The effects of a short-term memory task on postural control of stroke patients Hajar Mehdizadeh1, Ghorban Taghizadeh1,2, Hamed Ghomashchi3, Mohammad Parnianpour4, Kinda Khalaf5, Reza Salehi6, Ali Esteki7, Ismaeil Ebrahimi8, Bahram Sangelaji9 1
Department of Neurosciences, School of Advanced Technologies in Medicine, Tehran University of Medical Sciences, Tehran, Iran, 2Occupational Therapy Department, Faculty of Rehabilitation Sciences, Iran University of Medical Sciences, Tehran, Iran, 3Faculty of Mechanical and Industrial Engineering, Islamic Azad University, Qazvin Branch, Iran, 4Department of Mechanical Engineering, Sharif University of Technology, Tehran, Iran, 5 Department of Biomedical Engineering, Khalifa University of Science, Technology and Research, Abu Dhabi, United Arab Emirates, 6School of Rehabilitation Sciences, Ahvaz Jundishapur University of Medical Sciences, Iran, 7Shahid Beheshti University of Medical Science, Tehran, Iran, 8Faculty of Rehabilitation Sciences, Iran University of Medical Science, Tehran, Iran, 9Hayateno Rehabilitation Center (Iranian MS Society), Tehran, Iran Background: Many studies have been conducted on the changes in the balance capabilities of stroke patients. However, results regarding the effects of dual-task activities on postural control in these patients have been variable. Objective: To evaluate the effects of a short-term memory task on the sway characteristics of stroke patients. Method: Center of pressure (COP) fluctuations were measured in three levels of postural difficulty (rigid surface with closed and open eyes and foam surface with closed eyes), as well as two levels of cognitive difficulty (easy and difficult). COP parameters included mean velocity, standard deviation of velocity in both medial–lateral (M.L) and anterior–posterior (A.P) directions, total phase plane portrait, area. Nineteen stroke patients and 19 gender, age, height, and weight matching healthy volunteers participated in this study. Results: Our findings indicate that mean velocity (F514.21, P50.001), standard deviation of velocity in both M.L (F517.50, P50.000) and A.P (F511.03, P50.002) directions, total phase plane portrait (F544.12, P50.001), and area (F513.95, P50.01) of center of pressure of patients were statistically greater than normal subjects, while significant interaction of group|postural difficulty and postural|cognitive difficulty were observed for all parameters of postural sway. Conclusions: Different measures of postural sway showed complex response to postural and cognitive difficulties between stroke patients and normals. Cognitive error was not affected by the main effects of group and postural difficulty, while greatly increased at more difficult cognitive task (F575.73, P50.000). Keywords: Postural control, Dual-task, Stroke
Introduction Stroke causes a combination of sensory, motor, cognitive, and emotional impairments that limit the ability of performing basic activities of daily living and negatively impact participation in society.1 Balance impairment is a very common cause of disability in patients with stroke.2 In this population, balance can be affected in various ways including joint motion limitation, *Correspondence to: G. Taghizadeh, Department of Occupational Therapy, Faculty of Rehabilitation Sciences, Iran University of Medical Sciences, Shahnazari Street, Mirdamad Boulevard, Tehran, Iran; Department of Neurosciences, School of Advanced Technologies in Medicine, Tehran University of Medical Sciences, Tehran, Iran. Email: [email protected] ß W. S. Maney & Son Ltd 2015 DOI 10.1179/1074935714Z.0000000039
weakness, altered muscular tone, sensory deficits, abnormal postural reactions, and cognitive problems.3,4 Stroke survivors are at high risk for falls, which may be due to impaired standing balance compared with age-matched controls.5 Four-fold increased risk of hip fracture on the affected side, decreased independence in activities of daily living, and even death are serious fall-related consequences in stroke patients.6 Impairments of the mechanisms responsible for postural control can lead to unsteadiness and instability during upright standing.7 Postural control of upright standing requires complex and delicate sensorimotor coordination. It has been suggested that not only subcortical Topics in Stroke Rehabilitation
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structures contribute to postural control of upright standing through automated and reflective actions, but research shows that cerebral cortices also contribute to this function.8 In other words, it is well established that postural control has significant attentional (cognitive) requirements depending on the postural task as well as age and balance ability.9 The extent to which postural control and cognitive processes impact each other is typically investigated in ‘‘dual-task paradigms,’’ in which subjects perform cognitive and postural task simultaneously.10 Performance decrement in either task indicates interference between the two tasks and thus, implies shared attention resources for both tasks.11 Indeed, in individuals who perform different postural tasks (static or dynamic) simultaneously with cognitive tasks (e.g. conversing or listening to music while walking), the attentional resources should be divided to perform both tasks properly. Thus, the question arises as to whether dual-task conditions affect postural control function in stroke patients. Postural control assessment of stroke patients has evolved in the last few years. Brown et al. reported increased attentional demands for tasks of static postural control in stroke patients compared with healthy control subjects.12 In this study, only reaction time (as a secondary cognitive task) was reported and balance performance was not been compared between the groups during various task conditions. de Haart et al. found no consistent evidence of increased postural instability in stroke patients during dual tasks.13 Bensoussan et al. reported decreased postural performance of stroke patients during both dual tasks and eye-closed tasks.14 In these studies, participants should respond verbally to a visual stimulus, indicate verbally the correctness of each digit summation, and count backward loudly, respectively. However, it has been shown that vocal articulation inadvertently results in changes in postural sway that are not related to the concurrent cognitive task.15,16 Moreover, different levels of both postural and cognitive difficulty have not been considered in any of the aforementioned studies. Hence, the goal of this study is to investigate the effects of postural and cognitive difficulty on the performance of normal and stroke patients during quiet standing.
