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Ipsilateral Deficits in 1-Handed Shoe Tying After Left or Right Hemisphere Stroke Janet L. Poole, PhD, OTR/L, Joseph Sadek, PhD, Kathleen Y. Haaland, PhD ABSTRACT. Poole JL, Sadek J, Haaland KY. Ipsilateral deficits in 1-handed shoe tying after left or right hemisphere stroke. Arch Phys Med Rehabil 2009;90:1800-5. Objective: To examine 1-handed shoe tying performance and whether cognitive deficits more associated with left or right hemisphere damage differentially affect it after unilateral stroke. Design: Observational cohort comparing ipsilesional shoe tying, spatial and language skills, and limb praxis. Setting: Primary care Veterans Affairs and private medical center. Interventions: Not applicable. Participants: Volunteer right-handed sample of adults with left or right hemisphere damage and healthy demographically matched adults. Main Outcome Measure: The number of correct trials and the total time to complete 10 trials tying a shoe using the 1-handed method. Results: Both stroke groups had fewer correct trials and were significantly slower tying the shoe than the control group. Spatial skills predicted accuracy and speed after right hemisphere damage. After left hemisphere damage, accuracy was predicted by spatial skills and limb praxis, while speed was predicted by limb praxis only. Conclusions: Ipsilesional shoe tying is similarly impaired after left or right hemisphere damage, but for different reasons. Spatial deficits had a greater influence after right hemisphere damage, and limb apraxia had a greater influence after left hemisphere damage. Language deficits did not affect performance, indicating that aphasia does not preclude using this therapy approach. These results suggest that rehabilitation professionals should consider assessment of limb apraxia and ipsilesional skill training in the performance of everyday tasks. Key Words: Apraxias; Motor skills; Rehabilitation; Self care; Stroke. © 2009 by the American Congress of Rehabilitation Medicine
From the Occupational Therapy Graduate Program (Poole), Psychiatry (Sadek, Haaland), and Neurology (Haaland) Departments, University of New Mexico School of Medicine, Albuquerque, NM; and Research Service (Haaland) and Behavioral Health Care Line (Sadek, Haaland), New Mexico Veterans Affairs Healthcare System, Albuquerque, NM. Supported by the Department of Veterans Affairs (Rehabilitation Research and Development, grant no. B4125R, and Clinical Services Research and Development). No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit on the authors or on any organization with which the authors are associated. Reprint requests to Kathleen Y. Haaland, PhD, Research Service (151), NMVAHCS, 1501 San Pedro SE, Albuquerque, NM 87108, e-mail: khaaland@ unm.edu. 0003-9993/09/9010-00952$36.00/0 doi:10.1016/j.apmr.2009.03.019
Arch Phys Med Rehabil Vol 90, October 2009
RESSING IS A COMPLEX skill generally requiring the D use of balance; cognitive abilities, including limb praxis and spatial abilities; and both upper extremities. Unilateral stroke often results in significant residual motor impairment on 1 side of the body, requiring daily tasks to be performed using the upper extremity ipsilateral to damage. Dressing both upper and lower extremities has been reported to be difficult even at 2 years poststroke.1 Most of this literature has focused on upper-body dressing and the underlying deficits that influence the ability to relearn to dress, including limb apraxia and spatial deficits.2-5 Few studies have examined lower-extremity dressing, although 1 study showed that the severity of hemiparesis strongly predicted lower-body dressing ability2 because balance and gross motor functions are needed. Tying shoelaces is an aspect of dressing that has not been examined routinely.2 In the rehabilitation literature, a technique called 1-handed shoe tying has been developed to help people after stroke tie a shoe with 1 hand. This is an important practical issue because there are several advantages of wearing laced shoes versus shoes with Velcro or elastic closures. For example, laced shoes (1) may be more compatible with metal ankle foot orthoses6; (2) include top eyelets that provide a snug closure, which reduces heel slippage7; (3) provide more support to the arch of the foot6; and (4) are available in more shoe styles. The last point may be