3 [34]. Comprehensive assessment of aphasia must include speech fluency, content, comprehension, repetition, naming, spelling, reading, and observation of associated signs. Judging from the clinical manifestations of this patient with left cortical infarct (nonfluent speech, impaired repetition, but intact comprehension), he most likely has Broca aphasia, with ischemic insult to the left frontal operculum. The anatomic locations of various types of stroke-induced aphasia can be summarized both in tabular format (Table 4) and diagrammatically (Figure 2) [35-42]. In a study of 270 stroke patients with aphasia, the distribution of the various types of stroke-induced aphasia were: Broca 12%, Wernicke 16%, conduction 5%, transcortical motor 2%, transcortical sensory 7%, transcortical global 32%, anomic 25%, and what the researchers term isolation (transcortical mixed) 2% [43]. The severity of aphasia had a tendency to lessen over the first year after stroke. Global aphasia and Broca aphasia (nonfluent) could evolve into

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Table 4. Relationship Between Aphasia Type, Lesion Site, and Arterial Supply Type of Aphasia Broca Wernicke Conduction TC motor TC sensory TC mixed/global Anomic Optic (visual anomia)

Lesion Site

Arterial Supply

Left inferior frontal gyrus, adjacent to the left frontal operculum Left posterior superior portion of the temporal gyrus Left arcuate fasciculus Left prefrontal area Parieto-occipital area, adjacent to the posterior temporal isthmus All of the above Left angular gyrus Left occipital lobe

Middle cerebral artery Middle cerebral artery Middle cerebral artery Anterior cerebral artery Posterior cerebral artery Anterior, middle, posterior cerebral arteries Middle cerebral artery Posterior cerebral artery

TC ⫽ transcortical. Adapted from Albert and Helm-Estabrooks [35].

Wernicke aphasia and anomic aphasia (fluent), respectively. In this classic study, gender, age, or type of aphasia did not influence the outcome for language function. The best predictors of language outcome were initial stroke severity and initial severity of the aphasia. The same group demonstrated that the time course of aphasia recovery parallels that of motor and functional recovery, with the most rapid recovery occurring during the first month with statistical plateau by the end of the third month [44]. Two commonly used methods for treating aphasia are the Functional Communication treatment and the Stimulation approach. The former utilizes environmentally relevant information to enhance speech comprehension, processing, and production [45]. The latter focuses on stimulating the patient to respond to auditory or visual cues [46]. If effective speech production cannot be achieved despite adequate medical and rehabilitative treatments, then assistive devices, such as a communication board, may be prescribed as an alternative form of communication.. Other examples of behavioral strategies include Amer-In code treatment, which consists of about 250 iconic gestural signals for promoting

and stimulating communication [47], and Melodic intonation therapy, which takes advantage of the uninjured right hemisphere to initiate verbal communication [48]. 3.5 Clinical Activity: A 59-year-old man presents with right parietal lobe infarct and impulsivity, poor insight and noncompliance with instructions. Summarize the manifestation of cognitive impairments associated with right parietal lobe lesions and their relation to rehabilitation outcomes. Major cognitive impairments associated with right parietal lobe lesions include left hemispatial neglect, constructional apraxia, dressing apraxia, anosognosia, and inability to visualize overall pattern or gestalt [49,50]. These neurocognitive problems are often associated with reduced motivation to rectify problems that are obvious to others, such as compliance with therapy and basic standards of hygiene [50]. Left hemispatial neglect is manifested by an inability to identify, report, or respond to salient stimuli presented to the left side of the patient (contralateral to the lesion site). For example, patients may leave food untouched in the left visual space,

Figure 2. The anatomic locations of corresponding aphasia syndromes. From Lewis [42]. Adapted from material in public domain.

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Figure 3. Drawings of a clock (a), and of a house (b), copied by a patient with left hemispatial neglect. From Abdullaev and Posner [52]. Reproduced with permission.

