Inpatient Rehabilitation Outcomes of Patients With Apraxia After Stroke Andy J. Wu, PhD, MOT,1 Emily Burgard, MOT,2 and Jeff Radel, PhD1,3 1

Department of Occupational Therapy Education, University of Kansas Medical Center, Kansas City, Kansas; 2 St. Luke’s Hospital of Kansas City, Missouri; 3Departments of Ophthalmology and Molecular & Integrative Physiology, University of Kansas Medical Center, Kansas City, Kansas

Background: Stroke-induced paresis commands much attention during rehabilitation; other stroke-related consequences receive less consideration. Apraxia is a stroke disorder that may have important implications for rehabilitation and recovery. Objective: To investigate association of apraxia with stroke rehabilitation outcomes during inpatient rehabilitation. Methods: This cohort study compared patients with and without apraxia after a first left hemispheric stroke. All study patients received standard of care. Clinical measures were the Functional Independence Measure (FIM) and the upper extremity section of the Fugl-Meyer Assessment (FMA) administered upon admission and at discharge. Length of stay was also documented. Florida Apraxia Battery subtests were used to classify patients with apraxia. Results: Fifteen patients were included in this study, 10 of whom had apraxia. Data analysis revealed that patients with apraxia exhibited improvement from admission to discharge in clinical measures; however, admission FIM score was significantly lower compared to patients without apraxia. There was no statistically significant difference between groups on FMA score, length of stay, or amount of change on clinical measures. Conclusions: This study of acute patients found those with apraxia to be significantly less independent upon admission to inpatient rehabilitation compared to patients without apraxia. Although both groups improved a similar amount during rehabilitation, patients with apraxia discharged at a level of independence comparable to patients without apraxia upon admission. Such disparity in independence is of concern, and apraxia as a factor in stroke rehabilitation and recovery deserves further attention. Key words: activities of daily living, apraxia, rehabilitation, stroke

troke remains a major public health concern in the United States, affecting approximately 795,000 people a year.1 Stroke sequelae span multiple domains, including motor, cognitive, and sensory subsystems that all may compromise performance of activities of daily living and quality of life.2 Hence, stroke contributes significantly to long-term disability,3,4 and the field of rehabilitation continues to strive to effectively address the consequences of stroke. Upper extremity paresis is a common impairment following stroke, with reports of nearly 70% of patients with some degree of paresis upon hospital admission. 5 Paresis contributes to a vicious cycle of disuse after stroke, leading to central nervous system changes that may further decrease voluntary motor behavior.6 It is a frequent target of traditional rehabilitation efforts for these reasons7; less consideration, however, exists for other stroke

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sequelae that also may influence the nature or quality of overall movement performance.8-10 Apraxia is a disorder of learned skilled movements not attributable to other common stroke deficits, such as primary motor impairments, sensory impairments, or language comprehension difficulties11-13 (see Vanbellingen’s14 review on apraxia classification, assessment, and treatment). The apraxias are often associated with lesions involving the left inferior parietal lobule,15-18 and the parietal cortex appears to be critical to the praxis system, particularly in overlearned skilled motor behavior.19 Liepmann’s original concept of apraxia was that patients retain an accurate “movement formula” or movement representation (ie, spatio-temporal image of the action), but have difficulty with retrieval and translation into motor innervations necessary for movement.20 Consequently, patients know what to do, but

Corresponding author: Andy J. Wu, PhD, Department of Occupational Therapy Education, University of Kansas Medical Center, 3901 Rainbow Boulevard, Mail Stop 2003, Kansas City, KS 66160; phone: 913-935-7332; fax: 913-588-4568; e-mail: [email protected]

Top Stroke Rehabil 2014;21(3):211–219 © 2014 Thomas Land Publishers, Inc. www.strokejournal.com doi: 10.1310/tsr2103-211