especially important for young people with stroke. However, despite the advantages of wearing laced shoes and the need to be able to tie them with 1 hand for individuals with hemiparesis, the 1-handed shoe tying method has been considered difficult and impossible to learn by individuals with cognitive or perceptual deficits.8 Shoe tying involves a variety of cognitive skills that are impaired after unilateral stroke, including spatial skills, motor sequencing skills, and language skills to understand the task instructions. Spatial deficits, which are more common after RHD than LHD,9 have been shown to influence dressing,2 but their influence has not been examined in 1-handed shoe tying. Visual neglect, organizing complex spatial behaviors, and visuoperceptual deficits are just a few examples of the types of visuospatial deficits that are more impaired after RHD than LHD and could plausibly influence 1-handed shoe tying.9 There is evidence from functional imaging studies in neurologically intact adults10-12 and studies in patients with unilateral brain damage13-15 that sequencing is controlled more by the left than the right hemisphere, and such deficits are more common in those diagnosed with limb apraxia.16 In addition, more recent studies have shown that limb apraxia in the ipsilateral upper limb after stroke has a functional impact on a variety of tasks, including simulated activities of daily living.3-5,17-20 Limb apraxia could also affect the ability to learn 1-handed shoe tying. List of Abbreviations LHD OR RHD
left hemisphere damage odds ratio right hemisphere damage
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One small pilot study21,22 showed that patients with LHD could learn to tie shoes using the 1-handed method, but persons with limb apraxia21 required significantly more trials to learn and retain the task than healthy controls. Moreover, those with limb apraxia made more sequencing and perseveration errors, suggesting difficulty making transitions between steps of a sequence or remembering the steps.21 Therefore, the present study examined the ability to perform 1-handed shoe tying and examined whether cognitive deficits more associated with LHD or RHD would differentially affect ipsilesional shoe tying performance after unilateral stroke. Our study had 2 hypotheses: (1) patients with LHD or RHD after stroke would demonstrate similar degrees of 1-handed shoe tying impairment in the ipsilateral limb relative to a healthy control group using their left or right hand, and (2) the underlying mechanisms for the shoe tying impairment in the LHD and RHD groups would be different. That is, we predicted that limb apraxia, and possibly aphasia, would have a greater influence on the performance of the LHD group, and spatial deficits would have a greater influence on the performance of the RHD group. METHODS Participants We examined 110 right-handed participants: 20 with RHD, 28 with LHD, and 62 healthy, able-bodied control subjects with no self-report of neurologic diagnoses (healthy controls, 24 who tied the shoe with their right hand and 38 who tied the shoe with their left hand). Only participants with neuroradiologically confirmed strokes to either the left or right hemisphere were included. Participants with stroke were excluded if there was a history of (1) neurologic disease other than stroke, (2) damage to the cerebellum or brain stem or significant periventricular white matter changes or cortical atrophy confirmed neuroradiologically, (3) major psychiatric diagnosis, (4) hospitalization for substance abuse, (5) sensory or motor peripheral disorders, or (6) left handedness. Control participants were required to meet the same criteria and have no history of stroke. Informed consent was obtained from all participants according to the Declaration of Helsinki. The study was approved by the institutional review board of the New Mexico Veterans Affairs Health Care System. Table 1 shows the demographic characteristics and other descriptive information for all groups. Measures Ideomotor limb apraxia. Ideomotor limb apraxia was assessed with a 15-item test that assesses the ability to imitate 15 gestures: 5 meaningless, 5 intransitive, and 5 transitive.23,24 The test was videotaped, and when the scores of 2 independent raters were not the same, a consensus score was agreed on by the 2 raters. Participants were considered to have apraxia