Methods Participants Nineteen patients (10 women, 9 men, 8 with left hemisphere lesion, 11 with right hemisphere lesion) with stroke were recruited in this study. Their mean age was 51.5+ 12.2 years (range: 26–75 years); the mean height was 165.5+ 10.1 cm; the mean weight was 69.2+ 14.4 kg and the mean post stroke time was 2
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33.33+ 20.26 months. None of patients had a significant cognitive impairment (Mini-Mental State Examination: i23), dizziness, hemi-neglect, aphasia, diabetes, visual impairments not corrected by glasses, other neurological disorders, or pain in the trunk and lower limbs during the test. Nineteen healthy subjects with negative history of neurological deficit upon examination participated as healthy controls; they were matched for sex (10 women, 9 men), age (mean: 51.6+ 11.5 years; range: 27–73 years), height (mean: 165.6+ 9.9 cm), and weight (mean, 69.2+ 14.5 kg). All participants signed a written informed consent approved by the Ethics Committee at Iran University of Medical Sciences.
Procedure Subjects, arms relaxed at their side, stood barefoot in a bipedal stance position on a force platform, with their feet placed slightly apart. A strain gauge Bertec 4060-10 force platform (Bertec Corporation, Columbus, OH, USA) and a Bertec AM-6701 amplifier (Bertec Corporation) were used in this study. Center of pressure (COP) trajectory data were collected at a sampling frequency of 100 Hz. The subjects were asked to remain as stable as possible and not to speak or move their limbs and head during data collection. Three levels of postural difficulty [standing on a rigid surface of the force platform with open and closed eyes (RO and RC), and standing on a 10.5 cm tick foam with closed eyes (FC)] (Fig. 1), and two levels of cognitive difficulty (easy and difficult) were randomly combined to create conditions that varied in difficulty. In RC and FC conditions, participants wore a blindfold to close eyes. Subjects were asked to listen carefully to a string of random numbers before the postural data collection commenced and mentally repeat it in reverse order during data collection. At the end of each dual task, trial participants were asked to verbally report the numbers they memorized. The difficulty level of cognitive task was manipulated according to the ‘working memory capacity’ of an individual which was determined using the digits backward test of Wechsler Intelligence Scale.17 The number of digits displayed in a difficult cognitive task was the maximum number of digits correctly recalled plus 1. The easy cognitive task displayed half of the number of the difficult task, rounded up in case the maximum number of digits recalled was odd. The digit string was repeated twice at a constant volume and rate before the postural data collection. Subjects were asked and encouraged to perform the cognitive task at their best ability. During each experimental condition, the subjects performed a block of three 35-second trials separated by a
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Figure 1 The above figures illustrate the forceplate, foam, and blindfold used in the study. (A) RO condition: standing on rigid surface with open eyes; (B) RC condition: standing on rigid surface with closed eyes, and (C) FC condition: standing on foam surface with closed eyes.
30-second rest period. Five-minute rest intervals were used between experimental conditions. The order of experimental conditions was randomized for each subject.
Data analysis The interference in postural control in dual- versus single-task conditions was assessed by comparing the mean total velocity, the standard deviation (SD) of velocity along anterior–posterior (A.P) and medial– lateral (M.L) directions, the total phase plane portrait (square root of the sum of variances of velocity and of displacement),18 and the area (surface contained within the closed curve including all recorded COPs), ensuring evaluation of both the static and dynamic aspects of postural control behavior. These parameters have high reliability.19 Performance on the cognitive tasks was assessed by recording the number of cognitive errors. Three cognitive error types were recorded: a wrong number, order error, and omission.20 The subjects’ mean of three trials in each condition was used for analysis.
Statistical analysis The Kolmogorov–Smirnov test was used to study the normal distribution of the data. All of postural sway parameters were normally distributed, while cognitive errors did not have normal distribution. Therefore, a logarithmic transformation was used for cognitive errors. An average value for each dependent measure
was calculated over three trials of the same condition. The effects of cognitive difficulty and postural difficulty on the COP measures in both stroke and healthy groups (main effects and interaction of these effects) were analyzed using a 2|3|3 (group|cognitive difficulty|postural difficulty) mixed model analysis of variance (ANOVA). The Bonferroni adjustment method was used for multiple comparisons.21 The effects of cognitive difficulty and postural difficulty on the transformed cognitive errors were analyzed by using a 2|2|3 (group|cognitive difficulty|postural difficulty) mixed model ANOVA with alpha level set at 0.05.
Results Postural performance of COP parameters Table 1 shows the descriptive data for all the measures of postural performance. Table 2 represents a summary of ANOVA results for all the measures of postural performance. The main effects of group, postural difficulty, and cognitive difficulty were significant for all variables. Interactions of group by postural difficulty and postural by cognitive difficulty were significant for all variables. Interactions of group by cognitive difficulty, and group by postural by cognitive difficulty were not significant for any of the variables. Also, Fig. 2 shows two-way interaction effects of postural by cognitive difficulty and group by postural difficulty, respectively, on mean velocity. Topics in Stroke Rehabilitation