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not how, which manifests as specific spatial and temporal movement errors that interfere with efficient manipulation of objects. Patients with ideomotor apraxia commonly display spatial errors including difficulty with joint orientation (eg, demonstrating salting food above the head) or incorrect hand configuration (eg, demonstrating pincer grasp to hold a toothbrush). Apraxia is a stroke sequela that can have important implications for daily life functioning, however, apraxic deficits are most noticeable in a testing environment, particularly when eliciting pantomiming object use.21 The voluntary automatic dissociation (ie, difficulty with pantomime upon request and automatic performance in a natural situation) contributes to researchers and clinicians discounting the impact of apraxia on everyday life.13,22,23 Although task performance improves, kinematic analyses reveal that performance remains degraded despite the use of actual objects and tools in the appropriate situation.24 Estimates of the incidence of apraxia after left hemispheric stroke range from 30%25,26 to 50%27-29 versus approximately 13% to 20% after right hemispheric stroke.13,30 Still, a lack of consensus exists regarding resolution of apraxia; reports vary considerably, with recent studies indicating apraxia persisting into the chronic phase of stroke.26,31,32 Recent evidence suggests that apraxia does influence function. There are reports that greater severity correlates with reduced independence in daily living skills (such as mealtime or dressing activities, and brushing teeth)25,33-36 and reduced improvement in independent functioning. 26 Despite accumulating evidence that the presence of apraxia has a negative influence on daily functioning9,34,37,38 and more authors suggesting that rehabilitation programs consider the presence of apraxia,10,39,40 the potential impact of apraxia on stroke rehabilitation receives limited attention in many clinical settings. The present cohort study compared rehabilitation outcomes of patients with and without apraxia after first-time left hemispheric stroke within days after initial injury through inpatient rehabilitation stay. Specifically, we hypothesized differences in level of independence in activities of daily living and primary motor impairment of the more-affected upper extremity between patients with and

without apraxia. Also, we expected the amount of change on outcomes to be different between groups. Although similar to Unsal-Delialioglu’s study (see ref. 57) of individuals approximately 90 days post stroke, this study enhances our understanding about rehabilitation outcome during the acute phase of stroke, within days up to approximately 1 month post initial injury, which is a critical time for recovery. Methods Study patients

Between August 2011 and October 2012, occupational therapists at 2 study sites screened a total of 50 patients diagnosed with stroke using the following inclusion criteria: (a) age ≥18 years and ≤85 years, (b) first-time left hemispheric stroke confirmed by computed tomography (CT)/magnetic resonance imaging (MRI), and (c) admission to inpatient rehabilitation. Exclusion criteria used were (a) prior history of other central nervous system disease, (b) bilateral stroke, (c) dementia, and (d) major head trauma. Prior to enrollment in the study, patients provided informed consent approved by institutional review boards for the participating institutions. We excluded 24 patients with right hemispheric stroke, 5 patients with history of bilateral stroke, 2 patients with history of brain tumor, and 1 patient who declined to participate. Clinical measures

The Functional Independence Measure (FIM)41 assesses independence with 18 activities of daily living. The FIM demonstrates excellent reliability and validity,42,43 and all evaluators in this study were certified by the Uniform Data System. Items are rated on a 7-point ordinal scale ranging in level of assistance required (1 = total assistance to 7 = complete independence). Maximum total score is 126, with higher scores signifying greater independence. The Fugl-Meyer Assessment (FMA) 44 is a performance-based index recommended for clinical and research evaluation of motor impairment after stroke.45 The FMA demonstrates impressive test-

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retest reliability, interrater reliability, and construct validity.45-47 For the present study, we administered only the upper extremity motor subsection, which assessed voluntary movement, coordination, and reflex action of the patient’s right shoulder, elbow, forearm, wrist, and hand. Performance on tasks was scored on a 3-point ordinal scale (0 = cannot perform; 1 = performs partially; 2 = performs fully), and the total score (maximum score = 66) was used in the analysis; higher scores indicate less motor impairment. Apraxia testing