if they made spatiotemporal errors on 4 of the 15 items (2 SDs greater than the healthy control group).23 Spatiotemporal errors included errors in internal hand position, hand orientation, target (eg, shave hair, not face), and/or body-part-as-object (eg, use extended index finger to brush teeth). An item was scored as incorrect if any of these errors occurred, but additional errors on a single item did not result in a lower score. Interrater reliability for this limb apraxia test is high based on a previous study.24 Cognitive measures. Aphasia was assessed with the Western Aphasia Battery,25 which provides an Aphasia Quotient that reflects all aspects of language. Spatial abilities were measured with the Block Design subtest from the Wechsler
Table 1: Demographic, Neurologic, Neuropsychologic Variables, and Outcome Measures for All Groups Control (n⫽62)
Variable
Age (y) Sex (female, %) Education (y) Years poststroke Lesion volume (mL) Limb apraxia (no. correct)* Incidence of apraxia (%)§ Aphasia quotient* Block Design* Right motor index* Left motor index* Shoe time score* Total correct shoe trials*
LHD (n⫽28)
RHD (n⫽20)
64.6⫾12.0 59.6⫾12.1 66.2⫾12.2 41.9 21.4 45.0 14.5⫾2.4 13.7⫾3.5 13.7⫾2.8 NA 4.8⫾5.7 4.2⫾6.8 NA 70.8⫾76.0 96.1⫾130.3 13.6⫾1.1 11.8⫾2.7†‡ 13.6⫾1.4 NA 35.7 5.0 98.9⫾1.0 76.4⫾28.4†‡ 97.7⫾2.3† 8.5⫾2.2 7.5⫾2.6† 5.9⫾2.5†‡ 46.4⫾6.6 29.8⫾15.8†‡ 42.8⫾8.9 46.5⫾7.0 45.9⫾7.8 32.6⫾18.9†‡ 80.4⫾25.3 120.0⫾74.5† 118.9⫾48.8† 9.1⫾1.0 7.8⫾2.9† 7.8⫾2.4†
NOTE. Values are mean ⫾ SD or as otherwise indicated. Block Design is expressed as a scaled score (10⫾3) relative to the normative sample.45 Abbreviation: NA, not applicable. *Significant group difference across 3 groups using analysis of variance (P⬍.01). † Impaired relative to control group (Tukey test, P⬍.05). ‡ Impaired relative to other stroke group (Tukey test, P⬍.05). § Signficant group difference across 2 groups using chi-square (P⬍.05).
Adult Intelligence Scale–Revised.26 This test requires the construction of designs to match patterns on cards using 4 or 9 blocks; the blocks have 2 all red, 2 all white, and 2 half red and half white sides. Higher scores indicated higher spatial abilities. Motor indices. The motor indices are expressed as T scores with mean ⫾ SD of 50⫾10 relative to a normative sample, based on grip strength and finger tapping.27 Grip strength was the maximum grip scores for 2 trials measured with a Smedley hand dynamometer,a and the finger tapping score was the mean tapping rate of a telegraph key across five 10-second trials. The motor indices scores were calculated for descriptive purposes only. Higher scores indicated better motor function. 1-handed shoe tying. For the shoe tying task,28 the shoe was placed on a table in front of the participant to eliminate the impact of poor trunk balance on shoe tying performance. The shoe was laced in such a fashion that only 1 lace was available for tying (fig 1A). Participants were given the following verbal instructions with demonstration: “First you put the end of the shoe lace through the top lace on the shoe (fig 1B). Then you pull the lace until it is almost all the way through like this (leave about three fourths of an inch of lace that has not been pulled through) (fig 1C). Then take your thumb and index finger and reach through this small loop and pinch part of the loose lace (fig 1D). Then you pull the lace through making a knot.” Participants with stroke used the hand ipsilateral to the stroke. After the task was demonstrated using the same hand that the participants were to use, participants were instructed to try to tie the shoe 10 times in a row. Each trial was timed separately by the researcher. The researcher demonstrated the task with the initial instructions and then only after each incorrect attempt. The score was the number of correct trials (knot tied snug) out of 10 and the total time (summation of time for each trial) to complete 10 trials. Arch Phys Med Rehabil Vol 90, October 2009
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Fig 1. One-handed shoe tying. (A) Shoe laced, leaving 1 end of lace available for 1-handed shoe tying. (B) End of shoe lace inserted through top horizontal lace on the shoe and pulled, leaving about three fourths of an inch of lace loop. (C) Thumb and index finger reach through this small loop and pinch part of the loose lace. (D) Looped lace pulled through, making a knot.
