Stroke-related motor outcome measures: Do they quantify the neurophysiological aspects of upper extremity recovery?

+

MODEL

Journal of Bodywork & Movement Therapies (2013) xx, 1e12

Available online at www.sciencedirect.com

ScienceDirect journal homepage: www.elsevier.com/jbmt

STROKE OUTCOME MEASURE: CRITICAL REVIEW

Stroke-related motor outcome measures: Do they quantify the neurophysiological aspects of upper extremity recovery? Shanta Pandian, Superintendent OT (OPD), MOT (Neuro.) , Kamal Narayan Arya, Sr. Occupational Therapist, MOT, PhD* Pandit Deen Dayal Upadhaya Institute for the Physically Handicapped (University of Delhi), Ministry of Social Justice and Empowerment, Govt. of India, 4 VD Marg, New Delhi 110002, India Received 24 August 2013; received in revised form 23 October 2013; accepted 31 October 2013

KEYWORDS Brunnstrom recovery stages; FugleMeyer Assessment; Hemiparesis; Motor recovery; Outcome measures; Stroke rehabilitation; Upper extremity

Summary Various stroke rehabilitation outcome measures are used in clinical and research practice. Severe upper extremity paresis serves as a challenge for the selection of an appropriate outcome measure. No single measure is universally acceptable and sufficient to record the minute clinically important changes. The objectives of the present review were to explore the stroke-specific upper extremity motor outcome measures and to better understand those measures’ ability to quantify upper extremity motor recovery. Seven outcome measures were selected for this review. The criteria used to select outcome measures for this review included performance-based tools that assessed the upper extremity’s voluntary motor control and outcome measures which had been used for the past 10 years. A critical review that referred to motor recovery stages and volitional control was performed. The upper extremity components of each measure were compared with the neurophysiological aspects of recovery (Brunnstrom Recovery Stages) and analyzed for their clinical relevance. The concepts of minimal detectable change and minimal clinically important difference were also considered while examining the outcome measures. The findings of this review reveal that there were very few measures available to precisely assess the upper extremity motor components and volitional control. Most of the measures are functional and performance-based. Only FugleMeyer Assessment was found to explore the individual joint motor control as per the sequential recovery stages. Further, there is a need to develop stroke-specific upper extremity outcome measures. Scoring criteria of the acceptable measures may be modified to discern precise and progressive, but clinically significant motor changes. ª 2013 Elsevier Ltd. All rights reserved.

* Corresponding author. E-mail address: [email protected] (K.N. Arya). 1360-8592/$ - see front matter ª 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jbmt.2013.11.006

Please cite this article in press as: Pandian, S., Arya, K.N., Stroke-related motor outcome measures: Do they quantify the neurophysiological aspects of upper extremity recovery?, Journal of Bodywork & Movement Therapies (2013), http://dx.doi.org/10.1016/ j.jbmt.2013.11.006

+

MODEL

2

Introduction Motor assessment and rehabilitation has always been a challenge in post-stroke hemiparesis. Motor deficits such as muscle weakness, abnormal synergy, and spasticity are commonly assessed among stroke subjects. Recovery occurs rapidly in the lower extremity compared with the upper extremity and the hand. Motor recovery in the upper extremity is a slow and continuous process. In spite of clinically observable changes, it is difficult to quantify the upper extremity recovery at a particular point of time. In addition, severity of paresis, poor recovery, complex movement demands and associated complications interfere with the upper extremity motor assessment (Alt Murphy et al., 2011; Carey et al., 2002). Only 38 percent of stroke clients regain hand functions and fulfill their daily tasks. Even with advanced rehabilitation techniques 11.6 percent of stroke clients achieve functional independence (O0 Sullivan and Schmitz, 2007). An evaluation of even small motor changes is very essential to select and provide a specific motor rehabilitation approach. Since years, various assessment methods have been used in clinical and research practice. However, their reliability, validity and sensitivity have always been a point of research. It is also evident that no single measure is universally acceptable and appropriate to capture the precise as well as clinically significant changes (Baker et al., 2011; J. H. Lin et al., 2009; Lin et al., 2010). The objective of the present study was to review the strokespecific motor assessment tools and to understand their ability to precisely quantify upper extremity motor recovery. The upper extremity movement components of the selected tools were analyzed in the context of post-stroke hemiparetic recovery.

Inclusion criteria for selection of outcome measures Outcome measures that were stroke-specific, performance based, assessed the motor behavior and volitional control, evaluated the upper extremity components or had the subsection for upper extremity and were commonly used in the past 10 years in clinical and research practice were included in the study (Baker et al., 2011). Measures that assessed quality of life and functional independence were excluded from the study. In the present study, on the basis of the inclusion criteria seven assessment tools were selected for the review. The selected measures were FugleMeyer Assessment (FMA), Action Research Arm Test (ARAT), Motor Assessment Scale (MAS), Wolf Motor Function Test (WMFT), Motricity Index (MI), ChedokeeMcMaster Stroke Assessment (CMSA) and Stroke Rehabilitation Assessment of Movement (STREAM) (Diserens et al., 2007; Gladstone et al., 2002; Sullivan et al., 2011). Appendix 1 briefly depicts the items, time of administration and psychometric properties of the measures.

Concepts of minimal detectable change and minimal clinically important difference The focus of the present study was to examine the ability of an outcome measure to precisely quantify the motor

S. Pandian, K.N. Arya changes in post-stroke hemiparesis. Hence, it is pertinent to discuss the related statistical properties. The minimal detectable change (MDC) and minimal clinically important difference (MCID) are key concepts that facilitate the interpretation of treatment outcome in clinical and research practice (Chuang-Stein et al., 2011; Finch et al., 2002; Lin et al., 2011). The MDC signifies the smallest change in an outcome measure and can be detected beyond the measurement error. It is an objective as well as a statistical attribute. The MCID is the smallest change in an outcome measure that would be considered important by the patient or clinician (Schmitt and Di Fabio, 2004). Patients who experience an estimated MCID score are more likely to experience a meaningful improvement in their disability level than those who do not experience such a score (Arya et al., 2011b) The MDC and MCID may provide some information about the minimal motor changes that are assessed by a measure. However, MDC and MCID of each measure in various contexts are sparsely available.

Brunnstrom recovery stage: a reference line for motor recovery assessment In the majority of post-stroke hemiparetic patients, a stereotyped sequence of events takes place during motor recovery. Each higher stage indicates positive recovery. Based on longitudinal observation of many patients, Signe Brunnstrom defined the motor recovery stages. (Sawner and LaVigne, 1992). Six to seven recovery stages each for the upper limb and hand have been described. The stages are given in Box 1 Brunnstrom recovery stage (BRS) is the only strokespecific and commonly used clinical method to classify the level of post-stroke motor recovery. BRS is a subjective method of classification, and it has also been used as an outcome measure in various studies. It is a reliable, valid and responsive measuring tool (Chang et al., 1990; Hashimoto et al., 2007; Huang et al., 2010; Hwang et al., 2005; Lee et al., 2012; Naghdi et al., 2010; Pandian et al., 2012; Safaz et al., 2009; Yavuzer et al., 2008). Brunnstrom Recovery Stage e arm (BRS-A) and Brunnstrom Recovery Stage e hand (BRS-H) were applied to record intrinsic recovery and prognosis of arm and hand in acute stroke. Recovery of the hand usually lags behind the rest of the limb (Chang et al., 1990). A stroke-specific measure should evaluate neuromuscular progress, revealing motor control by the central nervous system. The measure should also be able to detect any motor recovery in relation to the stage. In the present study, the outcome measures were reviewed considering while BRS as a reference line for post-stroke hemiparetic motor recovery.

