Comparison of Gait Parameters Across Three Attentional Loading Conditions During Timed Up and Go Test in Stroke Survivors Haidzir Manaf, BSc (Applied Rehab),1 Maria Justine, PhD,1 Goh Hui Ting, PhD, PT,2 and Lydia Abd Latiff, MD2 1
Department of Physiotherapy, Faculty of Health Sciences, Universiti Teknologi MARA, Puncak Alam Campus, Selangor, Malaysia; 2 Department of Rehabilitation Medicine, Faculty of Medicine, University Malaya, Kuala Lumpur, Malaysia Background: Little is known about the effects of attentional loading on performance of turning during walking in individuals with stroke. Objective: The authors used a cross-sectional experimental design to compare gait parameters in stroke survivors across 3 attentional loading conditions (single, dual-motor, and dual-cognitive conditions) during a Timed Up and Go (TUG) test. Methods: Data were collected from 20 stroke survivors (12 males, 8 females; mean age, 60.5 ± 10.6 years). We compared the number of steps and time measured during the TUG test under 3 attentional loading conditions and 2 turning directions (nonparetic and paretic sides). We further divided the TUG test into straight walking and turning phases. Results: The number of steps and the time taken during TUG test increased significantly from singleto dual-task conditions (dual motor and dual cognitive). However, there were no significant differences in gait parameters between turning toward the nonparetic and paretic sides. Conclusions: These findings suggested that gait performance was compromised during dual-task conditions for individuals with stroke. Attentional loading may be incorporated into routine gait assessment and rehabilitation to ensure a successful recovery. Key words: attention, cognitive, gait, motor, rehabilitation, stroke
oss of walking ability is one of the major activity limitations among stroke survivors. Approximately 65% to 85% of stroke survivors regain capability to walk independently within 6 months post stroke.1 Despite the increasing number of ambulating stroke survivors, concerns have been raised about the safety during walking, especially outdoor walking. Walking outdoors is a challenging task for stroke survivors, because they need to overcome obstacles and change direction (turning) under the pressure of many distractions.2 Skillful turning during walking is one of the key factors for functional ambulation.3 Turning during walking involves sequences of slowing down or stopping of walking and reorientation of head, trunk, and lower limbs toward the new direction.4,5 Stroke survivors with sensorimotor impairments may have difficulty in organizing
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proper turning sequences. This may put them at risk of falls. A previous study showed that fall injuries during turning were 8 times more likely than during straight walking.6 Furthermore, most falls occurred during turning toward the paretic side.7 Turning while performing other tasks further challenges gait safety as it impose great demands on the attentional system. 3,8 Attention is conceptualized as the information-processing capacity required to perform a task, and it can be categorized into sustained, selective, divided, and switching attention.9 We primarily focused on divided attention, which refers to the ability to carry out more than one task at the same time.9 Divided attention is often studied using a dual-task interference paradigm under the
Corresponding author: Haidzir Manaf, Physiotherapy Department, Faculty of Health Sciences, Universiti Teknologi MARA, Puncak Alam Campus, 42300 Puncak Alam, Selangor, Malaysia; phone: +60126615246; e-mail: [email protected],
Top Stroke Rehabil 2014;21(2):128–136 © 2014 Thomas Land Publishers, Inc. www.strokejournal.com
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doi: 10.1310/tsr2102-128
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assumption that the attentional resource is fixed in capacity. Dual-task interference might occur if the available attentional capacity is exceeded, thus causing a performance deterioration in either one or both tasks.10 Few studies have shown that dual-tasking had detrimental effects on gait parameters, including gait speed, stride length, and double-support time during straight walking in stroke survivors.11-14 To date, no study has investigated the effects of attentional loading or dual-tasking on gait performance during turning in stroke survivors. Therefore, it is paramount to investigate the effects of attentional loading on gait parameters to gain further insights of gait recovery post stroke. The Timed Up and Go (TUG) test is a performance-based tool used to assess balance and mobility performance as well as turning ability in the populations with various diagnoses.8 The TUG test measures the time taken for an individual to stand up from a chair, walk 3 meters, turn around, walk 3 meters back to the chair, and sit down.15 The time taken to complete the TUG test has been shown to predict falls in community-dwelling elderly16 and stroke survivors.17 Furthermore, if an individual takes more than 5 steps or more than 3 seconds to complete the turning during the TUG test, he or she is considered to have turning difficulty.18 The TUG test consists of dualtask conditions as well. Previous study has found that performing the TUG test under a dual-task condition increased the time taken to complete the task, and the effect was greater in elderly with history of falls than those without.16 The nature and sensitivity of the TUG test make it a good tool to capture the effects of attentional loading on gait parameters in turning and walking among stroke survivors. Accordingly, the objective of this study was to examine the effects of attentional loading conditions (dual-motor and dual-cognitive task conditions) on gait parameters in stroke survivors during the TUG test. We also compared the effects of turning direction in each condition. We hypothesized that stroke survivors would take a greater number of steps and longer time to complete the TUG test under attentional loading conditions (dual motor and dual cognitive) compared to a single-task condition, especially when turning toward the paretic side.
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Methods Participants
Twenty stroke survivors (12 males, 8 females) participated in this study. The inclusion criteria were as follows: (1) at least 6 months post stroke with unilateral hemiparesis as diagnosed by a medical physician, (2) age range between 40 to 80 years old, (3) able to walk continuously for 10 meters independently without walking aid,12 (4) able to hold a glass full of water with the nonaffected hand, and (5) able to follow one-step commands. Participants were excluded if they had more than one stroke or had other neurologic disorders (eg, Parkinson’s disease and traumatic brain injury) or orthopedic conditions (eg, joint deformities, osteoarthritis, and rheumatoid). They were also excluded if they had visual field defects or scored less than 24 on the MiniMental State Examination (MMSE).19 Prior to the procedure, participants signed an informed consent form approved by the institutional ethics committee.