Data Analysis T tests showed no significant differences in the shoe time scores or number of total correct trials between the 2 control groups who used their left or right hands. The shoe time score, mean ⫾ SD, was 84.3⫾27.0 for the control group that tied the shoe with the right hand and 77.0⫾23.5 for the group that tied the shoe with the left hand (F1,59⫽1.25; P⫽.268). The total correct, mean ⫾ SD, was 8.9⫾1.1 for the group that tied the shoe with the right hand and 9.2⫾1.0 for the group that tied the shoe with the left hand (F1,59⫽0.78; P⫽.380). Therefore, we pooled the data from these 2 groups for comparison with the LHD and RHD stroke groups. Demographic and clinical characteristics, as well as the primary dependent measures (shoe tying times and number of correct trials) for the 3 groups, were compared using 1-way univariate analyses of variance with post hoc Tukey tests to identify which groups differed from each other. Chi-square test was used to assess group differences for nominal variables, such as sex or lesion location. To determine whether shoe tying was associated with different underlying cognitive deficits in the 2 stroke groups, we conducted bivariate correlations between the cognitive measures (limb praxis, Aphasia Quotient, Block Design) and the shoe tying measures. A follow-up logistic regression was conducted in the LHD group. RESULTS There were no significant differences in age, education, or sex (P⬎.05) among the 3 groups (see table 1). The 2 stroke groups were similar in time poststroke and lesion volume, but the absolute lesion volume was higher in the RHD group, and the lack of a statistically significant group difference was likely
a result of high variability within each group. However, when the nonparametric Mann-Whitney U test was calculated, the mean rankings for lesion volume were 24.55 for the RHD group and 23.59 for the LHD group, which were not significantly different (U⫽259; P⫽.813). Group differences were present for the Aphasia Quotient (F2,105⫽24.52; P⬍.001) and Block Design performance (F2,107⫽9.75; P⬍.001) related to poorer performance of the LHD group for the Aphasia Quotient and poorer performance of the RHD group on Block Design. In addition, the LHD group performed significantly worse on the limb apraxia assessment (F2,107⫽11.75; P⬍.001) than both the control group and the RHD group. Consistent with this finding, the incidence of limb apraxia (–2 SD below normative group23) was greater in the LHD than the RHD group (2⫽6.2; P⫽.013). Performance on the shoe tying tasks differed across the 3 groups. As can be seen in figure 2, there were significant group differences in shoe tying speed (F2,107⫽9.43; P⬍.001) and number of correct trials (F2,107⫽5.93; P⫽.004). Post hoc Tukey tests demonstrated that both stroke groups performed similarly to one another but more poorly than the control group for speed (P⬍.001) and number of correct trials (P⬍.001). To determine whether shoe tying performance was associated with different underlying cognitive deficits, we conducted bivariate correlations and follow-up ordinal logistic regressions within each brain-damaged group. We examined whether spatial skills (Block Design performance), limb praxis, and language skills (Aphasia Quotient from the Western Aphasia Battery) were associated with number of correct trials and speed for ipsilesional shoe tying. Because of the limited range of the variables and because of inhomogeneous variance, we
Fig 2. Mean time to tie shoe on the left (A) and mean number of correct trials (out of 10) on the right (B) for the control group, LHD stroke group, and RHD stroke group. SE bars displayed.
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IPSILESIONAL DEFICITS AFTER STROKE, Poole Table 2: Correlations Between Shoe Tying Performance and Cognitive Variables RHD
LHD
Cognitive Variables
Shoe Time Score
Total Correct Shoe Trials
Shoe Time Score
Total Correct Shoe Trials
Block Design (scale score) Limb apraxia (no. correct) Aphasia quotient
⫺.65 (.002) ⫺.31 (.18) ⫺.31 (.19)
.70 (.001) .26 (.27) ⫺.11 (.66)
⫺.22 (.26) ⫺.46 (.013) ⫺.30 (.128)
.38 (.045) .46 (.014) .30 (.127)
NOTE. Values are Spearman correlations; P values are inside parentheses (P).