FugleMeyer Assessment FugleMeyer Assessment (FMA) is the first stroke-specific assessment tool that was developed on the basis of Brunnstrom’s motor recovery stages. It is a feasible, well-designed, responsive, and efficient tool (Fugl-Meyer et al., 1975; Gladstone et al., 2002). The FMA is based on the natural

Please cite this article in press as: Pandian, S., Arya, K.N., Stroke-related motor outcome measures: Do they quantify the neurophysiological aspects of upper extremity recovery?, Journal of Bodywork & Movement Therapies (2013), http://dx.doi.org/10.1016/ j.jbmt.2013.11.006

+

MODEL

Stroke-related motor outcome measures

3

Box-1. Brunnstrom Recovery Stages of the upper limb and hand

Brunnstrom Recovery Stages e arm (BRS-A) Stage 1: Immediately after stroke, there is complete flaccidity, and movement can not be initiated. Stage 2: The basic limb synergies may appear partially or whole with associated reactions. Stage 3: Spasticity becomes most severe at this stage, and all strong components of flexor and extensor synergies appear. Stage 4: Synergy deviates, spasticity reduces and movement combinations with fair motor control start appearing.  Arm moving to forward horizontal position with elbow straight  Taking hand to sacrum without using trunk  Pronationesupination, elbows at 90 and arm adducted

Stage 5: Spasticity reduces, and some more movement combinations with better motor control make their appearance.  Arm moving to side e horizontal position (shoulder 90 abduction) with elbow straight  Moving arm to forward and overhead without trunk compensation  Moving palm up and down with elbow extended and shoulder 90 flexed

Stage 6: Influence of synergy and spasticity almost disappears and movement combinations of stage 5 appear with good motor control. Individual joint movements are well performed in a near-to-normal fashion. Stage 7: Considered the last stage of recovery, near-to-normal motor functions are achieved; very few clients reach this stage. Brunnstrom Recovery Stages e hand (BRS-H) Stage 1: Total flaccidity Stage 2: Little or no active finger flexion with a mild increase in muscle tone. Stage 3: Mass grasp and hook grasp appear without release, only reflex digit extension Stage 4: Lateral prehension, release by thumb movement, and semi-voluntary partial-range finger extension Stage 5: Awkward palmar prehension, cylindrical and spherical grasp, and complete voluntary and partial mass digit extension with less skillful functions Stage 6: Good control of prehensile with more skillful functions, complete voluntary and full extension of digits, individual finger movements possible, less precise than the other side

progression in post-stroke hemiparesis (Dipietro et al., 2007). The upper extremity subsection of FMA (FMA-UE) is commonly used as compared with other parts in post-stroke patients (Michielsen et al., 2011). The FMA-UE comprises 33 items related to the movements of proximal and distal upper extremity. The maximum motor performance score is 66 points for upper extremity. Scoring is done on a 3-point ordinal scale ranging from 0 (item cannot be performed) to 2 (items can be performed faultlessly) by the direct observation of the movement performance. The FMA-UE requires 10e20 min for its administration (Finch et al., 2002; Velozo and Woodbury, 2011). The FMA has exhibited excellent intra-rater and interrater reliability, and validity (Duncan et al., 1983; Sanford et al., 1993; Wood-Dauphinee et al., 1990). Specifically, inter-rater reliability was found to be higher for the upper extremity as compared with the lower extremity (Sullivan et al., 2011) The reliability for other sections of this measure was found to be low as compare to the motor section. The FMA-UE has demonstrated good correlation with ARAT (Page et al., 2012). The responsiveness of FMA was also found to be significantly higher than WMFT, indicating its acceptable concurrent and predictive validity (Fu et al., 2012). The MCID value can be considered a reference value for interpreting the progress in sub-acute stroke (Arya et al., 2011b). The FMA is obviously a reliable and highly recommended measure in clinical and research practice (Aruin et al., 2012; Chae et al., 2002; Dohle et al., 2009;

Duff et al., 2013; Duncan et al., 1983; Gladstone et al., 2002; Kim et al., 2003; Krabben et al., 2012; Kwakkel and Kollen, 2007; Lee et al., 2012; Michaelsen et al., 2011; Ohn et al., 2013; Pandian et al., 2012; Pang et al., 2006; Sanford et al., 1993; Sullivan et al., 2011; Takebayashi et al., 2013; Velozo and Woodbury, 2011; Wu et al., 2013). The FMA-UE assesses the post-stroke subjects as per the sequential recovery stages. The items are hierarchically organized from synergistic to voluntary movements. Synergistic movement exhibits an abnormal stereotyped behavior that does not allow the combination of different movement patterns. For example, an attempt to raise the arm results in elbow flexion, shoulder abduction and internal rotation. The components of flexor and extensor synergy are tested before the movements combining synergies and out of synergy. Further, each item of FMA-UE subsection has multiple components that allow an examination of the wide and complex motor changes (O0 Sullivan and Schmitz, 2007). The FMA-UE items (upper arm) assess reflex activity, voluntary movements within-, combining- and without synergy. Out of 33 FMA-UE items, 15 items are allocated for the wrist and hand, which is an essential part of the upper extremity function. The wrist and hand assessment comprises wrist stability and mobility, finger movements, and varied hand functions ranging from mass grasp to tip-to-tip prehension. The wrist function is tested at different shoulder-elbow positions. In addition, the coordination and

Please cite this article in press as: Pandian, S., Arya, K.N., Stroke-related motor outcome measures: Do they quantify the neurophysiological aspects of upper extremity recovery?, Journal of Bodywork & Movement Therapies (2013), http://dx.doi.org/10.1016/ j.jbmt.2013.11.006

+

MODEL

4 speed hand items assess awkwardness of the upper extremity movements. A subject can only perform the coordinated movements by near-to-normal recovery stage; hence, the item is placed at the end of the FMA-UE subsection (O0 Sullivan and Schmitz, 2007). The FMA-UE has few items that are related to deep tendon reflexes. Although reflex activity is supplementary to the voluntary motor control assessment, its presence does not affect the stability of FMA-UE (Woodbury et al., 2008). Further, some of the reflex items are assessed after a certain stage of recovery (BRS-A stage 5). It would be relevant to test the reflex items initially before flexor synergy using comprehensive scoring criteria. The wrist items are hierarchically placed before the hand and finger. For example, wrist flexionextension is mentioned before the mass grasp. However, components such as wrist circumduction usually appear after good control of the hand components. The scoring criteria of FMA do not quantify every component of motor recovery. For instance, when a patient can perform different degrees (incomplete) of wrist movement and various levels of awkwardness, a score of 1 would be awarded for each performance. A score of 2 would only be awarded when the patient performs faultlessly. There is no scoring criterion for the different types of partial performance (Finch et al., 2002).

Action Research Arm Test The ARAT comprises 19 items in 4 categories: grasp (6 items), grip (4 items), pinch (6 items), and gross movements (3 items). Each item grades from 0 to 3 (0; can perform no part of test and 3; can perform test normally) on a 4-point ordinal scale. The total score of ARAT ranges from 0 to 57; maximum score indicates the absence of upper extremity dysfunction. In the former 3 subscales, the ability to grasp, move and release objects differing in size, weight, and shape is tested. The fourth subtest consists of three gross movements (place hand behind the head, place hand on the top of the head and move hand to mouth) (Van der Lee et al., 2001b). It is a reliable, valid, and standardized functional assessment tool but lacking in its MDC (Connell and Tyson, 2012; Hsieh et al., 2009). The ARAT has demonstrated good correlation with WMFT and FMA (Houwink et al., 2011; Nijland et al., 2010; Platz et al., 2005; Rabadi and Rabadi, 2006). The ARAT measures one aspect of motor recovery and attains only an ordinal score. Further, the sub score is not comparable with the group score. Hence, the individual use of subscale is not recommended. However, ARAT grip and gross sub items are more commonly used as compared to pinch and grasp sub items (Kwakkel and Kollen, 2007; Morris and Van Wijck, 2012). The ARAT items do not assess the voluntary motor control of an individual joint with different movement combinations as per the stroke recovery process. The scoring is based on the successful functional performance of an item rather than on the awkwardness and incoordination between the muscles present during the performance. Lifting of a wooden block of any size is not possible before BRS-A stage 3e4 and BRS-H stage 3. Hence, most of the grasp items (grasp ball, grasp block 5 cm, and grasp block 2.5 cm) were not found suitable for moderate-to-severe hemiparetic subjects. The ARAT evaluates the upper extremity

S. Pandian, K.N. Arya functional abilities rather than the precise movement (Koh et al., 2006; Pandian and Arya, 2012). In spite of having good correlation with FMA, ARAT is less sensitive for assessing the clinical changes over time (Lin et al., 2010; Van der Lee et al., 2001b; Wei et al., 2011). All the subtests of grip that require prehensions can only be assessed at BRS-H stage 5 (awkward prehension). Similarly, pinch subtests can only be performed at BRS-H stage 6 that is described as near to normal (awkwardness). However, the pinch items assess only functional performance rather than awkwardness of the movement. Subtests of gross movements are inadequate to assess movements out of synergy. Other functional tasks with different shoulder, elbow and forearm movement combinations are not being tested in this measure. Further, the gross movement section assesses the upper arm movement in the descending sequence of the hand behind the head, to hand to mouth. If a subject scores 3 in the first item (hand behind the head), a total score of 9 would be given for this section assuming that the other 2 lower level movements are possible. The difficulty level of initially placed items in a subtest allows leaving the gross items placed later in the subtest. Tasks of “hand behind the body” and “place hand on the top of the head” showed poor item sequence (Chen et al., 2012). The item organization is based on the biomechanical aspect rather than on neurophysiological recovery as in a stroke (Connell and Tyson, 2012).

