| | Changes in Postural Control in Hemiplegic Patients After Stroke Performing a Dual TaskAbstract Bensoussan L, Viton J-M, Schieppati M, Collado H, Milhe de Bovis V, Mesure S, Delarque A. Changes in postural control in hemiplegic patients after stroke performing a dual task. ObjectiveTo determine the effects of an attentional task on hemiplegic patients’ postural control performances. DesignRetrospective study. SettingDepartment of physical and rehabilitation medicine at a university hospital. ParticipantsTwenty-three hemiplegic patients and 23 healthy age- and sex-matched control subjects. InterventionsNot applicable. Main Outcome MeasuresSway area and sway path of the center of pressure were measured during 30 seconds in standing subjects and patients under 3 conditions: eyes open (EO), EO while performing a simple arithmetic task (EO-AT), and eyes closed (EC). ResultsIn the hemiplegic patients, the body sway area increased significantly with EC (P<.001) and during the EO-AT task (P<.017) in comparison with EO. Sway area with EO-AT remained, however, significantly smaller than with EC (P<.014). In the healthy subjects, the body sway did not differ significantly between the EO-AT and EO tasks (P<.42). The increase observed in the sway area and path in the hemiplegic population during the EO-AT task correlated significantly with age. ConclusionsThe postural performances of hemiplegic patients decreased during both the arithmetic task and the EC task. The cognitive task had no effect on healthy subjects’ postural performances. This study is the first to show the combined effects of age and dual task on the postural performances of hemiplegic subjects. CHRONIC STROKE PATIENTS have to deal with problems resulting from postural control alterations. Many studies have shown that changes in the postural control process occur in hemiplegic patients. Hemiplegic patients show changes in the patterns of recruitment and delayed contraction of the paretic muscle during balance disturbances.1 Weight distribution on the lower limbs is asymmetric, in favor of the sound lower limb,2, 3, 4, 5 and weight transfer from the sound to the hemiplegic limb is altered.6 Postural adjustments are also affected.7, 8, 9, 10 Sway of the center of pressure (COP), as measured by a force platform, is greater in standing hemiplegic patients than in healthy subjects.2, 4, 5, 11, 12 Some studies have also shown the existence of greater visual dependence4, 5 and altered vertical perception in hemiplegic patients.13, 14, 15, 16 Postural control problems are more frequent in patients with right brain damage.13, 17 Hemineglect may be responsible for balance disorders in hemiplegic patients after stroke.14 However, little is known about the interactions occurring between cognitive processes and the attentional demands involved in postural control in hemiplegic patients. Postural control in healthy subjects is usually assumed to be an automatic task, but many studies using a dual-task paradigm have shown that postural control requires attention.18 To define attention, we quote the most frequently used definition, which was given by William James in 1890: “It is the taking possession by the mind, in clear and vivid form, of one out of what seem several simultaneously possible objects or trains of thought. Focalization, concentration, of consciousness are of its essence. It implies withdrawal from some things in order to deal effectively with others. …”19(p403-4) Attention is the first step in learning. Information processing could be subdivided into 2 processes: an automatic process and a controlled or conscious process. The controlled process may be perturbed if another task has to be performed simultaneously or if the task is too lengthy. Attention can be selective, focused or divided, phasic or sustained. Each type of attention can be assessed using different tests, such as daily life questionnaires or arithmetic tests or by measuring reaction time. The aim of dual-task procedures is to assess the information processing capacity of subjects performing 2 tasks at the same time. The tasks can be said to be independent if each task is performed correctly, which shows that the attentional requirements of the 1 task are not necessary to perform the other task. However, if the performance level obtained in 1 of the 2 tasks decreases in comparison with that obtained when this task is performed alone, this means that the attentional requirements of the 2 tasks exceed the subject’s attentional capacity.20 Dual tasks have been used with many groups of subjects, such as lower-limb amputees21 and patients with traumatic brain injury22 performing a cognitive task (primary task) at the same time as a postural task (secondary task). If subjects’ attentional capacity is exceeded, their performance on 1 of the 2 tasks, or both, will deteriorate. With the dual-task paradigm, some studies