Testing procedure
The participants’ demographic data were recorded after consent. In addition, we measured their cognitive function with the MMSE,20 stroke severity with the Fugl-Myer Assessment (FMA),21 and balance with the Berg Balance Scale (BBS).22 The FMA is a valid measure of voluntary movement control after stroke; it consists of 33 items in the upper extremity subscale (score range, 0-66) and 17 items in the lower extremity subscale (score range, 0-34).23 A higher score in FMA suggests a less severe stroke compared to a lower score. BBS consists of 14 items that evaluate balance in different activities.22 Each item in the BBS is scored on a 5-point scale (0-4) with a maximum total score of 56 (higher scores indicates better balance). A cutoff score of 45 predicts risk of falls.24 After the clinical assessment, participants were asked to perform the TUG test. Prior to testing, the researcher demonstrated the procedure to the participants. The participants performed 3 practice trials to familiarize themselves with the test. The participants wore their regular footwear
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Turning 180° event start Straight walking (3-meter)
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Figure 1. Diagrammatic presentation of Timed Up and Go test.
and orthoses during testing. Gait performance was recorded using a digital video camera (30 frames per second). The researcher used a video camera mounted on a tripod that was placed in the sagittal plane of movement. The experiment was conducted in a physiotherapy gymnasium with fluorescent bright white lighting conditions. The floor was a standard hard and even surface. At the end of the 3-meter walkway, the turning area (1 x 1 meter) was marked on the floor to indicate the area in which participants were asked to turn around (Figure 1). The dimension was chosen because most of the turning set ups in the community such as hallways, doorways, and sidewalks have a similar dimension.25 Participants consistently walked inside the turning area on all the experimental trials. The test consisted of 3 conditions in the following order: 1. Single-task condition: During the single-task condition, stroke survivors performed the TUG test only (without secondary task). A standard armchair was used and a cone was placed at the 3-meter mark of the walk path. Participants sat comfortably with their back against the chair and the experimenter gave the following instruction: “When I say ‘go’, please stand up from the chair and walk to the cone. Turn to your right/left after you pass the cone, walk back, and sit down on the chair. Please walk at your comfortable speed.” The participants were asked to turn
toward the nonparetic side for 3 trials. After a 5-minute rest, participants repeated the same procedure but turned toward the paretic side for another 3 trials. Once the single-task condition was completed, participants were given a 5-minute rest prior to performing the dual-motor task TUG test. 2. Dual-motor task condition: For the dualmotor task condition, participants sat comfortably with their back against the chair while holding a glass full of water with their nonaffected hand. When the experimenter said “go,” they stood up from the chair, walked 3 meters at a comfortable speed, turned 180° toward the nonparetic side, walked 3 meters back to the chair, and sat down. This was repeated for 3 trials. After a 5-minute break, participants repeated the same procedure but turned toward the paretic side. During testing, participants were instructed to hold the glass without spilling the water (prioritized glass holding); if they spilled the water, the trial would be considered as a failed trial and be repeated. On average, 10% of trials were repeated. 3. Dual-cognitive task conditions: Participants sat comfortably with their back against the chair. The experimenter verbally gave them a number (any number from 20 to 100). Participants then counted backwards by 3 from the number consecutively and gave verbal responses. For example, if the given
Gait Parameters and TUG in Stroke Survivors
number was 50, participants responded as “47, 44, 41….” When they heard “go,” they stood up from the chair, walked 3 meters at a comfortable speed, turned 180° toward the non-paretic side, walked 3 meters back to the chair, and sat down. This was repeated for 3 times. After a 5-minute break, participants repeated the same procedure but turned toward the paretic side for 3 trials. During the test, participants had to count continuously; if they did not, it would be considered as a failed trial and be repeated. On average, 30% of trials were repeated. Outcome and statistical analysis
From the recorded video, we obtained our primary outcomes, which were time and number of steps taken to complete the TUG test. We averaged 3 trials for each condition. We further divided the TUG test into turning and straight walking phases to gain information about whether attentional loading had a differential effect on each phase. The turning phase started at the time when the foot first contacted the turning area after walking for 3 meters (Figure 1) and ended when the foot left the turning area.3 The straight walking phase consisted of the 3-meter walk toward to the turning area and 3-meter walk back to the chair. The data were analyzed using the IBM SPSS statistical software version 19 (IBM, Armonk, NY). Descriptive statistics and tests for normality were carried out for all outcome variables. Repeated measures analysis of variance (ANOVA) was used to analyze gait parameters across 3 attentional loading conditions (single-, dual-motor, and dualcognitive task conditions) and 2 turning directions (nonparetic and paretic). A post hoc Bonferroni comparison was performed when the repeated measure ANOVA test revealed a significant difference (P < .05). Results
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body weight was 66.1 ± 4.5 kg (range, 58-74 kg), and body height was 1.7 ± 0.1 m (range, 1.61.7 m). Twelve participants presented with left hemiparesis and 8 with right hemiparesis. The average score on the MMSE was 24 ± 1.2, the average score on the FMA was 23.9 ± 1.2 (motor) and 11.0 ± .3 (sensory), and the average rating on the BBS was 45.0 ± 6.7. TUG test
Figure 2A shows the time taken to complete the TUG test under 3 attentional loading conditions and 2 turning directions. Attentional loading had a significant influence on the time taken to complete the TUG test. This is confirmed by a significant condition effect, F(2, 38) = 8.14, P < .01. Post hoc pairwise comparisons with adjusted P value of .02 indicated that the dual-motor (P = .00) and dual-cognitive (P = .00) conditions led to a longer time taken compared to the single-task condition. However, there was no difference between dualmotor and dual-cognitive task conditions (P = 1.0). There was no significant difference between turning toward the nonparetic and paretic sides, F(1, 19) = 3.16, P = .09. In addition, there was no significant interaction between task conditions and turning directions, F(2, 38) = .68, P = .51. Number of steps taken to complete the TUG test was also affected by the attentional loading, which was confirmed by a significant condition effect, F(2, 38) = 8.36, P < .01 (Figure 2B). Post hoc pairwise comparisons showed that the dual-motor (P = .00) and dual-cognitive (P = .00) conditions resulted in significantly greater number of steps than the single-task condition. However, there was no difference between the dual-motor and dualcognitive task conditions (P = 1.0). There was no significant difference in the number of steps taken between the turning toward the nonparetic and paretic sides, F(1, 19) = .12, P = .74. In addition, there was no interaction between task conditions and turning directions, F(2, 38) = .65, P = .53.