Similar to previous investigations, 34,48,49 an abbreviated version of the Florida Apraxia Screening Test (FAST-R 50) – the pantomime expression test – was used to assess ideomotor apraxia (pantomime output pathways).51 Patients used only the ipsilesional (left) upper extremity during testing, so primary motor impairment did not influence apraxia testing. Patients were asked to pantomime a set of 10 transitive (tool-use) tasks, and they were encouraged to demonstrate the task as if actually holding the tool. Two trained judges, not involved in administering the test, scored the video-recorded responses of each task. Each task could receive a maximum score of 6 (total maximum raw score = 60), and errors resulted in deductions of 1 point except for an uncorrected body part as tool error (-3 points) and no response or unrecognizable (-6 points). Number and type of errors determine apraxia, and errors originated from 4 main categories: content (perseverative, related, nonrelated), spatial (amplitude, internal and external configuration, body part as tool, movement), timing (sequencing, timing, occurrence), and other (no response, unrecognizable). We used a cutoff score of 50%, based on previous reports, 50,51 to categorize patients with apraxia (≤50%) from those without apraxia (>50%). We did not include apraxia severity in our primary analysis. A modified version of the pantomime-tophotograph matching subtest derived from the Florida Apraxia Battery-Extended and Revised Sydney52 was administered after the pantomime expression test described previously to determine comprehension deficits. We chose to use the

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same set of 10 transitive pantomimes. Evaluators performed each pantomime and asked patients to point to the correct photograph of the tool. Responses were recorded as 0 = incorrect or 1 = correct. We only included patients scoring 70% or higher in the final analyses. Occupational therapists with at least 4 years of inpatient rehabilitation experience administered assessments. Regular meetings and frequent review of testing procedures helped to ensure consistency among administrators. After collecting informed consent from the study patients, occupational therapists obtained demographic information from patient interviews and medical records. FIM and FMA data were collected within at least 3 days upon admission to and 3 days before discharge from inpatient rehabilitation. Length of stay was also documented. Apraxia testing was video-recorded at admission for later scoring by trained judges not involved in patient care. All therapists knew of the study’s purpose, but they were unaware of apraxia categorization to avoid potential attention bias or influence on daily rehabilitation interventions. Inpatient rehabilitation

Study sites were large urban hospitals with organized inpatient unit stroke care similar to that described by the Stroke Unit Trialists’ Collaboration.53 Board-certified physical medicine and rehabilitation physicians directed patient care, including coordinating a multidisciplinary team comprised of medicine, nursing, social work, occupational, physical, and speech therapies. Patients admitted to an inpatient rehabilitation facility received at minimum 3 hours a day of a combination of occupational, physical, and speechlanguage therapy 5 days per week. Study patients differed only from other patients with respect to completing periodic assessments described previously; otherwise, they received standard of care. Rehabilitation therapists established intervention plans that were individualized according to patient presentation and included activities of daily living retraining, therapeutic activities/exercises, neuromuscular reeducation, mobility/gait training, speech-language, and cognitive retraining. Team meetings occurred

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weekly to review patient progress, to establish a prognosis, and to plan for discharge.

admission FIM score from discharge FIM score and dividing by length of stay.

Statistical analyses

Results

All statistical analyses were performed using IBM SPSS Statistics v. 20.0.54 Level of significance for all statistical analyses was set a priori as α = 0.05. Patient demographic information was summarized using descriptive statistics, including means and standard deviations (see Table 1). Nonparametric statistics were chosen for use due to small sample size and lack of normality in data from clinical measures. Mann-Whitney U tests compared clinical measures at admission, change scores, and length of stay between groups. Wilcoxon signed-rank tests compared withingroup differences on clinical measures to establish whether patients with apraxia demonstrated improvement after rehabilitation. Interrater reliability analysis using the kappa statistic was performed on 5 pantomime expression test scores to determine consistency among the raters. We calculated FIM change per day (an index of rehabilitation efficiency)55 by subtracting