have shown that the attentional capacity of hemiplegic patients is lower than that of healthy subjects.23 Other studies have shown that the attentional demands increase depending on the difficulty of the postural task24 (sitting, standing feet together) and that attention is altered in hemiplegic subjects with balance disorders and in fallers.25 In these studies, changes in the cognitive performances have been assessed during a postural task, whereas changes in postural performances were not assessed during the cognitive task. Another study has assessed the effects of rehabilitation on hemiplegic subjects’ balance capacity.26 This longitudinal study on patients before and after rehabilitation showed that the postural control processes changed in postacute stroke patients performing dual tasks with their eyes closed (EC) as compared with the eyes open (EO) condition, in terms of weight bearing and COP velocity. The hemiplegic patients were not compared, however, with healthy sex- and age-matched subjects. No studies have therefore been performed so far on postural control in chronic hemiplegic patients performing a cognitive task in comparison with healthy subjects. We have also addressed the influence of age on postural control during the performance of a dual task by hemiplegic patients. Several studies on healthy older subjects have shown the occurrence of changes in the postural control of body sway under dual-task conditions18, 27 and during gait.28 To our knowledge, however, the effects of age on dual-task performance have never been studied in hemiplegic subjects. The aim of the present study was therefore to determine whether any changes in the postural control processes occur in hemiplegic patients of various ages with chronic stroke performing a cognitive task, and what differences they may show in comparison with healthy subjects. The dual task used here was designed to establish the importance of attention in postural control, to obtain further information about the postural control processes, and to develop new tools for assessing postural control in hemiplegic patients. Studies on dual-task paradigms are of considerable clinical importance. Hemiplegic subjects frequently perform dual tasks in everyday life, such as standing and talking or standing and washing or standing and dressing. It is therefore necessary to determine what effects the performance of dual tasks may have on postural control. If the performance of a dual task can sensitize the dynamometric recordings, then this paradigm may also constitute a useful simple test for assessing the postural abilities of hemiplegic subjects in clinical practice. Methods  We used an AMTI forceplatea measuring 0.6×0.4m to assess the displacement of the COP in hemiplegic patients and healthy subjects. The sampling rate was 100Hz. The AMTInetforce software programa was used for the data recording and the Bioanalysis software programa was used for the data processing. The parameters measured were the sway area and the sway path. A GAITRite systemb was used to assess subjects’ walking speed, in order to characterize the 2 populations of hemiplegic and healthy subjects. Participants This retrospective study was carried out on hemiplegic patients undergoing postural assessment at our department who had a stroke at least 5 months previously. Assessments of this kind are carried out routinely on hemiplegic patients at our department. The inclusion criteria were: poststroke hemiplegia and the ability to maintain a standing position without any help for 30 seconds. The exclusion criteria were: vestibular disease, cerebellar disease, visual impairments not corrected by glasses, cognitive disorders making it impossible to perform the dual task, and aphasia. We included 23 hemiplegic patients in this study. There were 13 men and 10 women (mean age ± standard deviation, 50.3±14.9y; range, 22−77y), including 12 left hemiplegic patients and 11 right hemiplegic patients. Four of these patients had suffered from hemorrhagic strokes and 19 from ischemic strokes. The mean time elapsing since stroke was 37±28 months (range, 5−110mo). Hemiplegic patients were compared with 23 healthy age- and sex-matched control subjects (10 men, 13 women) with a mean age of 44.4±14.4 years (range, 24−78y). Assessment Procedure We performed a clinical assessment on each subject to quantify the lesion, neurologic and joint impairments, hemineglect, balance, and gait impairments. The Fugl-Meyer Assessment modified by Lindmark and Hamrin29 was used to assess balance control. Sensory impairments were clinically assessed to detect any epicritic and proprioceptive sensory deficits. The pick and touch test and graphesthesia test were used for epicritic sensory assessment, and the arthrokinesia test and pallesthesic test for proprioception assessment. Quantitative assessments of balance were carried out under the following