Participants
Turning phase of TUG
The mean age of the participants was 60.5 ± 10.6 years (range, 45-80). The average time post stroke was 9.7 ± 3.5 months (range, 6-18 months),
Attentional loading had a significant influence on time taken to complete the 180° turning. This is confirmed by a significant condition effect,
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task condition (P = .01). However, there was no difference between the dual-cognitive and single-task conditions (P = .05). In addition, there was no difference between the dual-motor and
F(2, 38) = 4.7, P = .02 (Figure 2C). Post hoc pairwise comparisons with an adjusted P value of .02 indicated that the dual-motor condition led to a longer time taken compared to the singleA
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Figure 2. Comparison of gait parameters across three attentional loading conditions: (A) time taken to complete Timed Up and Go (TUG) test; (B) number of steps to complete TUG; (C) time taken to complete turning 180°; (D) number of steps to complete turning 180°; (E) time taken to complete straight walking; (F) number of steps to complete straight walking phase.
Gait Parameters and TUG in Stroke Survivors
dual-cognitive task conditions (P = 1.0). There was no significant difference between turning toward the nonparetic and paretic sides, F(1, 19) = .07, P = .79. In addition, there was no significant interaction between task conditions and turning directions, F(2, 38) = .83, P = .45. Number of steps taken to complete the 180° turning was also affected by the attentional loading, which was confirmed by a significant condition effect, F(2, 38) = 3.9, P = .03 (Figure 2D). However, post hoc pairwise comparisons failed to detect any significant difference in number of steps among any pairs (dual motor vs single, P = .05; dual cognitive vs single, P = .84; dual motor vs dual cognitive, P =.32). There was no significant difference between turning toward the nonparetic and paretic sides, F(1, 19) = .07, P = .26. In addition, there was no interaction between task conditions and turning directions, F(2, 38) = .83, P = .64. Straight walking phases
Attentional loading had a significant influence on time taken to complete the straight walking phase of the TUG test. This is confirmed by a significant condition effect, F(2, 38) = 7.98, P 1.0). There was no significant difference in the time taken between turning toward the nonparetic and paretic sides, F(1, 19) = 2.81, P = .11. In addition, there was no significant interaction between task conditions and turning directions, F(2, 38) = .76, P = .48. Attentional loading also had a significant influence on number of steps taken to complete the straight walking. This is confirmed by a significant condition effect, F(2, 38) = 8.42, P < .01 (Figure 2F). Post hoc pairwise comparisons indicated that both the dual-motor (P =.00) and dual-cognitive (P =.00) conditions led to a greater number of steps taken compared to the single-task condition. However, there was no difference between the dual-motor and dual-cognitive task conditions (P = 1.0). There was no significant difference between
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turning toward the nonparetic and paretic sides, F(1, 19) = .003, P = .96. In addition, there was no significant interaction between task conditions and turning directions, F(2, 38) = .58, P = .57. Discussion Deterioration of gait performance during attentional loading in stroke survivors has been reported previously.11,12,14,26 Little is known about the effects of the attentional loading during turning in stroke survivors. This study focused on the divided attention 27 in which stroke survivors performed turning while walking (TUG test) and carried out a secondary task simultaneously (holding a cup or counting backward). We presented a few important findings. First, attentional loading adversely affected gait performance in stroke. Second, the loading types and turning directions did not lead to differential effects in TUG performance. Last, attentional loading effects on gait performance during straight walking and turning were not similar. Attentional loading conditions
We found that stroke survivors experienced a marked deterioration in their gait performance (time taken and number of steps) when they were required to perform 2 tasks simultaneously. This is possibly due to a combination of various factors including deficits in executive function, impaired divided attention, and gait impairments.9 Dual-task interference in motor performance has been explained by several neuropsychological theories including the capacity-sharing theory, bottleneck model, and multiple resource model.10 Our data are best explained by the capacitysharing theory. The capacity-sharing theory assumes that attentional resources are fixed in capacity and task performance depends on the amount of resources that are allocated to the task.9 Superior performance is expected when most of the resources are allocated to the task as in a single-task condition. Under a dual-task condition, deterioration of task performance will be observed as attentional resources that are allocated to both tasks are reduced. The deterioration of performance will be
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observed in either one or both tasks, depending on task prioritization strategy. In this study, both the TUG test and secondary task (motor or cognitive) may tax the limited attention resource. Participants were given the instruction to prioritize the performance of the secondary task (holding the glass or counting backwards); therefore, the walking and turning task (TUG) was compromised to optimize performance on the secondary task. As a result, stroke survivors demonstrated deterioration in gait performance when they were required to perform 2 tasks simultaneously. Another interesting observation in this study was the similar effects of attentional loading between dual-motor and dual-cognitive task conditions. Initially, the dual-cognitive task condition was speculated to be more challenging than the dual-motor task condition, and we expected to observe greater deterioration in gait under the dual-cognitive task condition than the dual-motor condition. One possible explanation for this finding may be related to the strategy chosen by the participants. In this study, stroke survivors were given the instruction to prioritize the secondary task. However, when inspecting the video, we found that stroke survivors took a longer time to perform backward counting continuously and some of the answers were not accurate. This unexpected finding could be a result of compensatory strategies such as sacrificing dual-cognitive task performance (reaction time, accuracy) for stability.