Motor Assessment Scale Motor Assessment Scale (MAS) is a performance-based measure that uses the functional motor activities. It consists of 9 sections (8; motor functions and 1; muscle tone), each section carries 6 levels. Motor functions comprise supine to side lying, supine to sitting over the side of the bed, balanced sitting, sit-to-stand, walking, upper arm functions, hand movements, and advanced hand activities. Hierarchical scoring is done on a 7-point ordinal scale ranging from 0 to 6. The highest score is 54; this means higher functioning on the affected side and the lowest is 0. For example, upper arm function would be awarded a score of 5 when a subject can lift (sitting position) his arm with some external rotation, hold for 10 s, and lower the arm with shoulder external rotation and supination. Similarly, every scoring criterion for all three sections has been specifically defined. Scoring of upper arm function mainly comprises scapular protraction and shoulder flexion in both supine and sitting positions. Similarly, scoring of hand movements consists of wrist extension, radial deviation, pronation-supination, reaching for and picking up an object, and thumb opposition. Advanced hand activities range from holding and manipulating a pen to combing hair at the back of one’s head (Carr et al., 1985). The MAS has demonstrated satisfactory reliability and internal consistency (Lannin, 2004). Good correlation with FMA exhibits its acceptable validity (Poole and Whitney, 1988). The developers of MAS have recommended it for providing feedback regarding motor recovery to patients (Carr et al., 1985). Such a recommendation gives an impression of MAS being a gross motor assessment tool. The MDC and MCID values of MAS have

Please cite this article in press as: Pandian, S., Arya, K.N., Stroke-related motor outcome measures: Do they quantify the neurophysiological aspects of upper extremity recovery?, Journal of Bodywork & Movement Therapies (2013), http://dx.doi.org/10.1016/ j.jbmt.2013.11.006

+

MODEL

Stroke-related motor outcome measures not yet been established. Very few studies have been found to use MAS as an outcome measure (Hayes et al., 2013; Nystrom and Hellstrom, 2013). It has been proposed to be used as a measure in a recent longitudinal multisite randomized trial for maintenance of the motor function after a stroke (Askim et al., 2012). Although some of the item movements are based on usual motor recovery of stroke, they are not analyzed as an individual component. Further, advanced hand activities can only be scored for mild hemiparetic subjects. Inconsistencies in scoring criteria were also exhibited for hand functions and advanced hand activities. Hence, changes in the hierarchical scoring system were suggested for upper limb items in MAS (Sabari et al., 2005).

Wolf motor function test The Wolf Motor Function Test (WMFT) was exclusively developed for post-stroke subjects receiving constraint-induced movement therapy (CIMT). The test is used to quantify motor function in stroke patients with upper extremity (UE) motor deficits (Ang and Man, 2006; Woodbury et al., 2010). It comprises 17 tasks that are sequenced to progressively use more UE joints and include simple to complex movements. The task such as bringing the hand to a table top requires simple movement, whereas lifting a pen needs complex movement. The tasks are performed in a specified manner using a designed template. Scoring is done on 2 bases: time of performance (in seconds) and functional ability (0, no movement to 5, normal movement). The WMFT has exhibited good clinimetric properties in the stroke population (Edwards et al., 2012; J. H. Lin et al., 2009). It demonstrated high inter-rater and intra-rater reliability for both performance time and functional ability scores (Morris et al., 2001). The WMFT showed acceptable criterion validity with FMA among post-stroke patients (Wolf et al., 2001). The MCID of both WMFT time and WMFT functional ability may be used to demonstrate a real change in the recovery (Fritz et al., 2012; K. C. Lin et al., 2009). The WMFT items are organized hierarchically and involve movements from shoulder flexion to fine finger flexion. The items may be regarded as an indicator of the recovery process of post-stroke hemiparesis. However, considering BRSs the motor components can not be assessed systematically using WMFT. Furthermore, most of the items can not be performed by a severe paretic subject (“ConstraintInduced Movement Therapy Research Group. Manual:Graded Wolf Motor Function Test (Revised). University of Alabama at Birmingham and Birmingham Veteran’s Administration Center.,” 2002.). The time scoring focuses on awkwardness and skillfulness, an important aspect of recovery that is usually evident in the later stages of recovery. The scoring criteria of functional ability, have some components of synergy influence (score 3) (“Constraint-Induced Movement Therapy Research Group. Manual:Upper Extremity e Motor Activity Log. University of Alabama at Birmingham and Birmingham Veteran’s Administration Center.,” 2004; Wolf et al., 2001). Statistically, discriminant analysis of WMFT exhibited 86.7% agreement for classifying post-stroke subjects as per BRSs. Furthermore, there was a strong correlation

5 between WMFT, BRSs and FMA (Ang and Man, 2006). The construct validity of WFMT is well supported (Wolf et al., 2001). However, clinically the patient exhibits motor improvements that usually lie between the items. For instance, if the patient achieves some amount of motor control at the wrist and is not able to perform reaching for and lifting items, the functional ability score remains the same. In order to assess a post-stroke patient with severe paresis, a graded version of WMFT was also developed. The version comprises items focusing on the proximal joints with partial control. The items and scoring system were modified into two levels to enable performance and to achieve scoring by subjects having minimal motor control (“Constraint-Induced Movement Therapy Research Group-Manual:Graded Wolf Motor Function Test (Revised), University of Alabama at Birmingham and Birmingham Veteran’s Administration Center.,” 2002). In comparison to the original version, the graded version can discern a few motor components. However, considering the framework of BRS, both the versions are not able to assess stage-specific and precise motor changes.

Motricity Index Motricity Index (MI) is a stroke-specific measure comprising 3 components each for the arm and leg. The components of the arm are pinch grip (using 2.5 cm cube), maximum 67 points; elbow flexion (from 90 touching shoulder), maximum 14 points; and shoulder abduction (from flexed elbow off the chest), maximum 19 points. The total score of arm components is 100 points, whereas minimum is 0. The MI was found to be a responsive tool when compared with the BRS. The effect size (magnitude of a treatment effect) for BRS was recorded as .97, whereas for MI, the score was .91 (Safaz et al., 2009). The MI has been used as an outcome measure along with other responsive measures (Cho et al., 2007; Kwakkel and Kollen, 2007; Platz et al., 2008). Clinically, the scoring criteria for this measure are not convenient for the assessor. Furthermore, MI does not follow a sequential pattern of motor recovery. It is possible to perform pinch grip only after BRS-H stage 5. As per the sequential motor recovery process, awkwardness persists till the last stage of recovery and holding a 2.5 cm of cube between the thumb and forefingers can only be performed after BRS-H stage 6. It is a well established fact that BRS-H stage 6 can not be achieved before BRS-A stage 6 (Pandian and Arya, 2012). These are considered the last stages of recovery; hence, the score will be 0 during the initial stages. Therefore, the measure is relatively less popular in the clinical and research field as compared with the other motor-specific measures. The second component, elbow 90 horizontal and touching the shoulder, is the stereotypical synergy pattern. Abduction of shoulder and elbow 90 are the strongest components of synergy. Elbow extension with different angles of shoulder movements are not a part of MI. As per BRS-A stage 4e6, these are the few important movements that are used to record voluntary motor control. Shoulder abduction (flexed elbow off the chest) does not test the voluntary motor control of an individual joint. Shoulder forward horizontal position with elbow 0 (not a part of this measure) appears earlier than

Please cite this article in press as: Pandian, S., Arya, K.N., Stroke-related motor outcome measures: Do they quantify the neurophysiological aspects of upper extremity recovery?, Journal of Bodywork & Movement Therapies (2013), http://dx.doi.org/10.1016/ j.jbmt.2013.11.006

+

MODEL

6 the said component. The assessment tool does not specify the individual motor component as per the neurophysiological recovery process (Finch et al., 2002).