conditions. The subjects were asked to adopt the most stable standing position, barefoot, on a piece of hardback paper fixed to the forceplate. The foot position chosen by the subjects was drawn on the hardback paper to ensure that the same position would be adopted by the subject under the various test conditions. The recording session lasted for 30 seconds. The first test was run in the EO condition. After a break of 15 seconds, the second test was run in the EC condition. After a further break of 15 seconds, the third test was run in the eyes open with an arithmetic task (EO-AT) condition. The arithmetic task was a 1-digit count-down from 50 (50, 49, 48, …). During the EO tasks, the subjects were asked to fix a target placed in front of them at eye level. Before each recording began, subjects were asked not to talk (except in the dual task), to keep their arms alongside their trunk, and not to move. In the dual task, subjects were asked to perform the task while counting loudly at a normal talking speed to check the execution of the dual task. To assess the body weight distribution, we used a second AMTI forceplate. The weight distribution between the lower limbs was measured in the hemiplegic patients in the standing position with their eyes open, with 1 leg on each AMTI forceplate. The 2 forceplates were used only to determine the body weight distribution, and not during the performance of the dual or eyes closed tasks. Data Analysis The displacement (sway path length [in centimeters]) and the sway area of the foot COP (the 95% confidence ellipse drawn on the distribution of the data points [in cm2]) were analyzed during the 30-second recording epoch. These data were analyzed under the 3 conditions EO, EC, and EO-AT. The right and the left hemiplegic patients were also compared separately under the same conditions. Statistical Analysis We used the Student t test to check the differences between the 2 populations. Analysis of variance (ANOVA) was performed on all the other comparisons. EO sway path was compared with the EC path and EO-AT, and the EC sway path was compared with the EO-AT path in both hemiplegic and healthy subjects. Similar comparisons were carried out on the sway areas. The results obtained on hemiplegic patients in the 3 conditions were also compared to those obtained on healthy subjects under the same conditions. Linear regression was performed to compare the effects of age on sway area and path between healthy subjects and hemiplegic patients. The data subjected to the ANOVA were normally distributed (as confirmed using the Kolmogorov-Smirnov test). Results Population In the hemiplegic patients’ group, there were 12 subjects with superficial sensory impairments and 10 subjects with proprioceptive sensory impairments on the hemiplegic side (test with arthrokinesia), and 4 subjects showed hemineglect in the Bells test.30 This population included 1 patient with type 2 diabetes without any neuropathy at the clinical examination. This patient was being treated with oral medication for the diabetes. No subjects had any clinical signs of neuropathy at the clinical examination performed on the sound limb. There were 3 fallers scoring less than 1 fall a week. The mean value of the hemiplegic patients’ self-selected walking speed was .42±.23m/s, as compared with that of the healthy subjects, which was 1.16±0.14m/s. The weight distribution in hemiplegic patients was asymmetric, and significantly in favor of the sound leg in comparison with the hemiplegic leg (P<.001). Sway Area and Path in Hemiplegic Patients The sway area was greater in the EC condition than in the EO condition in hemiplegic patients (P<.001). The sway area was also greater in the EO-AT condition than in the EO condition (P<.017). The sway area differed significantly between conditions EO-AT and EC in hemiplegic patients (P<.014) (fig 1). The sway path was longer in the EC condition than in the EO condition in hemiplegic patients (P<.001). The sway path length differed significantly between conditions EO-AT and EO (P=.05). The sway path was longer in the EC condition than in the EO-AT condition (P<.01) (see fig 1). Sway Area and Path in Healthy Subjects The sway area was larger in the EC condition than in the EO condition (P<.036) in healthy subjects. The sway area did not differ significantly in these subjects between conditions EO-AT and EO (P<.42). The sway area was larger in condition EC than in condition EO-AT in healthy subjects (P<.01) (see fig 1). The sway path did not differ significantly between conditions EC and EO (P<.12) in healthy subjects. These subjects’ sway paths did not differ significantly between conditions EO-AT and EO (P<.58), nor did their sway paths differ significantly between conditions EC and EO-AT (P<.15) (see fig 1). Comparisons Between Hemiplegic Patients Versus Healthy Subjects Sway area in the EO condition did not