In the present study, we hypothesized that stroke survivors would demonstrate gait performance decrement and turning difficulties when turning toward the paretic side compared to nonparetic side, because stroke survivors often show difficulty when weight-shifting toward the paretic side. In this study, we found no difference in gait performance between turning directions. The findings are consistent with a previous study in which no significant difference in turning toward the paretic or nonparetic sides was found.28 This is probably due to the training effect on each turning directions; stroke survivors may adopt the stepping strategy to navigate the turn toward the paretic side.
Straight walking vs turning phases
Study limitations
We found that straight walking was influenced by both types of attentional loading. However, only the dual-motor task condition increased the time taken to complete the turning phase. The difference in response to attentional loading between straight walking and turning suggests that straight walking and turning may involve different motor control mechanisms and should be examined separately. During the straight walking phase, participants first accelerated and then decelerated when they approached the target (turning area or chair). Therefore, speed control may be the priority. In contrast, during the turning phase, the reorientation of body segments to the
There are several limitations of this study. First, we did not control the trade-off between the walking task and the counting backward task. Some of the participants showed little change in the gait performance, but their cognitive task performance was compromised, as demonstrated by slower responses. Second, we did not randomize the order for each condition and turning direction, which may have caused a training effect and resulted in no difference between conditions and turning directions. In addition, some of the participants were asked to repeat failed trials with an average of 2 to 3 trials for each dual-task condition. Repeating trials may
new direction in a coordinated manner may be critical. Hence, it is not surprising to observe such differences when different attentional loading was imposed. During the dual-motor condition, the longer time taken to turn was not accompanied by an increased number of steps. This may be related to the stepping strategy used during the TUG test. During 180° turning, participants slowed down their gait speed and paused between steps. The pauses between steps may explain why the time taken to complete turning increased under the dual-motor task whereas the number of steps remained the same. Turning direction
Gait Parameters and TUG in Stroke Survivors
enhance the training effects. Third, this study only included stroke survivors but not age-matched controls. Thus, it is inconclusive whether the gait deterioration under the dual-task condition was a result of stroke or aging. It is recommended that future studies compare stroke survivors to healthy age- and gender-matched controls. In addition, the procedure was conducted in a controlled environment (lab) that was quiet and with a level walking surface that might not be representative of a regular environment encountered by the participants on a daily basis. Conclusions
Turning difficulty is a common activity limitation in stroke survivors. The current study revealed that stroke survivors required a longer time and a greater number of steps to perform
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a turn under a dual-task condition. Thus, it is recommended that dual-task turning may be incorporated in gait assessment to provide information in addition to straight walking, ascending and descending stairs, and overcoming barriers (eg, slopes, curbs). Acknowledgments Financial support/disclosures: This study was supported by Research Management Institute (RMI) via Research Intensive Faculty (RIF) grants, Universiti Teknologi MARA (UiTM) Malaysia [600-RMI/DANA 5/3/RIF (247/2012)]. Conflicts of interest: The authors declare no potential conflicts of interest with respect to the authorship and/or publication of this article.
REFERENCES 1. Wade D, Wood V, Heller A, Maggs J, Langton HR. Walking after stroke. Measurement and recovery over the first 3 months. Scand J Rehabil Med. 1987;19(1):25. 2. Lord SE, Rochester L, Weatherall M, McPherson KM, McNaughton HK. The effect of environment and task on gait parameters after stroke: A randomized comparison of measurement conditions. Arch Phys Med Rehabil. 2006;87(7):967-973. 3. Lam T, Luttmann K. Turning capacity in ambulatory individuals poststroke. Am J Phys Med Rehabil. 2009;88(11):873-883; quiz 884-876, 946. 4. Imai T, Moore ST, Raphan T, Cohen B. Interaction of the body, head, and eyes during walking and turning. Exp Brain Res. 2001;136(1):1-18. 5. Patla AE, Adkin A, Ballard T. Online steering: Coordination and control of body center of mass, head and body reorientation. Exp Brain Res. 1999;129(4):629-634. 6. Cumming RG, Klineberg RJ. Fall frequency and characteristics and the risk of hip fractures. J Am Geriatr Soc. 1994;42(7):774-778. 7. Hyndman D, Ashburn A, Stack E. Fall events among people with stroke living in the community: Circumstances of falls and characteristics of fallers. Arch Phys Med Rehabil. 2002;83(2): 165-170. 8. Hollands KL, Hollands MA, Zietz D, Wing AM, Wright C, van Vliet P. Kinematics of turning 180 degrees during the Timed Up and Go in stroke survivors with and without falls history. Neurorehabil Neural Repair. 2010;24(4): 358-367.
9. Yogev-Seligmann G, Hausdorff JM, Giladi N. The role of executive function and attention in gait. Movement Disord. 2008;23(3):329-342. 10. Pashler H. Dual-task interference in simple tasks: Data and theory. Psychol Bull. 1994;116(2):220. 11. Yang YR, Chen YC, Lee CS, Cheng SJ, Wang RY. Dual-task-related gait changes in individuals with stroke. Gait Posture. 2007;25(2):185-190. 12. Plummer-D’Amato P, Altmann LJ, Saracino D, Fox E, Behrman AL, Marsiske M. Interactions between cognitive tasks and gait after stroke: A dual task study. Gait Posture. 2008;27(4):683-688. 13. Hyndman D, Pickering RM, Ashburn A. Reduced sway during dual task balance performance among people with stroke at 6 and 12 months after discharge from hospital. Neurorehabil Neural Repair. 2009;23(8):847-854. 14. Bowen A, Wenman R, Mickelborough J, Foster J, Hill E, Tallis R. Dual-task effects of talking while walking on velocity and balance following a stroke. Age Ageing. 2001;30(4):319-323. 15. Podsiadlo D, Richardson S. The timed “Up & Go”: A test of basic functional mobility for frail elderly persons. J Am Geriatr Soc. 1991;39(2):142. 16. Shumway-Cook A, Brauer S, Woollacott M. Predicting the probability for falls in communitydwelling older adults using the Timed Up & Go Test. Phys Ther. 2000;80(9):896-903. 17. Ng SS, Hui-Chan CW. The Timed Up & Go Test: Its reliability and association with lower-limb impairments and locomotor capacities in people with chronic stroke. Arch Phys Med Rehabil. 2005;86(8):1641-1647.