Use of the aforementioned inclusion and exclusion criteria yielded 15 patients. We identified 10 of 15 (66.67%) patients as having apraxia using the pantomime expression test. Interrater reliability on 5 pantomime expression test scores was κ= 0.809 with P < .001, indicating substantial agreement between trained raters.56 Groups at admission did not differ significantly on age or stroke period as indicated by separate MannWhitney U tests (age, U = 15, z = -1.592, P = .129; stroke period, U = 18, z = -0.860, P = .440). Patient characteristics are summarized in Table 1. Patients with apraxia improved from admission to discharge on clinical measures (Table 2). Wilcoxon signed-rank tests indicated statistically significant improvement in independence, measured by FIM (z = -2.805, P = .005) and in right upper extremity motor impairment, measured by FMA (z = -2.207, P = .027). See Table 2 for mean FIM and FMA scores.

Table 1.

Patient demographic and stroke characteristics

Patient

Age, years

Sex

Apraxia score

Stroke type

No apraxia 1 2 3 4

56 60 43 42

F F M F

0.58 0.70 0.93 0.87

Ischemic Ischemic Ischemic Unknown

6 9 6 5

59

F

0.78

Ischemic

1

5 Mean (SD) Apraxia 1 2 3 4 5 6 7 8 9 10 Mean (SD)

52 (8.80) 64 68 79 63 70 63 50 66 61 76 66 (8.11)

Stroke period, days

Lesion site Po IC F-T, BG Corona radiata and post limb of left IC Posterior corona radiata

5.4 (2.88) M F M M M M M M M M

0.47 0.47 0.35 0.45 0 0 0 0.50 0.45 0.27

Ischemic Ischemic Ischemic Ischemic Ischemic Hemorrhagic Ischemic Ischemic Ischemic Ischemic

8 8 9 2 20 7 5 12 14 12 9.7 (5.06)

Po BG F-P O IC F-P F-P Po F F

Note: APR score = score from pantomime expression test; BG = basal ganglia; F = frontal; IC = internal capsule; O = occipital; P = parietal; Po = pons; stroke period = time from stroke to admission to inpatient rehabilitation; T = temporal.

Apraxia and Stroke Rehabilitation Outcome

Table 2. Within-group comparisons for subjects with apraxia for FIM and FMA scores Variable

Admission

Discharge

Pa

FIM FMA

33.50 ± 19.67 14.10 ± 18.48

67.10 ± 21.90 23.40 ± 22.55

.005* .027*

Note: Values are mean ± SD. FIM = Functional Independence Measure; FMA = Fugl-Meyer Assessment (upper extremity portion only; max = 66). a P values from Wilcoxon’s signed-rank test. *Denotes statistical significance P < .05.

Table 3 displays means and standard deviation by assessment time point and comparisons between groups for clinical measures and length of stay. Mann-Whitney U tests were used to evaluate scores between patients with and without apraxia on admission FIM and FMA scores, the amount of change on FIM and FMA from admission to discharge, and length of stay. We found significant between-group differences in mean admission FIM scores (U = 6, z = -2.329, P = .019); patients with apraxia exhibited lower mean admission FIM scores compared to patients without apraxia. Additional analysis of FIM subsections revealed lower mean cognitive subtotal score between groups. On admission, patients with apraxia scored significantly lower than patients without apraxia (mean 9.5 ± 6.13 vs mean 24 ± 5.05) on the FIM cognitive subtotal score (U = 2.5, z = –2.776, P = .003), but did not differ significantly Table 3. Between-group comparisons for FIM, FMA scores, and length of stay Variable FIM Admission Discharge Δ FMA Admission Discharge Δ Length of stay, days

Apraxia (n = 10)