differ significantly between hemiplegic patients and healthy subjects (P=.99). Sway area in the EC condition differed significantly between hemiplegic patients and healthy subjects (P=.016). A greater sway area was recorded in the EO-AT condition in hemiplegic patients than in healthy subjects (P=.004) (see fig 1). Sway path was longer in the EO condition in hemiplegic patients than in healthy subjects (P=.03). Sway path was longer in the EO-AT condition in hemiplegic patients than in healthy subjects (P<.001). Sway path was also longer in the EC condition in hemiplegic patients than in healthy subjects (P<.001) (see fig 1). Effects of Age on Dual-Task Performances In hemiplegic patients, a significant increase in the sway area (P=.05) was found to occur with age in the dual-task condition. The slope of the linear regression was significantly steeper in hemiplegic patients than in healthy subjects (t=12.08, P<.001) (fig 2). In hemiplegic patients, a significant increase in sway path length (P<.01) was found to occur under the dual-task conditions with age. The slope of the linear regression was significantly steeper with hemiplegic patients than with healthy subjects (t=7.24, P<.001) (see fig 2). The sway path length and sway area of the hemineglect patients were also compared with those of the other hemiplegic subjects to check whether hemineglect was more prevalent with age, because this might be a factor contributing to the differences between the performances of older and younger patients. The 2 groups did not differ significantly in terms of age (P=.727), sway path (P=.681), or sway area (P=.387). Comparisons Between Left Versus Right Hemiplegic Patients Body sway area did not differ significantly between left and right hemiplegic patients (P=.63). Body sway path length did not differ significantly between left and right hemiplegic patients (P=.28) (fig 3). Weight Distribution in Hemiplegic Patients The weight distribution data were analyzed (fig 4) and compared between the left and right hemiplegic groups. In the left hemiplegic group, the asymmetry of the weight distribution was significantly greater than in the right hemiplegic group. In the left hemiplegic group, the weight bearing on the sound lower limb was greater than on the contralateral side (P<.001). In the right hemiplegic group, there was no significant difference in the weight distribution between the limbs (P=.067). Discussion The results obtained in the present study show that changes in the postural control processes occur in hemiplegic patients with chronic stroke of various ages performing a cognitive task. Changes in postural control were found to occur in the patients performing attention-demanding cognitive tasks: the body sway area and path length, as recorded by a dynamometric platform, increased when hemiplegic patients were performing a dual task. This was not the case in healthy subjects. In addition, the effects of age on the dual-task performance were established: under dual-task conditions, body sway was greater in the older than in the younger hemiplegic patients. The effects of dual task on postural control have been previously documented in patients with other pathologies as well as in young and older healthy subjects18 but not in chronic hemiplegic patients as compared with control subjects. Our results are in agreement with those of de Haart et al,26 who reported that a change in postural control occurred under dual-task conditions as compared with eyes open conditions. However, the aim of that study26 was to assess recovery of balance in postacute stroke patients and no comparisons were made with control sex- and age-matched subjects. To our knowledge, the present study is the first to assess postural control using posturographic methods in chronic stroke patients under dual-task conditions. In the present study, the hemiplegic patients showed an increase in body sway area and path length in the EC condition as well as in the EO-AT condition. Nardone et al12 have described this effect under EC versus EO conditions in hemiplegic patients in comparison with healthy subjects. These authors noted that the sway area was larger under EC than EO conditions in the case of the hemiplegic patients. This suggests that attention is as necessary as vision for postural control in hemiplegic patients. The second important finding to emerge from this study concerns the effects of age on the dual-task performances of hemiplegic patients. The stance stability of older hemiplegic patients decreased in the dual-task condition in comparison with younger hemiplegic subjects and healthy subjects. Moreover, increasing age was found to be closely correlated with decreasing postural performances in hemiplegic subjects when they performed the arithmetic task. This was in keeping with the results of studies performed on healthy older subjects described by Woollacott and