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18. Thigpen MT, Light KE, Creel GL, Flynn SM. Turning difficulty characteristics of adults aged 65 years or older. Phys Ther. 2000;80(12):1174-1187. 19. Zarina Z, Zahiruddin O, AH CW. Validation of Malay Mini Mental State Examination. Malaysian J Psychiatry. 2007;16(1). 20. Folstein MF, Folstein SE, McHugh PR. “Minimental state.” A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12(3):189-198. 21. Fugl-Meyer A, Jääskö L, Leyman I, Olsson S, Steglind S. The post-stroke hemiplegic patient. 1. A method for evaluation of physical performance. Scand J Rehabil Med. 1975;7(1):13. 22. Berg K. Measuring balance in the elderly: Preliminary development of an instrument. Physiother Canada. 1989;41(6):304-311. 23. Duncan PW, Propst M, Nelson SG. Reliability of the Fugl-Meyer assessment of sensorimotor recovery following cerebrovascular accident. Phys Ther. 1983;63(10):1606-1610.
24. Maeda N, Kato J, Shimada T. Predicting the probability for fall incidence in stroke patients using the Berg Balance Scale. J Int Med Res. 2009;37(3):697-704. 25. Orendurff MS, Segal AD, Berge JS, Flick KC, Spanier D, Klute GK. The kinematics and kinetics of turning: Limb asymmetries associated with walking a circular path. Gait Posture. 2006;23(1):106-111. 26. Haggard P, Cockburn J, Cock J, Fordham C, Wade D. Interference between gait and cognitive tasks in a rehabilitating neurological population. J Neurol Neurosurg Psychiatry. 2000;69(4):479-486. 27. Woollacott M, Shumway-Cook A. Attention and the control of posture and gait: A review of an emerging area of research. Gait Posture. 2002;16(1):1-14. 28. Faria C, Teixeira-Salmela LF, Nadeau S. Effects of the direction of turning on the Timed Up & Go Test with stroke subjects. Top Stroke Rehabil. 2009;16(3):196-206.
Department of Physiotherapy, Faculty of Health Sciences, Universiti Teknologi MARA, Puncak Alam Campus, Selangor, Malaysia; 2 Department of Rehabilitation Medicine, Faculty of Medicine, University Malaya, Kuala Lumpur, Malaysia Background: Little is known about the effects of attentional loading on performance of turning during walking in individuals with stroke. Objective: The authors used a cross-sectional experimental design to compare gait parameters in stroke survivors across 3 attentional loading conditions (single, dual-motor, and dual-cognitive conditions) during a Timed Up and Go (TUG) test. Methods: Data were collected from 20 stroke survivors (12 males, 8 females; mean age, 60.5 ± 10.6 years). We compared the number of steps and time measured during the TUG test under 3 attentional loading conditions and 2 turning directions (nonparetic and paretic sides). We further divided the TUG test into straight walking and turning phases. Results: The number of steps and the time taken during TUG test increased significantly from singleto dual-task conditions (dual motor and dual cognitive). However, there were no significant differences in gait parameters between turning toward the nonparetic and paretic sides. Conclusions: These findings suggested that gait performance was compromised during dual-task conditions for individuals with stroke. Attentional loading may be incorporated into routine gait assessment and rehabilitation to ensure a successful recovery. Key words: attention, cognitive, gait, motor, rehabilitation, stroke
oss of walking ability is one of the major activity limitations among stroke survivors. Approximately 65% to 85% of stroke survivors regain capability to walk independently within 6 months post stroke.1 Despite the increasing number of ambulating stroke survivors, concerns have been raised about the safety during walking, especially outdoor walking. Walking outdoors is a challenging task for stroke survivors, because they need to overcome obstacles and change direction (turning) under the pressure of many distractions.2 Skillful turning during walking is one of the key factors for functional ambulation.3 Turning during walking involves sequences of slowing down or stopping of walking and reorientation of head, trunk, and lower limbs toward the new direction.4,5 Stroke survivors with sensorimotor impairments may have difficulty in organizing
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proper turning sequences. This may put them at risk of falls. A previous study showed that fall injuries during turning were 8 times more likely than during straight walking.6 Furthermore, most falls occurred during turning toward the paretic side.7 Turning while performing other tasks further challenges gait safety as it impose great demands on the attentional system. 3,8 Attention is conceptualized as the information-processing capacity required to perform a task, and it can be categorized into sustained, selective, divided, and switching attention.9 We primarily focused on divided attention, which refers to the ability to carry out more than one task at the same time.9 Divided attention is often studied using a dual-task interference paradigm under the
Corresponding author: Haidzir Manaf, Physiotherapy Department, Faculty of Health Sciences, Universiti Teknologi MARA, Puncak Alam Campus, 42300 Puncak Alam, Selangor, Malaysia; phone: +60126615246; e-mail: [email protected],
Top Stroke Rehabil 2014;21(2):128–136 © 2014 Thomas Land Publishers, Inc. www.strokejournal.com
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assumption that the attentional resource is fixed in capacity. Dual-task interference might occur if the available attentional capacity is exceeded, thus causing a performance deterioration in either one or both tasks.10 Few studies have shown that dual-tasking had detrimental effects on gait parameters, including gait speed, stride length, and double-support time during straight walking in stroke survivors.11-14 To date, no study has investigated the effects of attentional loading or dual-tasking on gait performance during turning in stroke survivors. Therefore, it is paramount to investigate the effects of attentional loading on gait parameters to gain further insights of gait recovery post stroke. The Timed Up and Go (TUG) test is a performance-based tool used to assess balance and mobility performance as well as turning ability in the populations with various diagnoses.8 The TUG test measures the time taken for an individual to stand up from a chair, walk 3 meters, turn around, walk 3 meters back to the chair, and sit down.15 The time taken to complete the TUG test has been shown to predict falls in community-dwelling elderly16 and stroke survivors.17 Furthermore, if an individual takes more than 5 steps or more than 3 seconds to complete the turning during the TUG test, he or she is considered to have turning difficulty.18 The TUG test consists of dualtask conditions as well. Previous study has found that performing the TUG test under a dual-task condition increased the time taken to complete the task, and the effect was greater in elderly with history of falls than those without.16 The nature and sensitivity of the TUG test make it a good tool to capture the effects of attentional loading on gait parameters in turning and walking among stroke survivors. Accordingly, the objective of this study was to examine the effects of attentional loading conditions (dual-motor and dual-cognitive task conditions) on gait parameters in stroke survivors during the TUG test. We also compared the effects of turning direction in each condition. We hypothesized that stroke survivors would take a greater number of steps and longer time to complete the TUG test under attentional loading conditions (dual motor and dual cognitive) compared to a single-task condition, especially when turning toward the paretic side.