ChedokeeMc Master Stroke Assessment Scale ChedokeeMc Master Stroke Assessment Scale (CMSA) is a 2part assessment scale: impairment inventory and disability inventory. Impairment inventory has six dimensions: shoulder pain, postural control, arm movement and foot movement. Each dimension except shoulder pain is rated on a 7-point ordinal scale corresponding to the seven stages of BRS. The shoulder pain rating scale is unique and relates to its severity. The maximum total score of physical impairment is 42. Disability inventory is purely functional and is based with 10 gross motor items and 5 walking items. Each activity is scored out of 7, similar to functional independence measure criteria. Although a few studies confirmed its reliability and validity, a large error was demonstrated in the second part, doubting its predictive validity (Dang et al., 2011; Gowland et al., 1993). The outcome measure was found to be broad, complex, and time taking; hence, it was less popular in clinical practice. Motor recovery as assessed by CMSA (arm and hand subsection of impairment inventory) basically categorizes the impairment rather than objectively identifying and quantifying the specific motor impairment. The arm subsection comprises seven stages; the highest stage is given when the subject can perform at least 2 out of 3 items that are designated for the stage. For example, to be at stage 5, the client should be able to perform at least 2 items from (a) flexion synergy, then extensor synergy, (b) shoulder abduction to 90 with pronation, and (c) shoulder flexion to 90 : pronation and then supination. This criterion for scoring is very subjective and gross. The flexion and extension synergies comprise a broad range of upper extremity movements that cannot be evaluated in a single item. Some of the CMSA stages are not based on hierarchical motor recovery: stage 4, which requires finger extension and then flexion, and stage 5, where finger flexion followed by extension is linked in reverse order. Although most of the items/stages are organized in relation to the motor recovery process, the measure lacks clarity in the type of movement and scoring criteria. Very few studies, the majority from Canada, have used this tool as an outcome measure for the trunk and limbs (Hacmon et al., 2012).

Stroke Rehabilitation Assessment of Movement The Stroke Rehabilitation Assessment of Movement (STREAM) was developed to measure voluntary movement and basic mobility in a stroke. It comprises 30 items, 10 each for voluntary motor ability of the upper extremity and lower extremity, and 10 items for basic mobility. A 3-point (0, unable to perform the movement to 2, able to perform the movement in a manner that is comparable to the sound side) ordinal scale is used for scoring voluntary movement of the extremities (Ahmed et al., 2003; Daley et al., 1999). The STREAM exhibited acceptable inter-rater agreement on scores for individual items. It also demonstrated very high inter-rater reliability for total and sub scores. Excellent validity was found when it was compared with the

S. Pandian, K.N. Arya score of FMA (Wang et al., 2002). It has also shown good convergent and predictive validity in relation to Barthel Index (Hsueh et al., 2003). Similar psychometric properties were found in relation to Functional Independence Measure and Stoke Impact Scale in an acute-stage patient (Ward et al., 2011). The upper extremity items such as scapular protraction, and hand behind the body adequately focus on the recovery of the upper arm. However, the hand, an important aspect of recovery, has not been given enough consideration in the measure. STREAM only assesses the closing and opening of the hand and thumb opposition. There is no item that evaluates the wrist control. The recommended testing postures are supine and sitting. The scapular protraction and elbow extension are to be tested in supine position, whereas other items such as scapular elevation and forearm pronationesupination are to be tested in sitting position. The scoring is done on 3-point scale with a maximum score of 20 for the UE subscale. The criteria also assess the quality (deviation/normal) and magnitude (partial/complete) of performed movement. The score of 1 is divided into 3 categories: 1a (partial and marked deviation), 1b (partial and no deviation) and 1c (complete and marked deviation). This gives an accurate presentation of a specific item. However, the total score will be same, irrespective of the category (Ahmed et al., 2003; Daley et al., 1999). The STREAM has been modified to a short and simplified version with only five items for the UE subscale (Y. W. Hsieh et al., 2007; Hsueh et al., 2006). The subscale comprises scapular protraction, elbow extension, raising arm to fullest elevation, making a fist and total extension of fingers. Although the modified version demonstrated good discriminative and predictive abilities, clinically, it lacks ability to comment on the status and recovery of the specific movement component. In spite of the shortcomings, STREAM has been used in many recent stroke rehabilitation studies (Likhi et al., 2013).

Discussion Various stroke-specific outcome measures are being used in clinical and research practice. However, very few measures are available to exclusively assess the upper extremity motor recovery (Finch et al., 2002). The upper limb motor impairments are more severe and challenging than the lower extremity impairments in post-stroke hemiparesis (O0 Sullivan and Schmitz, 2007). Hence, the outcome measure should accurately and specifically judge the upper limb motor issues. As per the literature review, no measure other than BRS and FMA assesses individual motor components. Furthermore, the other outcome measures are not exclusively motor specific. Most of the measures assess either the entire affected body side with a few upper extremity components or functional performance only. Further, various voluntary motor components are not analyzed appropriately, providing an incomplete motor presentation of a post-stroke subject. In a stroke, even a small amount of motor recovery is a big achievement clinically, which does not get reflected in most of the standardized assessments (Shumway-Cook and Woollacott, 2007). The motor treatment plan based on such an assessment might lead to exaggeration of an abnormal synergy

Please cite this article in press as: Pandian, S., Arya, K.N., Stroke-related motor outcome measures: Do they quantify the neurophysiological aspects of upper extremity recovery?, Journal of Bodywork & Movement Therapies (2013), http://dx.doi.org/10.1016/ j.jbmt.2013.11.006

+

MODEL

Stroke-related motor outcome measures pattern. In addition, most of the measures are not appropriate for all types of severity and motor recovery stages. A hemiparetic subject achieves the upper extremity motor recovery in an incremental and step-wise process (Sawner and LaVigne, 1992). It is necessary to examine the motor control of an individual movement in an objective treatment plan. Clinically, only FMA has been found to document the motor control of an individual movement component. Other scales are either function or therapy based. For instance, WFMT is solely based on CIMT; if a subject is not suitable to receive the technique, then it would not be appropriate to apply the measure. The MAS is not evident to exclusively assess the upper extremity. This measure exhibits the motor status of the subject as a whole rather than the motor level of the affected upper extremity (Sabari et al., 2005). Loss of voluntary motor control is one of the key challenges in post-stroke hemiparesis. Post-stroke subjects exhibit a variation in the type and severity of motor loss. Depending on the severity, an outcome measure may be inappropriate to assess the impairment. For instance, in mild hemiparetic subjects, pinch items of ARAT may be partially or fully performed; however, a severely paralyzed subject would not be able to perform majority of the ARAT items during the prolonged recovery period (Van der Lee et al., 2001b). Further, no floor and ceiling effects have been found for ARAT (Houwink et al., 2011; Nijland et al., 2010). The 4-point ordinal scale has been found to be disordered in its rating (H. F. Chen et al., 2012). In contrast, changes in FMA score may be observed even for a severely paralyzed hand progressing toward voluntary motor response (Velozo and Woodbury, 2011). It is recommended to revise ARAT considering the type of items and interval scale properties (Koh et al., 2006). Stroke rehabilitation has been evolving very rapidly during the last few decades. Initially, motor rehabilitation focused on intrinsic recovery utilizing different neurophysiological approaches such as Brunnstrom’s movement therapy, Neurodevelopmental technique and Proprioceptive neuromuscular facilitation technique. However, due to a lack of evidence for most of the neurophysiological approaches, the use of outcome measures such as FMA has been reduced (Stein et al., 2009). Traditionally, the intrinsic recovery was supposed to occur during acute and subacute phases and cease at the chronic stage of a stroke. Such concepts forced the practitioners to consider the contemporary approaches that entirely depend on the various compensatory rehabilitative principles. The wide spread use of the approaches made the outcome measures such as ARAT and MAS popular in clinical practice (Carr and Shephered, 1987). Recent motor control theories have changed the various concepts related to intrinsic neurological recovery. The current concept of neuroplasticity emphasized the synaptogenesis, neural regeneration and cortical reorganization even many years after stroke (Richards et al., 2008). The concept has rejuvenated the intervention and assessments based on intrinsic recovery. This has encouraged the use of FMA in clinical and research practice even after more than 35 years of its development (Fugl-Meyer et al., 1975). Clinically, only a few outcome measures are appropriate at most of the post-stroke recovery stages. The FMA has been found to be applied at any stage/chronicity, which could be the reason for its wide

7 acceptance. Although FMA is the most practical and useful in assessing motor recovery processes, there are a few limitations in the measure. For instance, the scoring criterion is only 3-point based; thus, observed motor recovery between 2 successive points can not be scored. In addition, scoring criteria for testing dysmetria/tremor are not justified. A subject with either marked incoordination or no/ poor voluntary control will score 0 for the item. The CIMT is applicable only in subjects having 20-degree wrist extension and 10-degree finger extension (Morris et al., 2006; Sirtori et al., 2009; Wolf et al., 2006). However, most of the post-stroke hemiparetic subjects do not reach this level of the hand recovery and, therefore, may not be eligible for CIMT (Arya et al., in press; Sawner and LaVigne, 1992; Wolf, 2007). Consequently, the use of WMFT becomes limited in spite of having excellent internal consistency, testeretest reliability, and adequate stability (Morris et al., 2001). Although, MAS and MI comprise three items each, can be quickly applied, they only assess the gross and subjective motor recovery of upper extremity. They can only be used as a screening tool. Similar to BRS, CMSA can only classify the post-stroke hemiparetic subjects into different recovery stages rather than assessing precise motor control (Dang et al., 2011). The STREAM comprises upper arm movements related to stroke recovery stages; however, the items for wrist and hand are negligible. Considering the other measures except FMA, the STREAM can also be used to assess the motor recovery stage of upper extremity (Ahmed et al., 2003). The MDC and MCID and other psychometric/clinometric properties of most of the outcome measures are available. Both values may be considered as reference points for clinical decision making (K. C. Lin et al., 2009). However, statistical acceptance is not enough to quantify the complex upper extremity motor changes among post-stroke hemiparesis.