used nonparametric correlations () (table 2). Aphasia quotient did not correlate with either shoe tying measure for either group. For the RHD group, only spatial skills were associated with shoe tying performance (⫽⫺.65, P⬍.01 for shoe tying speed; ⫽.70, P⫽.001 for shoe tying number correct). For the LHD group, limb praxis (number correct) was associated with shoe tying performance (⫽⫺.46, P⬍.05 for shoe tying speed; ⫽.46, P⬍.05 for shoe tying number correct), but spatial skills were also significantly associated with shoe tying accuracy (⫽.38, P⬍.05). To explore in the LHD group whether limb praxis or spatial abilities were uniquely associated with shoe tying accuracy, we conducted a regression with shoe tying accuracy as the dependent variable and limb praxis accuracy and Block Design scores as the predictor variables. The data did not meet statistical assumptions for linear regression, so a nonparametric ordinal logistic regression was used. The ordinal logistic regression (simultaneous entry method) indicated that both limb praxis and Block Design were unique predictors (Wald statistic⫽4.50, P⬍.05, df⫽1, OR⫽.33 for Block Design; Wald statistic⫽4.98, P⬍.05, df⫽1, OR⫽.33 for limb praxis). Thus it appears that only spatial skills predict shoe tying performance accuracy and speed in the RHD group. While limb praxis uniquely predicts shoe tying speed in the LHD group, both limb praxis and spatial skills predict shoe tying accuracy in that group. DISCUSSION Shoe tying performance of patients with LHD or RHD was impaired relative to an able-bodied control group for speed and accuracy. While the 2 stroke groups performed similarly, our results showed that the cognitive deficits that were associated with ipsilateral shoe tying deficits were somewhat different in the 2 groups. We found that spatial skills, which are most impaired after RHD, were most strongly associated with the RHD group’s shoe tying accuracy and speed. Limb praxis, which is most impaired after LHD, predicted shoe tying accuracy and speed after LHD. However, spatial skills also predicted shoe tying accuracy in the LHD group. While there is not an obvious reason why shoe tying accuracy but not speed was associated with spatial skills after LHD, this pattern of group differences generally reflects the cognitive deficits differentially associated with LHD or RHD, and the dependence of shoe tying on limb praxis as well as spatial ability. For all 3 groups, there was a negative correlation between total correct and shoe tying time (healthy control, ⫽⫺.63, P⬍.001; RHD, ⫽⫺.53, P⬍.05; LHD, ⫽⫺.72, P⬍.01). In all groups, participants who had more correct trials tied the shoe more quickly, suggesting there was no evidence of the typical speedaccuracy tradeoff in which increased accuracy is associated with increased performance time. Many studies have demonstrated the left hemisphere’s dominance for limb praxis and the right hemisphere’s dominance for spatial abilities.9,29,30 In addition, while spatial skills are more frequently associated with the right hemisphere, there is evidence that the left hemisphere also plays a role, as evi-
denced by more subtle and qualitatively different deficits in Block Design performance after left than RHD.31,32 While it is possible that these Block Design deficits after LHD could be a result of the spatial and temporal deficits associated with ideomotor limb apraxia, our results show that limb apraxia is not significantly associated with Block Design performance in the LHD group (⫽.28; P⫽.15) or the RHD group (⫽.32; P⫽.12). When motor tasks are dependent on cognitive skills, performance of the ipsilesional as well as the contralesional limb is often affected because the cognitive abilities necessary to direct the motor performance are impaired. Because shoe tying clearly requires spatial skills and spatial and temporal control of movement, which is impaired in people with ideomotor limb apraxia,16,33 it is not surprising that performance on this task was impaired in the ipsilesional limb of the LHD and RHD stroke groups in this study. These findings agree with others who have shown (1) ipsilesional deficits after stroke in functional tasks involving manipulation and (2) relationships between limb apraxia and activities of daily living,19 including dressing,2 mealtime behavior,17 and simulated activities of daily living.18 Other literature has also demonstrated that the deficits seen after stroke are dependent on task complexity in relation to site of brain damage. For simple motor tasks with minimal cognitive requirement, such as grip strength or finger tapping, contralesional but not ipsilesional deficits are seen after RHD or LHD.34 This is the case in the current data. In contrast, performance deficits in both the contralesional and ipsilesional upper limb are observed with more complex tasks that require greater cognitive processing, which increases the probability that bilateral hemispheric control is necessary. These complex