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Table 1 Descriptive data for COP measures in different conditions of postural and cognitive difficulty Cognitive task
No cognitive
Groups
Healthy
Stroke
Easy Healthy
Difficult Stroke
Healthy
Stroke
Standing on rigid surface with open eyes 1.29+ 0.12 1.48+ 0.24 1.3+ 0.11 1.54+ 0.38 Mean velocity (cm/s) 1.31+ 0.11 1.54+ 0.27 0.89+ 0.81 1.07+ 0.22 0.87+ 0.08 1.02+ 0.18 0.88+ 0.09 1.16+ 0.57 SD of velocity (M.La) (cm/s) 1.23+ 0.11 1.42+ 0.22 1.22+ 0.12 1.39+ 0.23 1.23+ 0.10 1.48+ 0.57 SD of velocity (A.Pb) (cm/s) 1.57+ 0.11 1.81+ 0.31 1.59+ 0.11 1.97+ 0.81 Total phase plane portrait (arbitrary unit) 1.59+ 0.12 1.90+ 0.34 1.34+ 0.77 3.28+ 2.71 1.35+ 0.90 2.62+ 1.85 1.12+ 0.72 2.86+ 3.12 Area (cm2) Standing on rigid surface with closed eyes 1.41+ 0.14 1.69+ 0.45 1.38+ 0.13 1.68+ 0.53 Mean velocity (cm/s) 1.44+ 0.13 1.73+ 0.45 0.90+ 0.09 1.02+ 0.18 0.89+ 0.09 1.18+ 0.48 SD of velocity (M.L) (cm/s) 0.93+ 0.10 1.16+ 0.36 1.36+ 0.16 1.63+ 0.47 1.34+ 0.15 1.57+ 0.46 SD of velocity (A.P) (cm/s) 1.39+ 0.15 1.67+ 0.49 1.71+ 0.18 2.09+ 0.60 1.68+ 0.16 2.07+ 0.68 Total phase plane portrait (arbitrary unit) 1.75+ 0.16 2.15+ 0.63 1.80+ 1.15 3.93+ 3.27 1.64+ 1.28 3.91+ 2.87 1.45+ 0.80 3.40+ 3.31 Area (cm2) Standing on foam surface with closed eyes 2.88+ 0.57 3.70+ 1.12 2.70+ 0.53 3.65+ 1.19 Mean velocity (cm/s) 3.09+ 0.84 4.24+ 1.30 2.09+ 0.48 2.85+ 0.88 1.94+ 0.46 2.76+ 0.89 SD of velocity (M.L) (cm/s) 2.27+ 0.70 3.27+ 1.02 2.62+ 0.49 3.24+ 1 2.47+ 0.45 3.24+ 1.07 SD of velocity (A.P) (cm/s) 2.78+ 0.79 3.80+ 1.24 3.60+ 0.66 4.60+ 1.35 3.33+ 0.64 4.52+ 1.44 Total phase plane portrait (arbitrary unit) 3.86+ 1.02 5.34+ 1.65 16.79+ 6.33 31.36+ 17.31 15.14+ 5.76 22.41+ 12.12 10.50+ 4.90 21.34+ 16.48 Area (cm2) Note: a M.L: medial–lateral. b A.P: anterior–posterior.
Mean velocity of COP increased at RC (closing eyes while standing on rigid surface) during all three cognitive difficulty conditions; and standing on foam with closed eyes (FC) further increased the mean velocity especially while performing difficult cognitive task (Fig. 2A). Only during FC, the performance of easy and difficult cognitive tasks significantly decreased the mean velocity. The mean velocity of COP was higher for stroke patients that the FC condition magnified the difference between two groups performance (Fig. 2B).
Cognitive performance Table 3 shows the descriptive data for the cognitive error, while Table 4 shows the summary of results for the cognitive error. As depicted in these tables, the main effect of group and postural difficulty were not significant, but the effect of cognitive difficulty was significant (F575.73, P50.000). No interaction effect was significant. The cognitive errors significantly increased when cognitive difficulty became more difficult.
Discussion The results showed that postural sway was greater in stroke patients as compared with that of healthy subjects across different postural difficulty levels. There are many potential explanations for these results. The loss of peripheral sensory input in stroke patients and incorrect sensory–motor integration may lead to the production of inappropriate synergies that are not as effective in maintaining postural balance, especially when the subject is asked to perform difficult cognitive tasks simultaneously. Challenges in terms of postural difficulty (FC) further increase due to group 4
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differences. Therefore, from a clinical/rehabilitation perspective, standing on foam with closed eyes is a challenging condition for stroke patients that can be important in rehabilitation. For example, the ‘‘TaskOriented Approach’’ emphasizes on challenging the learning process of activities used in daily living.22 Also, quiet standing on foam with closed eyes can be used as one of the activities for retraining of sensory strategy that should be used for postural control in stroke patients. Moreover, dual-task paradigm potentially enhances the scope of both assessment tests and rehabilitation protocols by simultaneously monitoring postural control and performance of cognitive activities.23
Postural performance
As expected, the results showed that the postural instability of stroke patients was greater than healthy subjects in during various postural tasks (Fig. 2B). This finding indicates that postural control dependency on visual and somatosensory information in stroke patients is higher than normal subjects. In comparison with healthy subjects, stroke patients show decreased between-limb synchronization, which is reflected in increased total postural sway of stroke patients. According to Marigold and Eng, weight bearing asymmetry may result in greater postural sway in stroke patients.24 In addition, impaired ankle proprioception may lead to increased sway in these patients.25 Furthermore, increased perceived threat to postural stability may cause greater sway.24 These results are in accordance with Mansfield et al., Bensoussan et al., and Nardone et al.5,14,26 The results of this study showed that significant differences between postural sway in
0.222 0.117 0.452 0.196 0.012 0.112 0.000 0.115 4.98 2.32 6.8 2.01 0.194 0.068 0.402 0.068 0.023 0.28 0.002 0.66 4.42 1.28 5.54 0.6 0.163 0.068 0.304 0.072 0.04 0.29 0.01 0.63 3.41 1.28 3.60 0.63 0.213 0.45 0.421 0.057 0.01 0.44 0.001 0.74
Cognitive performance Note: a M.L: medial–lateral. b A.P: anterior–posterior.