Conclusion The present review reveals that very few measures are available to precisely assess the upper extremity components and voluntary motor control. There is still a need to develop an upper extremity specific outcome measure considering the neurophysiological aspect of stroke recovery. The scoring criteria of the available measures may be modified to assess the possible minimal changes during motor recovery.

References Ahmed, S., Mayo, N.E., Higgins, J., Salbach, N.M., Finch, L., WoodDauphinee, S.L., 2003. The Stroke Rehabilitation Assessment of Movement (STREAM): a comparison with other measures used to evaluate effects of stroke and rehabilitation. Phys. Ther. 83 (7), 617e630. Alt Murphy, M., Willen, C., Sunnerhagen, K.S., 2011. Kinematic variables quantifying upper-extremity performance after stroke during reaching and drinking from a glass. Neurorehabil. Neural Repair 25 (1), 71e80.

Please cite this article in press as: Pandian, S., Arya, K.N., Stroke-related motor outcome measures: Do they quantify the neurophysiological aspects of upper extremity recovery?, Journal of Bodywork & Movement Therapies (2013), http://dx.doi.org/10.1016/ j.jbmt.2013.11.006

+

MODEL

8 Ang, J.H., Man, D.W., 2006. The discriminative power of the Wolf motor function test in assessing upper extremity functions in persons with stroke. Int. J. Rehabil. Res. 29 (4), 357e361. Aruin, A.S., Rao, N., Sharma, A., Chaudhuri, G., 2012. Compelled body weight shift approach in rehabilitation of individuals with chronic stroke. Top Stroke Rehabil. 19 (6), 556e563. Arya, K.N., Pandian, S., Verma, R., Garg, R.K., 2011a. Movement therapy induced neural reorganization and motor recovery in Stroke: a review. J. Body Work Movement Ther. 15, 528e537. Arya, K.N., Verma, R., Garg, R.K., 2011b. Estimating the minimal clinically important difference of an upper extremity recovery measure in subacute stroke patients. Top Stroke Rehabil. 18 (Suppl. 1), 599e610. Askim, T., Langhammer, B., Ihle-Hansen, H., Magnussen, J., Engstad, T., Indredavik, B., 2012. A long-term follow-up programme for maintenance of motor function after stroke: protocol of the life after stroke-the last study. Stroke Res. Treat. 2012, 392101. Baker, K., Cano, S.J., Playford, E.D., 2011. Outcome measurement in stroke: a scale selection strategy. Stroke 42 (6), 1787e1794. Bogard, K., Wolf, S., Zhang, Q., Thompson, P., Morris, D., NicholsLarsen, D., 2009. Can the wolf motor function test be streamlined? Neurorehabil. Neural Repair 23 (5), 422e428. Carey, L.M., Matyas, T.A., Oke, L.E., 2002. Evaluation of impaired fingertip texture discrimination and wrist position sense in patients affected by stroke: comparison of clinical and new quantitative measures. J. Hand Ther. 15 (1), 71e82. Carr, J.H., Shepherd, R.B., Nordholm, L., Lynne, D., 1985. Investigation of a new motor assessment scale for stroke patients. Phys. Ther. 65 (2), 175e180. Carr, J.H., Shephered, R.B., 1987. A Motor Relaerning Programme for Stroke. Aspen Systems Corporation, Michigan. Chae, J., Yang, G., Park, B.K., Labatia, I., 2002. Muscle weakness and cocontraction in upper limb hemiparesis: relationship to motor impairment and physical disability. Neurorehabil. Neural Repair 16 (3), 241e248. Chang, J.J., Sung, Y.T., Lin, Y.T., 1990. The relationship between early motor stage and hand function recovery six months after stroke. Gaoxiong Yi Xue Ke Xue Za Zhi 6 (1), 38e44. Chen, H.F., Lin, K.C., Wu, C.Y., Chen, C.L., 2012. Rasch validation and predictive validity of the action research arm test in patients receiving stroke rehabilitation. Arch. Phys. Med. Rehabil. 93 (6), 1039e1045. Chen, H.M., Hsieh, C.L., Sing Kai, L., Liaw, L.J., Chen, S.M., Lin, J.H., 2007. The test-retest reliability of 2 mobility performance tests in patients with chronic stroke. Neurorehabil. Neural Repair 21 (4), 347e352. Cho, S.H., Kim, D.G., Kim, D.S., Kim, Y.H., Lee, C.H., Jang, S.H., 2007. Motor outcome according to the integrity of the corticospinal tract determined by diffusion tensor tractography in the early stage of corona radiata infarct. Neurosci. Lett. 426 (2), 123e127. Chuang-Stein, C., Kirby, S., Hirsch, I., Atkinson, G., 2011. The role of the minimum clinically important difference and its impact on designing a trial. Pharm. Stat. 10 (3), 250e256. Collin, C., Wade, D., 1990. Assessing motor impairment after stroke: a pilot reliability study. J. Neurol. Neurosurg. Psychiatry 53 (7), 576e579. Connell, L.A., Tyson, S.F., 2012. Clinical reality of measuring upper-limb ability in neurologic conditions: a systematic review. Arch. Phys. Med. Rehabil. 93 (2), 221e228. Constraint-Induced Movement Therapy Research Group, 2002. Manual:Graded Wolf Motor Function Test (Revised). University of Alabama at Birmingham and Birmingham Veteran’s Administration Center. Constraint-Induced Movement Therapy Research Group, 2004. Manual:Upper Extremity e Motor Activity Log. University of Alabama at Birmingham and Birmingham Veteran’s Administration Center.

S. Pandian, K.N. Arya Daley, K., Mayo, N., Wood-Dauphinee, S., 1999. Reliability of scores on the Stroke Rehabilitation Assessment of Movement (STREAM) measure. Phys. Ther. 79 (1), 8e19. Dang, M., Ramsaran, K.D., Street, M.E., Syed, S.N., BarclayGoddard, R., Stratford, P.W., et al., 2011. Estimating the accuracy of the Chedoke-McMaster stroke assessment predictive equations for stroke rehabilitation. Physiother. Can. 63 (3), 334e341. Dipietro, L., Krebs, H.I., Fasoli, S.E., Volpe, B.T., Stein, J., Bever, C., et al., 2007. Changing motor synergies in chronic stroke. J. Neurophysiol. 98 (2), 757e768. Diserens, K., Perret, N., Chatelain, S., Bashir, S., Ruegg, D., Vuadens, P., et al., 2007. The effect of repetitive arm cycling on post stroke spasticity and motor control: repetitive arm cycling and spasticity. J. Neurol. Sci. 253 (1e2), 18e24. Dohle, C., Pullen, J., Nakaten, A., Kust, J., Rietz, C., Karbe, H., 2009. Mirror therapy promotes recovery from severe hemiparesis: a randomized controlled trial. Neurorehabil. Neural Repair 23 (3), 209e217. Duff, M., Chen, Y., Cheng, L., Liu, S.M., Blake, P., Wolf, S.L., et al., 2013. Adaptive mixed reality rehabilitation improves quality of reaching movements more than traditional reaching therapy following stroke. Neurorehabil. Neural Repair 27 (4), 306e315. Duncan, P.W., Propst, M., Nelson, S.G., 1983. Reliability of the Fugl-Meyer assessment of sensorimotor recovery following cerebrovascular accident. Phys. Ther. 63 (10), 1606e1610. Edwards, D.F., Lang, C.E., Wagner, J.M., Birkenmeier, R., Dromerick, A.W., 2012. An evaluation of the Wolf Motor Function Test in motor trials early after stroke. Arch. Phys. Med. Rehabil. 93 (4), 660e668. Finch, E., Brooks, D., Stratford, P.W., Mayo, E.N., 2002. Physical Rehabilitation Outcome Measures: a Guide to Enhanced Clinical Decision Making, second ed. Canadian Physiotherapy Association, Ontario. Fritz, S.L., Butts, R.J., Wolf, S.L., 2012. Constraint-induced movement therapy: from history to plasticity. Expert Rev. Neurother. 12 (2), 191e198. Fu, T.S., Wu, C.Y., Lin, K.C., Hsieh, C.J., Liu, J.S., Wang, T.N., et al., 2012. Psychometric comparison of the shortened FuglMeyer Assessment and the streamlined Wolf Motor Function Test in stroke rehabilitation. Clin. Rehabil. 26 (11), 1043e1047. Fugl-Meyer, A.R., Jaasko, L., Leyman, I., Olsson, S., Steglind, S., 1975. The post-stroke hemiplegic patient. 1. A method for evaluation of physical performance. Scand. J. Rehabil. Med. 7 (1), 13e31. Gladstone, D.J., Danells, C.J., Black, S.E., 2002. The fugl-meyer assessment of motor recovery after stroke: a critical review of its measurement properties. Neurorehabil. Neural Repair 16 (3), 232e240. Gowland, C., Stratford, P., Ward, M., Moreland, J., Torresin, W., Van Hullenaar, S., et al., 1993. Measuring physical impairment and disability with the Chedoke-McMaster Stroke Assessment. Stroke 24 (1), 58e63. Hacmon, R.R., Krasovsky, T., Lamontagne, A., Levin, M.F., 2012. Deficits in intersegmental trunk coordination during walking are related to clinical balance and gait function in chronic stroke. J. Neurol. Phys. Ther. 36 (4), 173e181. Hashimoto, K., Higuchi, K., Nakayama, Y., Abo, M., 2007. Ability for basic movement as an early predictor of functioning related to activities of daily living in stroke patients. Neurorehabil. Neural Repair 21 (4), 353e357. Hayes, S., Donnellan, C., Stokes, E., 2013. Associations between executive function and physical function poststroke: a pilot study. Physiotherapy 99 (2), 165e171. Houwink, A., Roorda, L.D., Smits, W., Molenaar, I.W., Geurts, A.C., 2011. Measuring upper limb capacity in patients after stroke:

Please cite this article in press as: Pandian, S., Arya, K.N., Stroke-related motor outcome measures: Do they quantify the neurophysiological aspects of upper extremity recovery?, Journal of Bodywork & Movement Therapies (2013), http://dx.doi.org/10.1016/ j.jbmt.2013.11.006

+

MODEL

Stroke-related motor outcome measures reliability and validity of the stroke upper limb capacity scale. Arch. Phys. Med. Rehabil. 92 (9), 1418e1422. Hsieh, C.L., Hsueh, I.P., Chiang, F.M., Lin, P.H., 1998. Inter-rater reliability and validity of the action research arm test in stroke patients. Age Ageing 27 (2), 107e113. Hsieh, Y.W., Lin, J.H., Wang, C.H., Sheu, C.F., Hsueh, I.P., Hsieh, C.L., 2007. Discriminative, predictive and evaluative properties of the simplified stroke rehabilitation assessment of movement instrument in patients with stroke. J. Rehabil. Med. 39 (6), 454e460. Hsieh, Y.W., Wang, C.H., Sheu, C.F., Hsueh, I.P., Hsieh, C.L., 2008. Estimating the minimal clinically important difference of the Stroke Rehabilitation Assessment of Movement measure. Neurorehabil. Neural Repair 22 (6), 723e727. Hsieh, Y.W., Wu, C.Y., Lin, K.C., Chang, Y.F., Chen, C.L., Liu, J.S., 2009. Responsiveness and validity of three outcome measures of motor function after stroke rehabilitation. Stroke 40 (4), 1386e1391. Hsueh, I.P., Wang, C.H., Sheu, C.F., Hsieh, C.L., 2003. Comparison of psychometric properties of three mobility measures for patients with stroke. Stroke 34 (7), 1741e1745. Hsueh, I.P., Wang, W.C., Wang, C.H., Sheu, C.F., Lo, S.K., Lin, J.H., et al., 2006. A simplified stroke rehabilitation assessment of movement instrument. Phys. Ther. 86 (7), 936e943. Huang, Y.C., Liang, P.J., Pong, Y.P., Leong, C.P., Tseng, C.H., 2010. Physical findings and sonography of hemiplegic shoulder in patients after acute stroke during rehabilitation. J. Rehabil. Med. 42 (1), 21e26. Hwang, I.S., Tung, L.C., Yang, J.F., Chen, Y.C., Yeh, C.Y., Wang, C.H., 2005. Electromyographic analyses of global synkinesis in the paretic upper limb after stroke. Phys. Ther. 85 (8), 755e765. Kim, S.H., Pohl, P.S., Luchies, C.W., Stylianou, A.P., Won, Y., 2003. Ipsilateral deficits of targeted movements after stroke. Arch. Phys. Med. Rehabil. 84 (5), 719e724. Koh, C.L., Hsueh, I.P., Wang, W.C., Sheu, C.F., Yu, T.Y., Wang, C.H., et al., 2006. Validation of the action research arm test using item response theory in patients after stroke. J. Rehabil. Med. 38 (6), 375e380. Krabben, T., Prange, G.B., Molier, B.I., Stienen, A.H., Jannink, M.J., Buurke, J.H., et al., 2012. Influence of gravity compensation training on synergistic movement patterns of the upper extremity after stroke, a pilot study. J. Neuroeng Rehabil. 9 (44). Kwakkel, G., Kollen, B., 2007. Predicting improvement in the upper paretic limb after stroke: a longitudinal prospective study. Restor Neurol. Neurosci. 25 (5e6), 453e460. Lannin, N., 2004. Reliability, validity and factor structure of the upper limb subscale of the Motor Assessment Scale (UL-MAS) in adults following stroke. Disabil. Rehabil. 26 (2), 109e116. Lee, M.M., Cho, H.Y., Song, C.H., 2012. The mirror therapy program enhances upper-limb motor recovery and motor function in acute stroke patients. Am. J. Phys. Med. Rehabil. 91 (8), 689e696. Likhi, M., Jidesh, V.V., Kanagaraj, R., George, J.K., 2013. Does trunk, arm, or leg control correlate best with overall function in stroke subjects? Top Stroke Rehabil. 20 (1), 62e67. Lin, J.H., Hsu, M.J., Sheu, C.F., Wu, T.S., Lin, R.T., Chen, C.H., et al., 2009. Psychometric comparisons of 4 measures for assessing upper-extremity function in people with stroke. Phys. Ther. 89 (8), 840e850. Lin, K.C., Chuang, L.L., Wu, C.Y., Hsieh, Y.W., Chang, W.Y., 2010. Responsiveness and validity of three dexterous function measures in stroke rehabilitation. J. Rehabil. Res. Dev. 47 (6), 563e571. Lin, K.C., Fu, T., Wu, C.Y., Hsieh, C.J., 2011. Assessing the strokespecific quality of life for outcome measurement in stroke rehabilitation: minimal detectable change and clinically important difference. Health Qual. Life Outcomes 9 (5).