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Methods Participants
Twenty stroke survivors (12 males, 8 females) participated in this study. The inclusion criteria were as follows: (1) at least 6 months post stroke with unilateral hemiparesis as diagnosed by a medical physician, (2) age range between 40 to 80 years old, (3) able to walk continuously for 10 meters independently without walking aid,12 (4) able to hold a glass full of water with the nonaffected hand, and (5) able to follow one-step commands. Participants were excluded if they had more than one stroke or had other neurologic disorders (eg, Parkinson’s disease and traumatic brain injury) or orthopedic conditions (eg, joint deformities, osteoarthritis, and rheumatoid). They were also excluded if they had visual field defects or scored less than 24 on the MiniMental State Examination (MMSE).19 Prior to the procedure, participants signed an informed consent form approved by the institutional ethics committee.
Testing procedure
The participants’ demographic data were recorded after consent. In addition, we measured their cognitive function with the MMSE,20 stroke severity with the Fugl-Myer Assessment (FMA),21 and balance with the Berg Balance Scale (BBS).22 The FMA is a valid measure of voluntary movement control after stroke; it consists of 33 items in the upper extremity subscale (score range, 0-66) and 17 items in the lower extremity subscale (score range, 0-34).23 A higher score in FMA suggests a less severe stroke compared to a lower score. BBS consists of 14 items that evaluate balance in different activities.22 Each item in the BBS is scored on a 5-point scale (0-4) with a maximum total score of 56 (higher scores indicates better balance). A cutoff score of 45 predicts risk of falls.24 After the clinical assessment, participants were asked to perform the TUG test. Prior to testing, the researcher demonstrated the procedure to the participants. The participants performed 3 practice trials to familiarize themselves with the test. The participants wore their regular footwear
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Turning 180° event start Straight walking (3-meter)
1m 1m
Chair
Straight walking (3-meter) Turning 180° event finish
Figure 1. Diagrammatic presentation of Timed Up and Go test.
and orthoses during testing. Gait performance was recorded using a digital video camera (30 frames per second). The researcher used a video camera mounted on a tripod that was placed in the sagittal plane of movement. The experiment was conducted in a physiotherapy gymnasium with fluorescent bright white lighting conditions. The floor was a standard hard and even surface. At the end of the 3-meter walkway, the turning area (1 x 1 meter) was marked on the floor to indicate the area in which participants were asked to turn around (Figure 1). The dimension was chosen because most of the turning set ups in the community such as hallways, doorways, and sidewalks have a similar dimension.25 Participants consistently walked inside the turning area on all the experimental trials. The test consisted of 3 conditions in the following order: 1. Single-task condition: During the single-task condition, stroke survivors performed the TUG test only (without secondary task). A standard armchair was used and a cone was placed at the 3-meter mark of the walk path. Participants sat comfortably with their back against the chair and the experimenter gave the following instruction: “When I say ‘go’, please stand up from the chair and walk to the cone. Turn to your right/left after you pass the cone, walk back, and sit down on the chair. Please walk at your comfortable speed.” The participants were asked to turn
toward the nonparetic side for 3 trials. After a 5-minute rest, participants repeated the same procedure but turned toward the paretic side for another 3 trials. Once the single-task condition was completed, participants were given a 5-minute rest prior to performing the dual-motor task TUG test. 2. Dual-motor task condition: For the dualmotor task condition, participants sat comfortably with their back against the chair while holding a glass full of water with their nonaffected hand. When the experimenter said “go,” they stood up from the chair, walked 3 meters at a comfortable speed, turned 180° toward the nonparetic side, walked 3 meters back to the chair, and sat down. This was repeated for 3 trials. After a 5-minute break, participants repeated the same procedure but turned toward the paretic side. During testing, participants were instructed to hold the glass without spilling the water (prioritized glass holding); if they spilled the water, the trial would be considered as a failed trial and be repeated. On average, 10% of trials were repeated. 3. Dual-cognitive task conditions: Participants sat comfortably with their back against the chair. The experimenter verbally gave them a number (any number from 20 to 100). Participants then counted backwards by 3 from the number consecutively and gave verbal responses. For example, if the given