0.188 0.005 0.309 0.058 0.026 0.37 0.01 0.73 4.04 1.02 3.68 0.50
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standing on foam with closed eyes and standing on a rigid surface with both open and closed eyes exist in all parameters between stroke and healthy subjects. On the other hand, postural sway differences were not significant in some parameters in comparing standing on rigid surface with closed eyes and open eyes within groups. Therefore, it can be suggested that visual deprivation alone does not affect postural sway significantly, while visual deprivation accompanied with incorrect somatosensory inputs induces significant differences in postural sway. Our results indicate that postural sway decreased with increasing difficulty level of cognitive tasks. In this study, subjects could not behave adaptively and they prioritized their postural control by freezing their posture and this choice resulted in decreased postural sway, while their cognitive errors increased at higher level of cognitive difficulty. According to the ‘‘limited capacity of attention theory,’’ when someone is doing two tasks simultaneously and if the two tasks are beyond his/her total capacity, the quality of performance of each of these tasks or both may be compromised.27 It is noteworthy that this result is inconsistent with Bensoussan et al. and de Haart et al.13,14 In these studies, participants had to verbally indicate the correctness of each digit summation and count backward loudly, respectively. Dault et al. and Yardely et al. showed that vocal articulation, with its associated facial movements and changes in breathing patterns, may inadvertently increase postural sway.15,16 The present results and those of Riley et al. and Anderson et al., which used the same cognitive tasks, indicate that increasing the difficulty level of a cognitive task is accompanied with enhanced postural stability (i.e. reduced postural sway) in quiet standing.20,28
4.72 0.82 5.99 0.49
0.279 0.808 0.462 0.01 0.000 0.000 13.95 73.47 15.04 0.282 0.879 0.363 0.001 0.000 0.000 44.12 127.41 9.95 0.235 0.861 0.281 0.002 0.000 0.003 11.03 108.70 6.83 0.327 0.862 0.309 0.000 0.000 0.02 17.50 109.21 7.81 0.283 0.865 0.338 0.001 0.000 0.001 14.21 112.33 8.93
Main effect Group Postural difficulty Cognitive difficulty Interaction Group|postural difficulty Group|cognitive difficulty Postural|cognitive difficulty Group|postural|cognitive difficulty
Effect size P Effect size P F ratio Effect size Independent variable
F ratio
P
Effect size
P
Effect size
P F ratio F ratio
Total phase plane portrait (arbitrary unit) SD of velocity (A.Pb) (cm/s) SD of velocity (M.La) (cm/s) Mean velocity (cm/s)
Table 2 Summary of analysis of variance for measures of postural performance: F ratios, P values, and effect sizes by variable
F ratio
Area (cm2)
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The results revealed that by increasing the difficulty level of cognitive task, the cognitive error increased. One explanation for this finding may be the limitation of the information processing capacity of the brain. Also, subjects may allocate less amount of their capacity to the cognitive task by prioritizing their postural control, therefore causing higher cognitive error associated with the increasing level of difficulty of particular cognitive task. According to traditional perspectives, more variability indicates a less stable and less healthy postural control system,29 but new perspectives which originated from dynamical system theory imply that a degree of variability or ‘‘optimal’’ amount of variability is in fact needed for maintaining functional skills Topics in Stroke Rehabilitation
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Mean velocity (cm/s)
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Mean velocity (cm/s)
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Figure 2 (A) The interaction plot of postural difficulty by cognitive difficulty of mean velocity of COP. The results of all multiple comparisons of means in three conditions (RO: standing on rigid surface with open eyes; RC: standing on rigid surface with closed eyes; FC: standing on foam surface with closed eyes) were significant (P< 0.05) which are shown by star. (B) The significant interaction of groups and postural difficulty levels (RO, RC, and FC) on mean velocity of COP. The results of all multiple comparisons of means in three conditions (RO: standing on rigid surface with open eyes; RC: standing on rigid surface with closed eyes; FC: standing on foam surface with closed eyes) between normal and stroke patients were significant which are shown by star.
like balance. On the other hand, excessive variability has been associated with instabilities in the behavior of neuromuscular system. Such instabilities may suggest a lack of control of the multiple degrees of freedom characteristic of that system and may indicate disorder in its organization.30 While the results of this study are in contrast with the traditional perspectives, they are consistent with the dynamical system theory and the ‘‘limited capacity of attention’’ since decreasing postural sway in dual tasking is considered as an indicator of decreasing flexibility or adaptability
and increasing rigidity of postural control system. This is also in alignment with Riley et al.20 Therefore, for more accurate investigation of flexibility and adaptability of postural control system, our future work includes studying the nonlinear parameters of COP.
Conclusion This study suggests that the dual tasking did not change the balancing of stroke patients any differently from healthy subjects. Postural difficulty increased the balance performance of both healthy and stroke
Table 3 Mean+ SD of cognitive errorsa in different conditions of postural and cognitive difficulty for stroke and normal subjects Levels of cognitive difficulty Easy Levels of postural difficulty Rigid surface — eyes open Rigid surface — eyes closed Foam surface — eyes closed
Difficult
Stroke
Normal
Stroke
0.00+ 0.00 0.00+ 0.00 0.25+ 0.11
0.00+ 0.00 0.25+ 0.11 0.00+ 0.00
0.21+ 0.22 0.22+ 0.23 0.24+ 0.22
Normal 0.13+ 0.17 0.19+ 0.21 0.15+ 0.19
Note: a Cognitive error was computed as the mean of three types of error: a wrong number, order error, and omission.
Table 4 Summary of analysis of variance for measures of cognitive errorsa: F ratios, P values, and effect sizes by variable Main effect
Independent variable Cognitive error F ratio P Effect size
Interaction
Group
Postural difficulty
Cognitive difficulty
Group| postural difficulty
Group| cognitive difficulty
Postural| cognitive difficulty
Group|postural| cognitive difficulty
2.464 0.125 0.064
0.534 0.591 0.03
75.735 0.000 0.678
0.68 0.513 0.037
2.453 0.126 0.064
0.108 0.898 0.006
0.061 0.941 0.003
Note: a Cognitive error was computed as the mean of three types of error: a wrong number, order error, and omission.
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populations. However, dual tasking affected both groups in similar manner. During the highest postural difficulty condition (FC), increasing the cognitive difficulty reduced postural sway measures. In future studies and for rehabilitation purposes, quiet standing on foam with closed eyes with or without cognitive tasks is recommended for stroke patients. Further research is required for more detailed investigation of dual tasking in stroke patients while considering the location of injury, different types of dual task (alternative cognitive and/or postural task), as well as nonlinear analysis of postural fluctuations.
Acknowledgements This work was supported by Iran University of Medical Sciences, Tehran, Iran. The authors wish thank all participants included in this study.
Contributors G Taghizadeh, H Mehdizadeh and M Parnianpour developed the idea and prepared the draft of this paper. All authors were involved in design and the protocol of the study. All authors reviewed the manuscript and approved the final version.
Funding This work recieved a grant from Research Program, Iran University of Medical Sciences, Tehran, Iran.