9 Lin, K.C., Hsieh, Y.W., Wu, C.Y., Chen, C.L., Jang, Y., Liu, J.S., 2009. Minimal detectable change and clinically important difference of the Wolf Motor Function Test in stroke patients. Neurorehabil. Neural Repair 23 (5), 429e434. Loewen, S.C., Anderson, B.A., 1990. Predictors of stroke outcome using objective measurement scales. Stroke 21 (1), 78e81. Malouin, F., Pichard, L., Bonneau, C., Durand, A., Corriveau, D., 1994. Evaluating motor recovery early after stroke: comparison of the Fugl-Meyer Assessment and the Motor Assessment Scale. Arch. Phys. Med. Rehabil. 75 (11), 1206e1212. Mao, H.F., Hsueh, I.P., Tang, P.F., Sheu, C.F., Hsieh, C.L., 2002. Analysis and comparison of the psychometric properties of three balance measures for stroke patients. Stroke 33 (4), 1022e1027. Michaelsen, S.M., Rocha, A.S., Knabben, R.J., Rodrigues, L.P., Fernandes, C.G., 2011. Translation, adaptation and inter-rater reliability of the administration manual for the Fugl-Meyer assessment. Rev. Bras Fisioter. 15 (1), 80e88. Michielsen, M.E., Selles, R.W., van der Geest, J.N., Eckhardt, M., Yavuzer, G., Stam, H.J., et al., 2011. Motor recovery and cortical reorganization after mirror therapy in chronic stroke patients: a phase II randomized controlled trial. Neurorehabil. Neural Repair 25 (3), 223e233. Morris, D.M., Taub, E., Mark, V.W., 2006. Constraint-induced movement therapy: characterizing the intervention protocol. Eura Medicophys. 42 (3), 257e268. Morris, D.M., Uswatte, G., Crago, J.E., Cook 3rd, E.W., Taub, E., 2001. The reliability of the wolf motor function test for assessing upper extremity function after stroke. Arch. Phys. Med. Rehabil. 82 (6), 750e755. Morris, J.H., Van Wijck, F., 2012. Responses of the less affected arm to bilateral upper limb task training in early rehabilitation after stroke: a randomized controlled trial. Arch. Phys. Med. Rehabil. 93 (7), 1129e1137. Naghdi, S., Ansari, N.N., Mansouri, K., Hasson, S., 2010. A neurophysiological and clinical study of Brunnstrom recovery stages in the upper limb stroke. Brain Inj. 24 (11), 1372e1378. Nijland, R., van Wegen, E., Verbunt, J., van Wijk, R., van Kordelaar, J., Kwakkel, G., 2010. A comparison of two validated tests for upper limb function after stroke: the Wolf Motor Function Test and the Action Research Arm Test. J. Rehabil. Med. 42 (7), 694e696. Nystrom, A., Hellstrom, K., 2013. Fall risk six weeks from onset of stroke and the ability of the Prediction of Falls in Rehabilitation Settings Tool and motor function to predict falls. Clin. Rehabil. 27 (5), 473e479. O’Sullivan, S.B., Schmitz, T.J., 2007. Physical Rehabilitation, fifth ed. Jaypee, New Delhi. Ohn, S.H., Yoo, W.K., Kim, D.Y., Ahn, S., Jung, B., Choi, I., et al., 2013. Measurement of synergy and spasticity during functional movement of the post-stoke hemiplegic upper limb. J. Electromyogr. Kinesiol. 23 (2), 501e507. Page, S.J., Levine, P., Hade, E., 2012. Psychometric properties and administration of the Wrist/Hand subscales of the fuglmeyer assessment in minimally impaired upper extremity hemiparesis in stroke. Arch. Phys. Med. Rehabil. 93 (12), 2373e2376. Pandian, S., Arya, K.N., 2012. Relation between the upper extremity synergistic movement components and its implication for motor recovery in poststroke hemiparesis. Top Stroke Rehabil. 19 (6), 545e555. Pandian, S., Arya, K.N., Davidson, E.W., 2012. Comparison of Brunnstrom movement therapy and motor relearning program in rehabilitation of post-stroke hemiparetic hand: a randomized trial. J. Bodyw Mov Ther. 16 (3), 330e337. Pang, M.Y., Harris, J.E., Eng, J.J., 2006. A community-based upper-extremity group exercise program improves motor function and performance of functional activities in chronic

Please cite this article in press as: Pandian, S., Arya, K.N., Stroke-related motor outcome measures: Do they quantify the neurophysiological aspects of upper extremity recovery?, Journal of Bodywork & Movement Therapies (2013), http://dx.doi.org/10.1016/ j.jbmt.2013.11.006

+

MODEL

10 stroke: a randomized controlled trial. Arch. Phys. Med. Rehabil. 87 (1), 1e9. Platz, T., Pinkowski, C., van Wijck, F., Kim, I.H., di Bella, P., Johnson, G., 2005. Reliability and validity of arm function assessment with standardized guidelines for the Fugl-Meyer Test, Action Research Arm Test and Box and Block Test: a multicentre study. Clin. Rehabil. 19 (4), 404e411. Platz, T., Vuadens, P., Eickhof, C., Arnold, P., Van Kaick, S., Heise, K., 2008. REPAS, a summary rating scale for resistance to passive movement: item selection, reliability and validity. Disabil. Rehabil. 30 (1), 44e53. Poole, J.L., Whitney, S.L., 1988. Motor assessment scale for stroke patients: concurrent validity and interrater reliability. Arch. Phys. Med. Rehabil. 69 (3 Pt 1), 195e197. Rabadi, M.H., Rabadi, F.M., 2006. Comparison of the action research arm test and the Fugl-Meyer assessment as measures of upper-extremity motor weakness after stroke. Arch. Phys. Med. Rehabil. 87 (7), 962e966. Richards, L., Hanson, C., Wellborn, M., Sethi, A., 2008. Driving motor recovery after stroke. Top Stroke Rehabil. 15 (5), 397e411. Sabari, J.S., Lim, A.L., Velozo, C.A., Lehman, L., Kieran, O., Lai, J.S., 2005. Assessing arm and hand function after stroke: a validity test of the hierarchical scoring system used in the motor assessment scale for stroke. Arch. Phys. Med. Rehabil. 86 (8), 1609e1615. Safaz, I., Yilmaz, B., Yasar, E., Alaca, R., 2009. Brunnstrom recovery stage and motricity index for the evaluation of upper extremity in stroke: analysis for correlation and responsiveness. Int. J. Rehabil. Res. 32 (3), 228e231. Sanford, J., Moreland, J., Swanson, L.R., Stratford, P.W., Gowland, C., 1993. Reliability of the Fugl-Meyer assessment for testing motor performance in patients following stroke. Phys. Ther. 73 (7), 447e454. Sawner, K., LaVigne, J., 1992. Brunnstrom’s Movement Therapy in Hemiplegia: a Neurophysiological Approach, second ed. JB Lippincott, Philadelphia. Schmitt, J.S., Di Fabio, R.P., 2004. Reliable change and minimum important difference (MID) proportions facilitated group responsiveness comparisons using individual threshold criteria. J. Clin. Epidemiol. 57 (10), 1008e1018. Shelton, F.D., Volpe, B.T., Reding, M., 2001. Motor impairment as a predictor of functional recovery and guide to rehabilitation treatment after stroke. Neurorehabil. Neural Repair 15 (3), 229e237. Shumway-Cook, A., Woollacott, Marjorie H., 2007. Motor Control e Translating Research into Clinical Practice, third ed. Lippincott Williams & Wilkins:Wolters Kluwer, Philadelphia. Sirtori, V., Corbetta, D., Moja, L., Gatti, R., 2009. Constraintinduced movement therapy for upper extremities in stroke patients. Cochrane Database Syst. Rev. 7 (4), CD004433. Stein, J., Richards, L.H., Macko, R.F., Winstein, C.J., Zorowitz, R.D., 2009. Stroke Recovery and Rehabilitation. Jaypee Brother, New Delhi. Sullivan, K.J., Tilson, J.K., Cen, S.Y., Rose, D.K., Hershberg, J., Correa, A., et al., 2011. Fugl-Meyer assessment of sensorimotor function after stroke: standardized training procedure for clinical practice and clinical trials. Stroke 42 (2), 427e432. Takebayashi, T., Koyama, T., Amano, S., Hanada, K., Tabusadani, M., Hosomi, M., et al., 2013. A 6-month follow-up after constraint-induced movement therapy with and without transfer package for patients with hemiparesis after stroke: a pilot quasi-randomized controlled trial. Clin. Rehabil. 27 (5), 418e426. van der Lee, J.H., Beckerman, H., Lankhorst, G.J., Bouter, L.M., 2001. The responsiveness of the Action Research Arm test and