No apraxia (n = 5)

33.50 ± 19.67 67.10 ± 21.90 33.60 ± 16.99

62.80 ± 13.95 95.80 ± 10.38 33.00 ± 9.38

14.10 ± 18.48 23.40 ± 22.55 9.30 ± 13.99 24.40 ± 13.48

32.80 ± 28.89 45.00 ± 23.17 12.20 ± 16.80 18.40 ± 8.59

Pa .019* .768 .206 .679 .440

Note: Values are mean ± SD. FIM = Functional Independence Measure; FMA = Fugl-Meyer Assessment (upper extremity portion only; max = 66). a P values from Mann-Whitney U tests. *Denotes statistical significance P < .05.

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(mean 24 ± 15.62 vs 38.8 ± 17.2) in terms of FIM motor subtotal score (U = 12, z = –1.595, P = .129). Between-group FMA comparisons did not differ significantly at admission (U = 14, z = –1.353, P = .206). Comparing the amount of change in clinical measures between groups revealed no statistical differences on either FIM (U = 22.5, z = -0.308, P = .768) or FMA (U = 21.5, z = -0.437, P = .679). Mean changes for patients with apraxia on FIM and FMA were similar to mean changes for patients without apraxia on FIM and FMA. Although there was no between-group difference in mean FIM change, mean discharge FIM scores between groups remained statistically different. We observed the mean discharge FIM score of patients with apraxia to be similar to the mean admission FIM score of patients without apraxia (U = 20.5, z = -0.552; P = .581). There was no statistically significant difference in mean length of stay between patients with apraxia and patients without apraxia (U = 18.5, z = -0.675, P = .513). There was no significant difference between groups for rehabilitation efficiency (U = 8, z = -0.490, P = .730). We also examined an alternative grouping of patients based on pantomime expression test scores using the following categories: 0 to 0.35 as severe, 0.36 to 0.54 as moderate, and 0.55 to 1.0 as mild (no study patient scored 1.0). The resulting analyses did not yield significant findings or any meaningful pattern between groups. Discussion In the present cohort study, patients with apraxia after stroke improved during inpatient rehabilitation, exhibiting greater independence upon discharge from inpatient rehabilitation compared to admission. Unsal-Delialioglu 57 compared 26 patients with apraxia and 21 without apraxia and found improvements in both patient groups at discharge. Taken together, these findings are not surprising, because rehabilitation intensity provided in inpatient rehabilitation results in more favorable functional outcomes58 and, consequently, more patients are likely to be alive, independent, and living at home after 1 year.53 To address other study objectives, we categorized patients into 2 groups (with and without apraxia),

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with two-thirds of our sample identified with apraxia. This is higher proportion than in other studies, where approximately half of patients display apraxia after left hemispheric stroke,27-29 and is likely attributable to our small sample size. The patients we identified without apraxia had no lesions involving parietal regions, whereas many of our patients with apraxia possessed lesions in the frontal/parietal areas of the brain that are implicated in apraxia manifestation.15-18,59 Analysis of between-group data yielded mixed results, supporting differences between groups for admission FIM. Patients with apraxia admitted to inpatient rehabilitation exhibited less independence and scored approximately 30 points less on average on the FIM when compared to patients without apraxia, a difference considered clinically significant. 60 Despite having lower independence scores at admission, patients with apraxia still exhibited proportional improvement at discharge as did patients without apraxia. Observed mean discharge FIM score of patients with apraxia was similar to mean admission FIM score of patients without apraxia. This finding is in accordance with a recent study reporting discharge FIM scores of patients with apraxia failing to reach admission FIM scores of patients without apraxia.57 Moreover, Kaya et al29 suggests that apraxia may be present in patients who demonstrate low FIM scores, a result that is in agreement with our study. Unsal-Delialioglu57 studied patients within 90 days of inpatient rehabilitation admission; the present study included patients within 8 days of stroke. The congruency of results indicates a persistent disparity in independence between patients with and without apraxia, at least within the initial 3 months after stroke. Studies of patients 6 months after stroke yield similar findings, with patients having apraxia requiring more assistance with activities of daily living.35 The results of the present study contribute valuable insight about expectations for rehabilitation outcomes during the early, acute phase of stroke recovery in patients having apraxia. Variability in our sample appears quite high for both clinical measures; this should be taken in account when interpreting the results. However, categorizing patients using the alternate scheme for pantomime expression test score was not helpful in