Conflicts of Interest The authors declare that there is no conflict of interest.
Ethics Approval Approved by the Ethics Committee University of Medical Sciences.
at
Iran
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Department of Neurosciences, School of Advanced Technologies in Medicine, Tehran University of Medical Sciences, Tehran, Iran, 2Occupational Therapy Department, Faculty of Rehabilitation Sciences, Iran University of Medical Sciences, Tehran, Iran, 3Faculty of Mechanical and Industrial Engineering, Islamic Azad University, Qazvin Branch, Iran, 4Department of Mechanical Engineering, Sharif University of Technology, Tehran, Iran, 5 Department of Biomedical Engineering, Khalifa University of Science, Technology and Research, Abu Dhabi, United Arab Emirates, 6School of Rehabilitation Sciences, Ahvaz Jundishapur University of Medical Sciences, Iran, 7Shahid Beheshti University of Medical Science, Tehran, Iran, 8Faculty of Rehabilitation Sciences, Iran University of Medical Science, Tehran, Iran, 9Hayateno Rehabilitation Center (Iranian MS Society), Tehran, Iran Background: Many studies have been conducted on the changes in the balance capabilities of stroke patients. However, results regarding the effects of dual-task activities on postural control in these patients have been variable. Objective: To evaluate the effects of a short-term memory task on the sway characteristics of stroke patients. Method: Center of pressure (COP) fluctuations were measured in three levels of postural difficulty (rigid surface with closed and open eyes and foam surface with closed eyes), as well as two levels of cognitive difficulty (easy and difficult). COP parameters included mean velocity, standard deviation of velocity in both medial–lateral (M.L) and anterior–posterior (A.P) directions, total phase plane portrait, area. Nineteen stroke patients and 19 gender, age, height, and weight matching healthy volunteers participated in this study. Results: Our findings indicate that mean velocity (F514.21, P50.001), standard deviation of velocity in both M.L (F517.50, P50.000) and A.P (F511.03, P50.002) directions, total phase plane portrait (F544.12, P50.001), and area (F513.95, P50.01) of center of pressure of patients were statistically greater than normal subjects, while significant interaction of group|postural difficulty and postural|cognitive difficulty were observed for all parameters of postural sway. Conclusions: Different measures of postural sway showed complex response to postural and cognitive difficulties between stroke patients and normals. Cognitive error was not affected by the main effects of group and postural difficulty, while greatly increased at more difficult cognitive task (F575.73, P50.000). Keywords: Postural control, Dual-task, Stroke
Introduction Stroke causes a combination of sensory, motor, cognitive, and emotional impairments that limit the ability of performing basic activities of daily living and negatively impact participation in society.1 Balance impairment is a very common cause of disability in patients with stroke.2 In this population, balance can be affected in various ways including joint motion limitation, *Correspondence to: G. Taghizadeh, Department of Occupational Therapy, Faculty of Rehabilitation Sciences, Iran University of Medical Sciences, Shahnazari Street, Mirdamad Boulevard, Tehran, Iran; Department of Neurosciences, School of Advanced Technologies in Medicine, Tehran University of Medical Sciences, Tehran, Iran. Email: [email protected] ß W. S. Maney & Son Ltd 2015 DOI 10.1179/1074935714Z.0000000039
weakness, altered muscular tone, sensory deficits, abnormal postural reactions, and cognitive problems.3,4 Stroke survivors are at high risk for falls, which may be due to impaired standing balance compared with age-matched controls.5 Four-fold increased risk of hip fracture on the affected side, decreased independence in activities of daily living, and even death are serious fall-related consequences in stroke patients.6 Impairments of the mechanisms responsible for postural control can lead to unsteadiness and instability during upright standing.7 Postural control of upright standing requires complex and delicate sensorimotor coordination. It has been suggested that not only subcortical Topics in Stroke Rehabilitation
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structures contribute to postural control of upright standing through automated and reflective actions, but research shows that cerebral cortices also contribute to this function.8 In other words, it is well established that postural control has significant attentional (cognitive) requirements depending on the postural task as well as age and balance ability.9 The extent to which postural control and cognitive processes impact each other is typically investigated in ‘‘dual-task paradigms,’’ in which subjects perform cognitive and postural task simultaneously.10 Performance decrement in either task indicates interference between the two tasks and thus, implies shared attention resources for both tasks.11 Indeed, in individuals who perform different postural tasks (static or dynamic) simultaneously with cognitive tasks (e.g. conversing or listening to music while walking), the attentional resources should be divided to perform both tasks properly. Thus, the question arises as to whether dual-task conditions affect postural control function in stroke patients. Postural control assessment of stroke patients has evolved in the last few years. Brown et al. reported increased attentional demands for tasks of static postural control in stroke patients compared with healthy control subjects.12 In this study, only reaction time (as a secondary cognitive task) was reported and balance performance was not been compared between the groups during various task conditions. de Haart et al. found no consistent evidence of increased postural instability in stroke patients during dual tasks.13 Bensoussan et al. reported decreased postural performance of stroke patients during both dual tasks and eye-closed tasks.14 In these studies, participants should respond verbally to a visual stimulus, indicate verbally the correctness of each digit summation, and count backward loudly, respectively. However, it has been shown that vocal articulation inadvertently results in changes in postural sway that are not related to the concurrent cognitive task.15,16 Moreover, different levels of both postural and cognitive difficulty have not been considered in any of the aforementioned studies. Hence, the goal of this study is to investigate the effects of postural and cognitive difficulty on the performance of normal and stroke patients during quiet standing.