Shumway-Cook18 in their review. However, no difference was found to exist between older and young healthy subjects performing a dual task. These results may be explained by the fact that the arithmetic task was a simple one. Indeed, Woollacott and Shumway-Cook18 reported that the effects of cognitive task performance on postural control in older subjects depend on many factors, including the complexity of the cognitive task, the difficulty of the postural task, and the age and balance abilities of the subjects. There seem, therefore, to be additional effects of age and hemiplegia making dual tasks more difficult to perform. The dual task seems to be a useful paradigm for assessing postural control in hemiplegic patients. Using a simple cognitive task such as the present arithmetic task, we established that a change occurs in hemiplegic patients’ postural control as the result of the attentional demands imposed. This cognitive task is one that can be easily performed by most hemiplegic patients. The performance of tasks of this kind had no effect on healthy subjects. There are several possible explanations for the change in postural control occurring in hemiplegic patients during the performance of a cognitive task. In the first place, their attentional capacity may have decreased.23, 31, 32 Marshall et al23 have reported that hemiplegic patients performing a visual task showed an impaired attentional capacity, as shown by the lengthening of the dual-task performance times. Stapleton et al31 have reported that the sustained and selective auditory attention and the selective visual attention are affected in hemiplegic patients and that some patients also showed visual inattention. Many studies, such as that by LaBerge,20 have mapped the brain location of attentional processing. The brain regions responsible for processing attention are the prefrontal, posterior cortical, and thalamic regions. Van der Werf et al32 have reported attention disorders in stroke patients with complex attention deficits after damage to the intralaminar nuclei. Another explanation could be that the attentional demands involved in performing cognitive or postural tasks increase in hemiplegic patients. For example, the equinus varus foot of a hemiplegic subject was responsible for difficulties in maintaining the standing position, possibly due to an increase in the attentional demands involved in maintaining equilibrium. This hypothesis is more difficult to check. The third possible explanation is that under dual-task conditions, a decrease in attentional capacity may be associated with an increase in the attentional demands involved in performing the postural control task and the concomitant cognitive task. In this study, we did not observe the existence of any difference in body sway between left and right hemiplegic patients. Rode et al17 have reported a larger sway area and a greater displacement of the COP under the sound lower limb in left hemiplegic compared with right hemiplegic patients. Lesions affecting the right brain hemisphere may result in more severe postural control disorders in hemiplegic patients, and in more pronounced spatial data processing impairments. However, in that study, 11 subjects previously showed hemineglect that had disappeared at the moment of the assessment, but those patients may still have had persistent postural representation deficits. In our population, only 4 of the 12 left hemiplegic patients had hemineglect. Another possible explanation for the absence of any differences in body sway between left and right hemiplegic patients might be found in the methods used in the present study. Our hemiplegic patients were free to choose their most stable foot position. This probably reduced the importance of differences in the changes in postural control between the right and left hemiplegic patients’ groups. Another explanation for the lack of difference between left and right hemiplegic subjects is that the time elapsing between the acute stroke and the posturographic measurement was as long as 28 months on average, that is, quite a long time had elapsed since the acute event. The differences between these 2 groups probably decrease with time after stroke. However, the body weight distribution between the lower limbs was found to be more asymmetric in left than right hemiplegic patients: greater relative weight was placed on the sound lower limb in left than right hemiplegic subjects. This asymmetry of the body weight distribution has been observed in previous studies on hemiplegic subjects.13, 17 In our study, the hemiplegic patients with right brain damage showed greater changes in their postural control (asymmetry of body weight distribution) than the hemiplegic patients with left brain damage. This finding is in agreement with the data available in the literature. The present hemiplegic and healthy subjects were free to place