Gait Parameters and TUG in Stroke Survivors
number was 50, participants responded as “47, 44, 41….” When they heard “go,” they stood up from the chair, walked 3 meters at a comfortable speed, turned 180° toward the non-paretic side, walked 3 meters back to the chair, and sat down. This was repeated for 3 times. After a 5-minute break, participants repeated the same procedure but turned toward the paretic side for 3 trials. During the test, participants had to count continuously; if they did not, it would be considered as a failed trial and be repeated. On average, 30% of trials were repeated. Outcome and statistical analysis
From the recorded video, we obtained our primary outcomes, which were time and number of steps taken to complete the TUG test. We averaged 3 trials for each condition. We further divided the TUG test into turning and straight walking phases to gain information about whether attentional loading had a differential effect on each phase. The turning phase started at the time when the foot first contacted the turning area after walking for 3 meters (Figure 1) and ended when the foot left the turning area.3 The straight walking phase consisted of the 3-meter walk toward to the turning area and 3-meter walk back to the chair. The data were analyzed using the IBM SPSS statistical software version 19 (IBM, Armonk, NY). Descriptive statistics and tests for normality were carried out for all outcome variables. Repeated measures analysis of variance (ANOVA) was used to analyze gait parameters across 3 attentional loading conditions (single-, dual-motor, and dualcognitive task conditions) and 2 turning directions (nonparetic and paretic). A post hoc Bonferroni comparison was performed when the repeated measure ANOVA test revealed a significant difference (P < .05). Results
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body weight was 66.1 ± 4.5 kg (range, 58-74 kg), and body height was 1.7 ± 0.1 m (range, 1.61.7 m). Twelve participants presented with left hemiparesis and 8 with right hemiparesis. The average score on the MMSE was 24 ± 1.2, the average score on the FMA was 23.9 ± 1.2 (motor) and 11.0 ± .3 (sensory), and the average rating on the BBS was 45.0 ± 6.7. TUG test
Figure 2A shows the time taken to complete the TUG test under 3 attentional loading conditions and 2 turning directions. Attentional loading had a significant influence on the time taken to complete the TUG test. This is confirmed by a significant condition effect, F(2, 38) = 8.14, P < .01. Post hoc pairwise comparisons with adjusted P value of .02 indicated that the dual-motor (P = .00) and dual-cognitive (P = .00) conditions led to a longer time taken compared to the single-task condition. However, there was no difference between dualmotor and dual-cognitive task conditions (P = 1.0). There was no significant difference between turning toward the nonparetic and paretic sides, F(1, 19) = 3.16, P = .09. In addition, there was no significant interaction between task conditions and turning directions, F(2, 38) = .68, P = .51. Number of steps taken to complete the TUG test was also affected by the attentional loading, which was confirmed by a significant condition effect, F(2, 38) = 8.36, P < .01 (Figure 2B). Post hoc pairwise comparisons showed that the dual-motor (P = .00) and dual-cognitive (P = .00) conditions resulted in significantly greater number of steps than the single-task condition. However, there was no difference between the dual-motor and dualcognitive task conditions (P = 1.0). There was no significant difference in the number of steps taken between the turning toward the nonparetic and paretic sides, F(1, 19) = .12, P = .74. In addition, there was no interaction between task conditions and turning directions, F(2, 38) = .65, P = .53.
Participants
Turning phase of TUG
The mean age of the participants was 60.5 ± 10.6 years (range, 45-80). The average time post stroke was 9.7 ± 3.5 months (range, 6-18 months),
Attentional loading had a significant influence on time taken to complete the 180° turning. This is confirmed by a significant condition effect,
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task condition (P = .01). However, there was no difference between the dual-cognitive and single-task conditions (P = .05). In addition, there was no difference between the dual-motor and
F(2, 38) = 4.7, P = .02 (Figure 2C). Post hoc pairwise comparisons with an adjusted P value of .02 indicated that the dual-motor condition led to a longer time taken compared to the singleA
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Figure 2. Comparison of gait parameters across three attentional loading conditions: (A) time taken to complete Timed Up and Go (TUG) test; (B) number of steps to complete TUG; (C) time taken to complete turning 180°; (D) number of steps to complete turning 180°; (E) time taken to complete straight walking; (F) number of steps to complete straight walking phase.