groom only the right side of the body and bump into walls on their left side. Several clinical assessment methods—including reading, line bisection and drawing tasks— have been used to identify and quantify the level of neglect [51]. Drawings made by persons with hemispatial neglect have a characteristic absence of detail on the affected side (Figure 3) [52]. While constructional apraxia refers to difficulty with drawing, dressing apraxia represents failure to align the body axis with the direction of the clothing. The lack of awareness to one’s condition in patients with anosognosia is characteristic in patients with right hemisphere infarction. As described by Mesulam [50], this often includes “inappropriate jocularity in response to hemiplegia.” In contrast, patients with left hemisphere infarcts often develop dysphoria. This intriguing observation has led some researchers to hypothesize that the left and right hemispheres have opposite emotional inclinations. Irrespective of the speculations, the perceptual-cognitive impairments associated with right hemisphere infarct, commonly coupled with motivational indifference, could predispose the patients to poor compliance with medications and behavioral rehabilitation programs. Consistent with this notion, 3 independent studies, Gillen [53], Cherney [54], and Katz [55] all identified hemispatial neglect as a predictor of poor functional outcome. 3.6 Clinical Activity: A 53-year-old man with right middle cerebral artery stroke presents with mild extensor tone of the lower limb and complains of tripping over his left foot. On examination he exhibits circumduction and hip hiking to clear his toes during swing and genu recurvatum during stance. Discuss treatment options for improvement of his gait. This patient is demonstrating a gait pattern consistent with Brunnstrom stages 3 or 4 (see Activity 3.1). In persons with a middle cerebral artery stroke, a flexion synergy pattern can be evident in the upper extremity, while an extensor and

equinovarus pattern can be seen in the lower extremity, as described earlier in this chapter. As a patient gains improved motor control out of synergy, a proximal-to-distal recovery pattern is often seen. While improved hip control can allow for a significant increase in gait speed and efficiency, persistent plantar-flexion tone may destabilize the gait cycle. The proper treatment of gait deviation after stroke begins with a thorough evaluation of range of motion, muscle strength and tone both at rest and while ambulating. Severity of tone patterns at the knee and ankle should be measured with the Modified Ashworth Scale (see Study Guide Activity 4.3). To determine whether the tone is primarily in the soleus or in the gastrocnemius muscles, it is essential to evaluate ankle range of motion both with the knee flexed and with it extended. Range of motion examination of the ankle is essential in this case, as long-standing equinovarus tone may have resulted in a soft tissue contracture at the ankle. Manual muscle testing should be performed to appreciate any underlying muscle control that may become unveiled with spasticity treatment. Evaluation of wear patterns on the shoes may also lend clues to degeneration of gait when the patient fatigues. In this case, it is evident that the equinovarus position of the ankle throughout the gait cycle is resulting in several issues. In stance phase, the initial contact occurs with forefoot, which directs the ground reaction force anterior to knee with a resultant extensor moment. Weak hamstring muscles cannot overcome this force and genu recurvatum results. Constant force on the posterior elements of the knee over time may result in joint deformity and pain. In swing phase, the leg is again functionally lengthened due to decreased knee and hip flexion and ankle equinovarus, and in an attempt to avoid tripping on the foot, the patient “hikes” the hip and circumducts the leg. The appropriate management of this patient will depend significantly on the etiology of the disturbance. A severe contracture from fixed ankle plantar flexion may require

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surgical tendon lengthening by an experienced orthopedic surgeon; a contracture that is less significant may respond to an aggressive stretching program and resting splints. However, more recent studies have suggested surgery is a preferred method of treatment even for moderate equinovarus deformity [56]. Spasticity management with specific pharmacologic agents is discussed at length in Chapter 4. If contractures and spasticity are appropriately treated, orthotics can be considered. Ankle foot orthoses (AFOs) in persons with chronic strokes are shown to improve walking speed and stair climbing and also improve patients’ selfconfidence [57]. Traditionally, AFOs have been either made of metal or plastic. Metal AFOs facilitate more fluctuation of limb size, such as in a patient with renal or heart failure; however, they typically require permanent attachment to a single pair of shoes. Plastic AFOs enable a custom fit, weigh less and can be easily adjusted and moved from shoe to shoe, but they provide less control at the ankle compared to metal [58]. Depending on the amount of spasticity and voluntary control at the ankle, a posterior leaf spring or hinged ankle joint may be used in the AFO. While a solid-ankle AFO might assist with toe clearance during swing phase, it should be avoided in the ambulatory patient, because it will inhibit the normal progression of foot flat to toe off during stance phase. Novel devices have been developed to assist in gait deviations. An anterior AFO was shown to improve lateral weight shifting [59] and an in-shoe AFO improved stance phase [60]. For persons with foot-drop but who have adequate knee control, surface peroneal nerve stimulation will increase walking speed [61] and may be equivalent to an AFO [62].

ACKNOWLEDGMENTS The authors thank Sophie Cheng, MD; Gary Abrams, MD; Laura Mendelson, MS; Cari Nicholson, MA, CCC-SLP; Smita Shukla, OTR/L; and John H. Poole, PhD, all of whose expertise gave additional substance to this article.

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