their feet in the most stable position. The position of their feet was not imposed as in other studies in the literature, because many patients could not even stay in the standing position with their feet together. The freedom they were allowed to choose the position of their feet might explain why the same body sway area was recorded in hemiplegic patients and healthy subjects in the EO condition. Admittedly, the subjects were asked to count aloud during the dual-task condition. Some studies have mentioned changes in the body sway occurring when subjects are speaking.33 The respiratory and articulatory movements involved in speaking might account for these changes in the body sway. In our study we had to make sure that the arithmetic task was being performed, which is why we asked the patients and subjects to count aloud. However, performing the arithmetic task aloud did not affect the postural control parameters in our healthy subjects. It can therefore be concluded that this factor did not bias our study. Dual tasks provide a useful means of testing postural control in hemiplegic patients in clinical practice, because this situation often occurs in everyday life, when a subject is standing and talking or standing and washing or standing and dressing, for instance. In addition, dual tasks provide a simple test that increases the sensitivity of the postural tests commonly used in clinical practice. Studies on dual-task paradigms are therefore of considerable clinical importance. It would be interesting to conduct further studies to assess the relationships between the changes in postural control occurring during the performance of dual tasks and the risk of falling to which hemiplegic patients are exposed. This useful paradigm also provides a simple means of assessing whether hemiplegic subjects showing good postural control in simple tasks condition may use different postural control strategies under dual-task conditions, showing the existence of latent postural control abnormalities. In fact, this study has shown that the postural control of hemiplegic patients is superimposable on that of control subjects under eyes open conditions, whereas dual tasks involve changes in hemiplegic patients’ postural control patterns. Dual task conditions therefore increase the sensitivity of the postural tests available for use on hemiplegic subjects. This paradigm could also be used to assess the effects of therapy on hemiplegic subjects. It could be used for example to show the effects of botulinum toxin injection (intended to reduce spasticity) on postural control. The dual task can be used here to assess the attentional demands involved in postural control: if the patient’s stability improves after botulinum injection, this means that the attentional demand has decreased. Conclusions The results of this study show that hemiplegic patients’ postural control performances deteriorated during the performance of a dual task. The effects of age on hemiplegic patients’ dual-task performances were also reflected in the increase in sway area and sway path length recorded in the cases of the older patients performing the dual task. The performance of the simple arithmetic task had no effect on healthy subjects, whereas the attentional capacity of hemiplegic patients did not suffice to perform the dual task, and the quality of their stance decreased accordingly. Dual tasks therefore seem to be a useful means of assessing postural control in hemiplegic subjects. Tasks of this kind could be used in forthcoming studies to assess the changes in hemiplegic patients’ ability to cope with the demands of postural control after treatment. Suppliers References 1. 1Kirker SG, Jenner JR, Simpson DS, Wing AM. Changing patterns of postural hip muscle activity during recovery from stroke. Clin Rehabil. 2000;14:618–626. MEDLINE |
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a Department of Physical Medicine and Rehabilitation, Faculty of Medicine, University of the Mediterranean, Public Hospital System of Marseilles, University Hospital la Timone, Marseilles, France b CSAM, Human Movement Laboratory, Salvatore Maugeri Foundation, Scientific Institute of Pavia, and Department of Experimental Medicine, Section of Human Physiology, University of Pavia, Pavia, Italy c Movement and Perception, UMR 6152, Faculty of Sport Science, Marseilles, France.  Reprint requests to Laurent Bensoussan, MD, Fédération de Médecine Physique et de Réadaptation, CHU Timone, 264 rue Saint-Pierre, 13005 Marseille, France
No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the authors or upon any organization with which the authors are associated. PII: S0003-9993(07)00352-8 doi:10.1016/j.apmr.2007.05.009 © 2007 American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation. Published by Elsevier Inc. All rights reserved. | |
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