Gait Parameters and TUG in Stroke Survivors
dual-cognitive task conditions (P = 1.0). There was no significant difference between turning toward the nonparetic and paretic sides, F(1, 19) = .07, P = .79. In addition, there was no significant interaction between task conditions and turning directions, F(2, 38) = .83, P = .45. Number of steps taken to complete the 180° turning was also affected by the attentional loading, which was confirmed by a significant condition effect, F(2, 38) = 3.9, P = .03 (Figure 2D). However, post hoc pairwise comparisons failed to detect any significant difference in number of steps among any pairs (dual motor vs single, P = .05; dual cognitive vs single, P = .84; dual motor vs dual cognitive, P =.32). There was no significant difference between turning toward the nonparetic and paretic sides, F(1, 19) = .07, P = .26. In addition, there was no interaction between task conditions and turning directions, F(2, 38) = .83, P = .64. Straight walking phases
Attentional loading had a significant influence on time taken to complete the straight walking phase of the TUG test. This is confirmed by a significant condition effect, F(2, 38) = 7.98, P 1.0). There was no significant difference in the time taken between turning toward the nonparetic and paretic sides, F(1, 19) = 2.81, P = .11. In addition, there was no significant interaction between task conditions and turning directions, F(2, 38) = .76, P = .48. Attentional loading also had a significant influence on number of steps taken to complete the straight walking. This is confirmed by a significant condition effect, F(2, 38) = 8.42, P < .01 (Figure 2F). Post hoc pairwise comparisons indicated that both the dual-motor (P =.00) and dual-cognitive (P =.00) conditions led to a greater number of steps taken compared to the single-task condition. However, there was no difference between the dual-motor and dual-cognitive task conditions (P = 1.0). There was no significant difference between
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turning toward the nonparetic and paretic sides, F(1, 19) = .003, P = .96. In addition, there was no significant interaction between task conditions and turning directions, F(2, 38) = .58, P = .57. Discussion Deterioration of gait performance during attentional loading in stroke survivors has been reported previously.11,12,14,26 Little is known about the effects of the attentional loading during turning in stroke survivors. This study focused on the divided attention 27 in which stroke survivors performed turning while walking (TUG test) and carried out a secondary task simultaneously (holding a cup or counting backward). We presented a few important findings. First, attentional loading adversely affected gait performance in stroke. Second, the loading types and turning directions did not lead to differential effects in TUG performance. Last, attentional loading effects on gait performance during straight walking and turning were not similar. Attentional loading conditions
We found that stroke survivors experienced a marked deterioration in their gait performance (time taken and number of steps) when they were required to perform 2 tasks simultaneously. This is possibly due to a combination of various factors including deficits in executive function, impaired divided attention, and gait impairments.9 Dual-task interference in motor performance has been explained by several neuropsychological theories including the capacity-sharing theory, bottleneck model, and multiple resource model.10 Our data are best explained by the capacitysharing theory. The capacity-sharing theory assumes that attentional resources are fixed in capacity and task performance depends on the amount of resources that are allocated to the task.9 Superior performance is expected when most of the resources are allocated to the task as in a single-task condition. Under a dual-task condition, deterioration of task performance will be observed as attentional resources that are allocated to both tasks are reduced. The deterioration of performance will be
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observed in either one or both tasks, depending on task prioritization strategy. In this study, both the TUG test and secondary task (motor or cognitive) may tax the limited attention resource. Participants were given the instruction to prioritize the performance of the secondary task (holding the glass or counting backwards); therefore, the walking and turning task (TUG) was compromised to optimize performance on the secondary task. As a result, stroke survivors demonstrated deterioration in gait performance when they were required to perform 2 tasks simultaneously. Another interesting observation in this study was the similar effects of attentional loading between dual-motor and dual-cognitive task conditions. Initially, the dual-cognitive task condition was speculated to be more challenging than the dual-motor task condition, and we expected to observe greater deterioration in gait under the dual-cognitive task condition than the dual-motor condition. One possible explanation for this finding may be related to the strategy chosen by the participants. In this study, stroke survivors were given the instruction to prioritize the secondary task. However, when inspecting the video, we found that stroke survivors took a longer time to perform backward counting continuously and some of the answers were not accurate. This unexpected finding could be a result of compensatory strategies such as sacrificing dual-cognitive task performance (reaction time, accuracy) for stability.
In the present study, we hypothesized that stroke survivors would demonstrate gait performance decrement and turning difficulties when turning toward the paretic side compared to nonparetic side, because stroke survivors often show difficulty when weight-shifting toward the paretic side. In this study, we found no difference in gait performance between turning directions. The findings are consistent with a previous study in which no significant difference in turning toward the paretic or nonparetic sides was found.28 This is probably due to the training effect on each turning directions; stroke survivors may adopt the stepping strategy to navigate the turn toward the paretic side.
Straight walking vs turning phases
Study limitations
We found that straight walking was influenced by both types of attentional loading. However, only the dual-motor task condition increased the time taken to complete the turning phase. The difference in response to attentional loading between straight walking and turning suggests that straight walking and turning may involve different motor control mechanisms and should be examined separately. During the straight walking phase, participants first accelerated and then decelerated when they approached the target (turning area or chair). Therefore, speed control may be the priority. In contrast, during the turning phase, the reorientation of body segments to the
There are several limitations of this study. First, we did not control the trade-off between the walking task and the counting backward task. Some of the participants showed little change in the gait performance, but their cognitive task performance was compromised, as demonstrated by slower responses. Second, we did not randomize the order for each condition and turning direction, which may have caused a training effect and resulted in no difference between conditions and turning directions. In addition, some of the participants were asked to repeat failed trials with an average of 2 to 3 trials for each dual-task condition. Repeating trials may
new direction in a coordinated manner may be critical. Hence, it is not surprising to observe such differences when different attentional loading was imposed. During the dual-motor condition, the longer time taken to turn was not accompanied by an increased number of steps. This may be related to the stepping strategy used during the TUG test. During 180° turning, participants slowed down their gait speed and paused between steps. The pauses between steps may explain why the time taken to complete turning increased under the dual-motor task whereas the number of steps remained the same. Turning direction
Gait Parameters and TUG in Stroke Survivors
enhance the training effects. Third, this study only included stroke survivors but not age-matched controls. Thus, it is inconclusive whether the gait deterioration under the dual-task condition was a result of stroke or aging. It is recommended that future studies compare stroke survivors to healthy age- and gender-matched controls. In addition, the procedure was conducted in a controlled environment (lab) that was quiet and with a level walking surface that might not be representative of a regular environment encountered by the participants on a daily basis. Conclusions
Turning difficulty is a common activity limitation in stroke survivors. The current study revealed that stroke survivors required a longer time and a greater number of steps to perform
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a turn under a dual-task condition. Thus, it is recommended that dual-task turning may be incorporated in gait assessment to provide information in addition to straight walking, ascending and descending stairs, and overcoming barriers (eg, slopes, curbs). Acknowledgments Financial support/disclosures: This study was supported by Research Management Institute (RMI) via Research Intensive Faculty (RIF) grants, Universiti Teknologi MARA (UiTM) Malaysia [600-RMI/DANA 5/3/RIF (247/2012)]. Conflicts of interest: The authors declare no potential conflicts of interest with respect to the authorship and/or publication of this article.
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