S. Pandian, K.N. Arya the Fugl-Meyer Assessment scale in chronic stroke patients. J. Rehabil. Med. 33 (3), 110e113. Van der Lee, J.H., De Groot, V., Beckerman, H., Wagenaar, R.C., Lankhorst, G.J., Bouter, L.M., 2001. The intra- and interrater reliability of the action research arm test: a practical test of upper extremity function in patients with stroke. Arch. Phys. Med. Rehabil. 82 (1), 14e19. Velozo, C.A., Woodbury, M.L., 2011. Translating measurement findings into rehabilitation practice: an example using FuglMeyer Assessment-Upper Extremity with patients following stroke. J. Rehabil. Res. Dev. 48 (10), 1211e1222. Wang, C.H., Hsieh, C.L., Dai, M.H., Chen, C.H., Lai, Y.F., 2002. Inter-rater reliability and validity of the stroke rehabilitation assessment of movement (stream) instrument. J. Rehabil. Med. 34 (1), 20e24. Ward, I., Pivko, S., Brooks, G., Parkin, K., 2011. Validity of the stroke rehabilitation assessment of movement scale in acute rehabilitation: a comparison with the functional independence measure and stroke impact scale-16. Pm R. 3 (11), 1013e1021. Wei, X.J., Tong, K.Y., Hu, X.L., 2011. The responsiveness and correlation between Fugl-Meyer Assessment, Motor Status Scale, and the Action Research Arm Test in chronic stroke with upper-extremity rehabilitation robotic training. Int. J. Rehabil. Res. 34 (4), 349e356. Whitall, J., Savin Jr., D.N., Harris-Love, M., Waller, S.M., 2006. Psychometric properties of a modified Wolf Motor Function test for people with mild and moderate upper-extremity hemiparesis. Arch. Phys. Med. Rehabil. 87 (5), 656e660. Wolf, S.L., 2007. Revisiting constraint-induced movement therapy: are we too smitten with the mitten? Is all nonuse “learned”? and other quandaries. Phys. Ther. 87 (9), 1212e1223. Wolf, S.L., Catlin, P.A., Ellis, M., Archer, A.L., Morgan, B., Piacentino, A., 2001. Assessing Wolf motor function test as outcome measure for research in patients after stroke. Stroke 32 (7), 1635e1639. Wolf, S.L., Winstein, C.J., Miller, J.P., Taub, E., Uswatte, G., Morris, D., et al., 2006. Effect of constraint-induced movement therapy on upper extremity function 3 to 9 months after stroke: the EXCITE randomized clinical trial. JAMA 296 (17), 2095e2104. Wood-Dauphinee, S.L., Williams, J.I., Shapiro, S.H., 1990. Examining outcome measures in a clinical study of stroke. Stroke 21 (5), 731e739. Woodbury, M., Velozo, C.A., Thompson, P.A., Light, K., Uswatte, G., Taub, E., et al., 2010. Measurement structure of the Wolf Motor Function Test: implications for motor control theory. Neurorehabil. Neural Repair 24 (9), 791e801. Woodbury, M.L., Velozo, C.A., Richards, L.G., Duncan, P.W., Studenski, S., Lai, S.M., 2008. Longitudinal stability of the FuglMeyer Assessment of the upper extremity. Arch. Phys. Med. Rehabil. 89 (8), 1563e1569. Wu, C.Y., Fu, T., Lin, K.C., Feng, C.T., Hsieh, K.P., Yu, H.W., et al., 2011. Assessing the streamlined Wolf motor function test as an outcome measure for stroke rehabilitation. Neurorehabil. Neural Repair 25 (2), 194e199. Wu, D., Qian, L., Zorowitz, R.D., Zhang, L., Qu, Y., Yuan, Y., 2013. Effects on decreasing upper-limb poststroke muscle tone using transcranial direct current stimulation: a randomized shamcontrolled study. Arch. Phys. Med. Rehabil. 94 (1), 1e8. Yavuzer, G., Selles, R., Sezer, N., Sutbeyaz, S., Bussmann, J.B., Koseoglu, F., et al., 2008. Mirror therapy improves hand function in subacute stroke: a randomized controlled trial. Arch. Phys. Med. Rehabil. 89 (3), 393e398. Yozbatiran, N., Der-Yeghiaian, L., Cramer, S.C., 2008. A standardized approach to performing the action research arm test. Neurorehabil. Neural Repair 22 (1), 78e90.

Please cite this article in press as: Pandian, S., Arya, K.N., Stroke-related motor outcome measures: Do they quantify the neurophysiological aspects of upper extremity recovery?, Journal of Bodywork & Movement Therapies (2013), http://dx.doi.org/10.1016/ j.jbmt.2013.11.006

Outcome measures for the upper extremity motor recovery in post-stroke hemiparesis

FugleMeyer Assessment (Upper extremity subsection)

1975

Action Research Arm test

1981

Motor Assessment Scale (upper arm function, hand movements and advanced hand activities) Wolf Motor Function test

1985

1989

Time to Tools/equipment administer

Reliability

Test-retest: ICC Z .97 (Platz et al., 2005) Inter-rater: r Z .97 to .99 (Duncan et al., 1983; Sanford et al., 1993) Internal Consistency: a Z .97 (Wood-Dauphinee et al., 1990) 19 (under 20 min Woodblocks, a cricket Inter-rater: r Z .99 4 categories) ball, a sharpening Inter-rater: r Z .98 stone, two different (Platz et al., 2005; sizes of alloy tubes, Van der Lee et al., a washer and a bolt, 2001b; Yozbatiran two glasses, a marble et al., 2008) and a 6 mm Internal Consistency: ball bearing a Z .98 (Nijland et al., 2010) 3 (6 hierarchy 5 min Stopwatch, 8 jellybeans, Inter-rater: scoring criteria a rubber ball, a stool, r Z .89 to .99 for each item) comb, spoon, pen, Test-retest: r Z .98 teacups, water (Carr et al., 1985; and a table Poole and Whitney, 1988) 17 30e45 min Standardized table Test-retest: and chair, r Z .90 to .95 standardized test Inter-rater: item template, ICC Z .93 height-adjustable to .99(D. M. bedside table, Morris et al., 2001; box, Whitall et al., 2006; individual wrist Wolf et al., 2001) weights Internal Consistency: (1e20 pounds), a Z .92 12-oz beverage can, (Morris et al., 2001) 700 pencil with 6 flat sides, 200 paper clip,

33 (under 9 categories)

15 min

A scrap of paper, a ball, a pencil and a small cane

Validity

MCID/MDC

Modified version

Criterion: r Z .96 (Malouin et al., 1994) Construct: r Z .63 to .89(Mao et al., 2002; Shelton et al., 2001) Criterion: r Z .81 to .97 (Hsieh et al., 1998; J. H. Lin et al., 2009)

e MCID: 9 to 10(Arya et al., 2011b) MDC: 5.2 (J. H. Lin et al., 2009)

Construct: r Z .89 to .93 (Poole and Whitney, 1988)

e

Modified version (Loewen and Anderson, 1990)

Criterion: r Z .57 to .88 (Whitall et al., 2006; Wolf et al., 2001)

MCID: 1.5e4 s and .1 to .4 (Fritz et al., 2012; K. C. Lin et al., 2009) MDC: 12 (J. H. Lin et al., 2009)

Graded version (Bogard et al., 2009) Streamlined version (C. Y. Wu et al., 2011)

MCID: 5.7 e (van der Lee et al., 2001a) MDC: 3.5 (J. H. Lin et al., 2009)

11

(continued on next page)

MODEL

Year of Number of development items

+

Outcome measure

Stroke-related motor outcome measures

Please cite this article in press as: Pandian, S., Arya, K.N., Stroke-related motor outcome measures: Do they quantify the neurophysiological aspects of upper extremity recovery?, Journal of Bodywork & Movement Therapies (2013), http://dx.doi.org/10.1016/ j.jbmt.2013.11.006

Appendix 1

12

Outcome measure

Motricity Index

Year of Number of development items

1990

3

Time to Tools/equipment administer

2e5 min

7 stages each 10 min for arm and hand (3 items for each stage; except stage 1)

An adjustable table, Chair with armrests, floor mat, pillows, a pitcher with water, a measuring cup, a ball 2.5 inches in diameter, a footstool, stopwatch 5e10 min A Paper and a pencil

Stroke Rehabilitation 1997 Assessment of Movement (Upper limb movements)

10

Validity

MCID/MDC

Modified version

Test-retest: ICC Z .93 Inter-rater: r Z .88 (Collin and Wade, 1990) Test-retest: ICC Z .98 Inter-rater: ICC Z .97 to .99 (Gowland et al., 1993) Internal Consistency: ICC Z .98 (Gowland et al., 1993)

e

e

e

Criterion: r Z .79 to .95 Construct: r Z .95

e

e

Test-retest: ICC Z .93 to .98 (H. M. Chen et al., 2007) Inter-rater: ICC Z .99 Intra-rater: ICC Z .96 (Daley et al., 1999) Internal Consistency: a Z .98 (Daley et al., 1999)

Criterion: r Z .76 to .78 (Ahmed et al., 2003) Construct: r Z .76 to .80 (Hsueh et al., 2003)

MCID: 2.2 (Y. W. Hsieh et al., 2008) MDC: 2.3 (J. H. Lin et al., 2009)

Simplified version (Hsueh et al., 2006)

MODEL

Chedoke-McMaster Stroke 1993 Assessment (Impairment inventory-arm and hand)

3 checkers, three 300  500 note cards, lock and key board at 45 angle, face towel, basket, dynamometer, talcum powder and stopwatch 2.5 cm cube

Reliability

+

MCID e Minimal clinically important difference MDC e Minimal detectable change. (Carr et al., 1985; Collin and Wade, 1990; “Constraint-Induced Movement Therapy Research Group - Manual:Upper Extremity e Motor Activity Log, University of Alabama at Birmingham and Birmingham Veteran’s Administration Center.,” 2004; Finch et al., 2002; Fugl-Meyer et al., 1975; Gowland et al., 1993; Van der Lee et al., 2001b; Ward et al., 2011).

S. Pandian, K.N. Arya

Please cite this article in press as: Pandian, S., Arya, K.N., Stroke-related motor outcome measures: Do they quantify the neurophysiological aspects of upper extremity recovery?, Journal of Bodywork & Movement Therapies (2013), http://dx.doi.org/10.1016/ j.jbmt.2013.11.006

Appendix 1 (continued )