Methods Participants Nineteen patients (10 women, 9 men, 8 with left hemisphere lesion, 11 with right hemisphere lesion) with stroke were recruited in this study. Their mean age was 51.5+ 12.2 years (range: 26–75 years); the mean height was 165.5+ 10.1 cm; the mean weight was 69.2+ 14.4 kg and the mean post stroke time was 2
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33.33+ 20.26 months. None of patients had a significant cognitive impairment (Mini-Mental State Examination: i23), dizziness, hemi-neglect, aphasia, diabetes, visual impairments not corrected by glasses, other neurological disorders, or pain in the trunk and lower limbs during the test. Nineteen healthy subjects with negative history of neurological deficit upon examination participated as healthy controls; they were matched for sex (10 women, 9 men), age (mean: 51.6+ 11.5 years; range: 27–73 years), height (mean: 165.6+ 9.9 cm), and weight (mean, 69.2+ 14.5 kg). All participants signed a written informed consent approved by the Ethics Committee at Iran University of Medical Sciences.
Procedure Subjects, arms relaxed at their side, stood barefoot in a bipedal stance position on a force platform, with their feet placed slightly apart. A strain gauge Bertec 4060-10 force platform (Bertec Corporation, Columbus, OH, USA) and a Bertec AM-6701 amplifier (Bertec Corporation) were used in this study. Center of pressure (COP) trajectory data were collected at a sampling frequency of 100 Hz. The subjects were asked to remain as stable as possible and not to speak or move their limbs and head during data collection. Three levels of postural difficulty [standing on a rigid surface of the force platform with open and closed eyes (RO and RC), and standing on a 10.5 cm tick foam with closed eyes (FC)] (Fig. 1), and two levels of cognitive difficulty (easy and difficult) were randomly combined to create conditions that varied in difficulty. In RC and FC conditions, participants wore a blindfold to close eyes. Subjects were asked to listen carefully to a string of random numbers before the postural data collection commenced and mentally repeat it in reverse order during data collection. At the end of each dual task, trial participants were asked to verbally report the numbers they memorized. The difficulty level of cognitive task was manipulated according to the ‘working memory capacity’ of an individual which was determined using the digits backward test of Wechsler Intelligence Scale.17 The number of digits displayed in a difficult cognitive task was the maximum number of digits correctly recalled plus 1. The easy cognitive task displayed half of the number of the difficult task, rounded up in case the maximum number of digits recalled was odd. The digit string was repeated twice at a constant volume and rate before the postural data collection. Subjects were asked and encouraged to perform the cognitive task at their best ability. During each experimental condition, the subjects performed a block of three 35-second trials separated by a
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Figure 1 The above figures illustrate the forceplate, foam, and blindfold used in the study. (A) RO condition: standing on rigid surface with open eyes; (B) RC condition: standing on rigid surface with closed eyes, and (C) FC condition: standing on foam surface with closed eyes.
30-second rest period. Five-minute rest intervals were used between experimental conditions. The order of experimental conditions was randomized for each subject.
Data analysis The interference in postural control in dual- versus single-task conditions was assessed by comparing the mean total velocity, the standard deviation (SD) of velocity along anterior–posterior (A.P) and medial– lateral (M.L) directions, the total phase plane portrait (square root of the sum of variances of velocity and of displacement),18 and the area (surface contained within the closed curve including all recorded COPs), ensuring evaluation of both the static and dynamic aspects of postural control behavior. These parameters have high reliability.19 Performance on the cognitive tasks was assessed by recording the number of cognitive errors. Three cognitive error types were recorded: a wrong number, order error, and omission.20 The subjects’ mean of three trials in each condition was used for analysis.
Statistical analysis The Kolmogorov–Smirnov test was used to study the normal distribution of the data. All of postural sway parameters were normally distributed, while cognitive errors did not have normal distribution. Therefore, a logarithmic transformation was used for cognitive errors. An average value for each dependent measure
was calculated over three trials of the same condition. The effects of cognitive difficulty and postural difficulty on the COP measures in both stroke and healthy groups (main effects and interaction of these effects) were analyzed using a 2|3|3 (group|cognitive difficulty|postural difficulty) mixed model analysis of variance (ANOVA). The Bonferroni adjustment method was used for multiple comparisons.21 The effects of cognitive difficulty and postural difficulty on the transformed cognitive errors were analyzed by using a 2|2|3 (group|cognitive difficulty|postural difficulty) mixed model ANOVA with alpha level set at 0.05.
Results Postural performance of COP parameters Table 1 shows the descriptive data for all the measures of postural performance. Table 2 represents a summary of ANOVA results for all the measures of postural performance. The main effects of group, postural difficulty, and cognitive difficulty were significant for all variables. Interactions of group by postural difficulty and postural by cognitive difficulty were significant for all variables. Interactions of group by cognitive difficulty, and group by postural by cognitive difficulty were not significant for any of the variables. Also, Fig. 2 shows two-way interaction effects of postural by cognitive difficulty and group by postural difficulty, respectively, on mean velocity. Topics in Stroke Rehabilitation
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Table 1 Descriptive data for COP measures in different conditions of postural and cognitive difficulty Cognitive task
No cognitive
Groups
Healthy
Stroke
Easy Healthy
Difficult Stroke
Healthy
Stroke
Standing on rigid surface with open eyes 1.29+ 0.12 1.48+ 0.24 1.3+ 0.11 1.54+ 0.38 Mean velocity (cm/s) 1.31+ 0.11 1.54+ 0.27 0.89+ 0.81 1.07+ 0.22 0.87+ 0.08 1.02+ 0.18 0.88+ 0.09 1.16+ 0.57 SD of velocity (M.La) (cm/s) 1.23+ 0.11 1.42+ 0.22 1.22+ 0.12 1.39+ 0.23 1.23+ 0.10 1.48+ 0.57 SD of velocity (A.Pb) (cm/s) 1.57+ 0.11 1.81+ 0.31 1.59+ 0.11 1.97+ 0.81 Total phase plane portrait (arbitrary unit) 1.59+ 0.12 1.90+ 0.34 1.34+ 0.77 3.28+ 2.71 1.35+ 0.90 2.62+ 1.85 1.12+ 0.72 2.86+ 3.12 Area (cm2) Standing on rigid surface with closed eyes 1.41+ 0.14 1.69+ 0.45 1.38+ 0.13 1.68+ 0.53 Mean velocity (cm/s) 1.44+ 0.13 1.73+ 0.45 0.90+ 0.09 1.02+ 0.18 0.89+ 0.09 1.18+ 0.48 SD of velocity (M.L) (cm/s) 0.93+ 0.10 1.16+ 0.36 1.36+ 0.16 1.63+ 0.47 1.34+ 0.15 1.57+ 0.46 SD of velocity (A.P) (cm/s) 1.39+ 0.15 1.67+ 0.49 1.71+ 0.18 2.09+ 0.60 1.68+ 0.16 2.07+ 0.68 Total phase plane portrait (arbitrary unit) 1.75+ 0.16 2.15+ 0.63 1.80+ 1.15 3.93+ 3.27 1.64+ 1.28 3.91+ 2.87 1.45+ 0.80 3.40+ 3.31 Area (cm2) Standing on foam surface with closed eyes 2.88+ 0.57 3.70+ 1.12 2.70+ 0.53 3.65+ 1.19 Mean velocity (cm/s) 3.09+ 0.84 4.24+ 1.30 2.09+ 0.48 2.85+ 0.88 1.94+ 0.46 2.76+ 0.89 SD of velocity (M.L) (cm/s) 2.27+ 0.70 3.27+ 1.02 2.62+ 0.49 3.24+ 1 2.47+ 0.45 3.24+ 1.07 SD of velocity (A.P) (cm/s) 2.78+ 0.79 3.80+ 1.24 3.60+ 0.66 4.60+ 1.35 3.33+ 0.64 4.52+ 1.44 Total phase plane portrait (arbitrary unit) 3.86+ 1.02 5.34+ 1.65 16.79+ 6.33 31.36+ 17.31 15.14+ 5.76 22.41+ 12.12 10.50+ 4.90 21.34+ 16.48 Area (cm2) Note: a M.L: medial–lateral. b A.P: anterior–posterior.