explaining the high variability. Despite variability, patients with apraxia demonstrated mean FIM improvement greater than established criteria of minimally clinically important difference (MCID; FIM total score of 22 points60). We also observed this MCID between groups for mean admission FIM scores (see Table 1). Motor impairment findings appear to follow a similar pattern as FIM scores. Admission motor impairment findings between groups were not statistically significant, likely due to small sample size and lack of statistical power to detect differences [computed achieved power (1 – β) = 0.343] (GPower 3.161). However, the mean admission FMA score of patients with apraxia appears lower than the mean admission FMA score of patients without apraxia (MCID of FMA upper extremity portion of 10-point difference).62 Although the mean FMA change score of patients with apraxia does not reach the established MCID, it does meet minimal detectable change (5.2 for FMA upper extremity portion),63 representing true FMA change (accounting for error) from admission to discharge. Despite the sample size and data variability, our results are in keeping with previous studies demonstrating improved independence57 and increased function of the more-affected upper extremity.49 Further investigation is necessary, however, before definitive statements can be made. No differences in the amount of improvement in either clinical measure were apparent between groups. Patients with apraxia demonstrated equivalent amounts of improvement in independence and motor impairment compared to patients without apraxia. By contrast, previous studies have reported less improvement in independent functioning with more severe apraxia, suggesting apraxia’s adverse influence on recovery.26 Our results may reflect the scoring method used in the present study to classify patients with and without apraxia, as we did not take into account apraxia severity. The contralateral arm clearly is more affected after stroke, although studies also document diminished strength64-66 in the ipsilateral arm and less accuracy67 in movements. Future studies of apraxia should assess for baseline ipsilateral arm motor function. It would have been valuable to use the pantomime-to-photograph matching subtest

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to assess pantomime input pathways instead of additional exclusion criteria. Thus, we recommend collaborating with speech-language pathologists or administering a standardized measure to determine auditory comprehension. We were unable to control for covariates in our analysis due to sample size, but we suspect other variables besides presence of apraxia (ie, age, stroke period, side of stroke, etc) account for the between-group difference in admission FIM scores. Future studies should consider these factors and include patients immediately after right hemispheric stroke to help enhance the understanding of the relation between apraxia and rehabilitation outcome after stroke.

independence than patients without apraxia. Although patients with and without apraxia demonstrated a comparable amount of change in independence during rehabilitation, patients with apraxia displayed similar independence at discharge compared to patients without apraxia upon admission. This disparity of independence level at both admission and discharge is significant. It will be important for clinicians to recognize potential presence of apraxia, especially after left hemispheric stroke. Preliminary results from this study warrant additional investigation to further clarify the role of apraxia in rehabilitation outcome after acute stroke.

Conclusion

Acknowledgments

The findings of this study underscore the importance of considering apraxia and its relevance to rehabilitation outcomes of patients after stroke, particularly in the acute stage of recovery. Patients with apraxia in this study exhibited lower admission

Dr. Wu thanks all study patients for their time, Allie Majerle and Emily Burgard for coordinating data collection at the study sites, and his dissertation committee for their valuable contribution to this work in partial fulfillment of a PhD.

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Inpatient rehabilitation outcomes of patients with apraxia after stroke.

Stroke-induced paresis commands much attention during rehabilitation; other stroke-related consequences receive less consideration. Apraxia is a strok...
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