tasks include target aiming,35 peg rotation and insertion,34,36 maze coordination,34 and tasks associated with daily living, such as the Jebsen Hand Function Test18 and the Timed Motor Performance test.20 It is not known whether the ipsilesional deficits seen after LHD or RHD in the tasks mentioned are caused by different mechanisms, which is potentially important from a rehabilitation standpoint. Our kinematic studies of arm reaching have shown just this, not by relating motor deficits to cognitive deficits but by identifying different motor control deficits after LHD or RHD. These studies showed that LHD produced deficits in the dynamic characteristics of the movement (eg, poorer interjoint coordination resulting in greater curvature and less efficient movement) and RHD produced deficits in steady-state positional control, as measured by final position accuracy.37,38 However, we are not aware of kinematic studies that examined hemispheric difference in the interjoint coordination of the fingers. The current findings that limb apraxia and spatial deficits, not aphasia, were predictors of shoe tying is of interest from a therapeutic standpoint. Although language areas of the brain have been shown to be active in the early stages of motor learning of sequencing tasks,39 our findings suggest that language ability was less important than spatial abilities and limb praxis for learning this task. This may be because the mode of Arch Phys Med Rehabil Vol 90, October 2009
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instruction was visual (demonstration) as well as verbal, and it suggests that the presence of aphasia should not automatically exclude a patient from such training if it is one of their goals. The current results and those from a previous study suggest that persons with LHD or RHD caused by stroke can learn the 1-handed shoe tying method.21,22 Moreover, several studies have shown that individuals with limb apraxia can learn and improve their ability to perform daily tasks with practice, cognitive strategy training, and/or video feedback.3,5,40,41 A recent study showed that training focused on practicing symbolic and nonsymbolic gestures resulted in a significant reduction in errors in gestural performance in an LHD group compared with an LHD group who received conventional therapy for aphasia. A second study showed that improvements with this intervention generalized to improvements in functioning in activities of daily living.42 Videotape feedback with or without occupational therapy intervention has also been effective in learning to don socks and shoes poststroke,43 but limb apraxia was not examined. Study Limitations We assessed time and number of correct trials to tie the shoe but did not analyze errors. An analysis of errors may have identified qualitative differences among the groups that would allow us to explore underlying mechanisms for the deficits across groups. As noted, the shoe was placed on a table to eliminate the impact of poor balance on performance. Participants who were able to tie the shoe on the table might not be able to reach or maintain their balance to tie a shoe on their feet in a real-life situation. CONCLUSIONS Our findings in persons with chronic stroke suggest that deficits do persist in the ipsilesional limb after unilateral stroke when performing a 1-handed shoe tying task. This in combination with the fact that patients with hemiparesis (especially those with left hemiparesis) use their ipsilesional limb much more frequently than their contralesional limb44,45 suggests that rehabilitation professionals should consider assessment of limb apraxia and skill training and practice for the ipsilesional limb in the performance of everyday tasks. Further studies might want to examine whether interventions for apraxia and spatial deficits would lead to improved shoe tying. Acknowledgments: The authors thank Robert T. Knight, MD, for neuroimaging consultation. References 1. Grimby G, Andren E, Daving Y, Wright B. Dependence and perceived difficulty in daily activities in community-living stroke survivors 2 years after stroke: a study of instrumental structures. Stroke 1998;29:1843-9. 2. Walker MF, Lincoln NB. Factors influencing dressing performance after stroke. J Neurol Neurosurg Psychiatry 1991;54:699701. 3. van Heugten CM, Dekker J, Deelman BG, van Dijk AJ, Stehmann-Saris JC, Kinebanian A. Outcome of strategy training in stroke patients with apraxia: a phase II study. Clin Rehabil 1998; 12:294-303. 4. Walker CM, Sunderland A, Sharma J, Walker MF. The impact of cognitive impairment on upper body dressing difficulties after stroke: a video analysis of patterns of recovery. J Neurol Neurosurg Psychiatry 2004;75:43-8. 5. Goldenberg G, Hagmann S. Therapy of activities of daily living in patients with apraxia. Neuropsychol Rehabil 1998;8:123-41. Arch Phys Med Rehabil Vol 90, October 2009
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Arch Phys Med Rehabil Vol 90, October 2009