Mean velocity of COP increased at RC (closing eyes while standing on rigid surface) during all three cognitive difficulty conditions; and standing on foam with closed eyes (FC) further increased the mean velocity especially while performing difficult cognitive task (Fig. 2A). Only during FC, the performance of easy and difficult cognitive tasks significantly decreased the mean velocity. The mean velocity of COP was higher for stroke patients that the FC condition magnified the difference between two groups performance (Fig. 2B).
Cognitive performance Table 3 shows the descriptive data for the cognitive error, while Table 4 shows the summary of results for the cognitive error. As depicted in these tables, the main effect of group and postural difficulty were not significant, but the effect of cognitive difficulty was significant (F575.73, P50.000). No interaction effect was significant. The cognitive errors significantly increased when cognitive difficulty became more difficult.
Discussion The results showed that postural sway was greater in stroke patients as compared with that of healthy subjects across different postural difficulty levels. There are many potential explanations for these results. The loss of peripheral sensory input in stroke patients and incorrect sensory–motor integration may lead to the production of inappropriate synergies that are not as effective in maintaining postural balance, especially when the subject is asked to perform difficult cognitive tasks simultaneously. Challenges in terms of postural difficulty (FC) further increase due to group 4
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differences. Therefore, from a clinical/rehabilitation perspective, standing on foam with closed eyes is a challenging condition for stroke patients that can be important in rehabilitation. For example, the ‘‘TaskOriented Approach’’ emphasizes on challenging the learning process of activities used in daily living.22 Also, quiet standing on foam with closed eyes can be used as one of the activities for retraining of sensory strategy that should be used for postural control in stroke patients. Moreover, dual-task paradigm potentially enhances the scope of both assessment tests and rehabilitation protocols by simultaneously monitoring postural control and performance of cognitive activities.23
Postural performance
As expected, the results showed that the postural instability of stroke patients was greater than healthy subjects in during various postural tasks (Fig. 2B). This finding indicates that postural control dependency on visual and somatosensory information in stroke patients is higher than normal subjects. In comparison with healthy subjects, stroke patients show decreased between-limb synchronization, which is reflected in increased total postural sway of stroke patients. According to Marigold and Eng, weight bearing asymmetry may result in greater postural sway in stroke patients.24 In addition, impaired ankle proprioception may lead to increased sway in these patients.25 Furthermore, increased perceived threat to postural stability may cause greater sway.24 These results are in accordance with Mansfield et al., Bensoussan et al., and Nardone et al.5,14,26 The results of this study showed that significant differences between postural sway in
0.222 0.117 0.452 0.196 0.012 0.112 0.000 0.115 4.98 2.32 6.8 2.01 0.194 0.068 0.402 0.068 0.023 0.28 0.002 0.66 4.42 1.28 5.54 0.6 0.163 0.068 0.304 0.072 0.04 0.29 0.01 0.63 3.41 1.28 3.60 0.63 0.213 0.45 0.421 0.057 0.01 0.44 0.001 0.74
Cognitive performance Note: a M.L: medial–lateral. b A.P: anterior–posterior.
0.188 0.005 0.309 0.058 0.026 0.37 0.01 0.73 4.04 1.02 3.68 0.50
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standing on foam with closed eyes and standing on a rigid surface with both open and closed eyes exist in all parameters between stroke and healthy subjects. On the other hand, postural sway differences were not significant in some parameters in comparing standing on rigid surface with closed eyes and open eyes within groups. Therefore, it can be suggested that visual deprivation alone does not affect postural sway significantly, while visual deprivation accompanied with incorrect somatosensory inputs induces significant differences in postural sway. Our results indicate that postural sway decreased with increasing difficulty level of cognitive tasks. In this study, subjects could not behave adaptively and they prioritized their postural control by freezing their posture and this choice resulted in decreased postural sway, while their cognitive errors increased at higher level of cognitive difficulty. According to the ‘‘limited capacity of attention theory,’’ when someone is doing two tasks simultaneously and if the two tasks are beyond his/her total capacity, the quality of performance of each of these tasks or both may be compromised.27 It is noteworthy that this result is inconsistent with Bensoussan et al. and de Haart et al.13,14 In these studies, participants had to verbally indicate the correctness of each digit summation and count backward loudly, respectively. Dault et al. and Yardely et al. showed that vocal articulation, with its associated facial movements and changes in breathing patterns, may inadvertently increase postural sway.15,16 The present results and those of Riley et al. and Anderson et al., which used the same cognitive tasks, indicate that increasing the difficulty level of a cognitive task is accompanied with enhanced postural stability (i.e. reduced postural sway) in quiet standing.20,28
4.72 0.82 5.99 0.49
0.279 0.808 0.462 0.01 0.000 0.000 13.95 73.47 15.04 0.282 0.879 0.363 0.001 0.000 0.000 44.12 127.41 9.95 0.235 0.861 0.281 0.002 0.000 0.003 11.03 108.70 6.83 0.327 0.862 0.309 0.000 0.000 0.02 17.50 109.21 7.81 0.283 0.865 0.338 0.001 0.000 0.001 14.21 112.33 8.93
Main effect Group Postural difficulty Cognitive difficulty Interaction Group|postural difficulty Group|cognitive difficulty Postural|cognitive difficulty Group|postural|cognitive difficulty
Effect size P Effect size P F ratio Effect size Independent variable
F ratio
P
Effect size
P
Effect size
P F ratio F ratio
Total phase plane portrait (arbitrary unit) SD of velocity (A.Pb) (cm/s) SD of velocity (M.La) (cm/s) Mean velocity (cm/s)
Table 2 Summary of analysis of variance for measures of postural performance: F ratios, P values, and effect sizes by variable
F ratio
Area (cm2)
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The results revealed that by increasing the difficulty level of cognitive task, the cognitive error increased. One explanation for this finding may be the limitation of the information processing capacity of the brain. Also, subjects may allocate less amount of their capacity to the cognitive task by prioritizing their postural control, therefore causing higher cognitive error associated with the increasing level of difficulty of particular cognitive task. According to traditional perspectives, more variability indicates a less stable and less healthy postural control system,29 but new perspectives which originated from dynamical system theory imply that a degree of variability or ‘‘optimal’’ amount of variability is in fact needed for maintaining functional skills Topics in Stroke Rehabilitation
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Mean velocity (cm/s)
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Mean velocity (cm/s)
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Figure 2 (A) The interaction plot of postural difficulty by cognitive difficulty of mean velocity of COP. The results of all multiple comparisons of means in three conditions (RO: standing on rigid surface with open eyes; RC: standing on rigid surface with closed eyes; FC: standing on foam surface with closed eyes) were significant (P< 0.05) which are shown by star. (B) The significant interaction of groups and postural difficulty levels (RO, RC, and FC) on mean velocity of COP. The results of all multiple comparisons of means in three conditions (RO: standing on rigid surface with open eyes; RC: standing on rigid surface with closed eyes; FC: standing on foam surface with closed eyes) between normal and stroke patients were significant which are shown by star.
like balance. On the other hand, excessive variability has been associated with instabilities in the behavior of neuromuscular system. Such instabilities may suggest a lack of control of the multiple degrees of freedom characteristic of that system and may indicate disorder in its organization.30 While the results of this study are in contrast with the traditional perspectives, they are consistent with the dynamical system theory and the ‘‘limited capacity of attention’’ since decreasing postural sway in dual tasking is considered as an indicator of decreasing flexibility or adaptability
and increasing rigidity of postural control system. This is also in alignment with Riley et al.20 Therefore, for more accurate investigation of flexibility and adaptability of postural control system, our future work includes studying the nonlinear parameters of COP.
Conclusion This study suggests that the dual tasking did not change the balancing of stroke patients any differently from healthy subjects. Postural difficulty increased the balance performance of both healthy and stroke
Table 3 Mean+ SD of cognitive errorsa in different conditions of postural and cognitive difficulty for stroke and normal subjects Levels of cognitive difficulty Easy Levels of postural difficulty Rigid surface — eyes open Rigid surface — eyes closed Foam surface — eyes closed
Difficult
Stroke
Normal
Stroke
0.00+ 0.00 0.00+ 0.00 0.25+ 0.11
0.00+ 0.00 0.25+ 0.11 0.00+ 0.00
0.21+ 0.22 0.22+ 0.23 0.24+ 0.22
Normal 0.13+ 0.17 0.19+ 0.21 0.15+ 0.19
Note: a Cognitive error was computed as the mean of three types of error: a wrong number, order error, and omission.
Table 4 Summary of analysis of variance for measures of cognitive errorsa: F ratios, P values, and effect sizes by variable Main effect
Independent variable Cognitive error F ratio P Effect size
Interaction
Group
Postural difficulty
Cognitive difficulty
Group| postural difficulty
Group| cognitive difficulty
Postural| cognitive difficulty
Group|postural| cognitive difficulty
2.464 0.125 0.064
0.534 0.591 0.03
75.735 0.000 0.678
0.68 0.513 0.037
2.453 0.126 0.064
0.108 0.898 0.006
0.061 0.941 0.003
Note: a Cognitive error was computed as the mean of three types of error: a wrong number, order error, and omission.
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populations. However, dual tasking affected both groups in similar manner. During the highest postural difficulty condition (FC), increasing the cognitive difficulty reduced postural sway measures. In future studies and for rehabilitation purposes, quiet standing on foam with closed eyes with or without cognitive tasks is recommended for stroke patients. Further research is required for more detailed investigation of dual tasking in stroke patients while considering the location of injury, different types of dual task (alternative cognitive and/or postural task), as well as nonlinear analysis of postural fluctuations.
Acknowledgements This work was supported by Iran University of Medical Sciences, Tehran, Iran. The authors wish thank all participants included in this study.
Contributors G Taghizadeh, H Mehdizadeh and M Parnianpour developed the idea and prepared the draft of this paper. All authors were involved in design and the protocol of the study. All authors reviewed the manuscript and approved the final version.
Funding This work recieved a grant from Research Program, Iran University of Medical Sciences, Tehran, Iran.
Conflicts of Interest The authors declare that there is no conflict of interest.
Ethics Approval Approved by the Ethics Committee University of Medical Sciences.
at
Iran
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