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Brain Injury, June 2011; 25(6): 581–586 Effect of concurrent cognitive tasks on gait features among children post-severe traumatic brain injury and typically-developed controls MICHAL KATZ-LEURER1,2, HEMDA ROTEM2, OFER KEREN3, & SHIRLEY MEYER2 1Sackler Faculty of Medicine, School of Health Professions, Physical Therapy Department, Tel-Aviv University, Israel, 2Alyn Children’s Orthopedic Hospital and Rehabilitation Center, Jerusalem, Israel, and 3Acquired Brain Injury, Rehabilitation Department Sheba Medical Center, Sackler Faculty of Medicine, Tel Aviv University, Israel (Received 23 April 2010; revised 24 February 2011; accepted 14 March 2011) Abstract Aim: To investigate and compare the influence of concurrent cognitive tasks on gait characteristics in children post-traumatic brain injury (TBI) and typically-developed (TD) controls. Methods: Fifteen children post-TBI (aged 9.5� 2.2 years) and 15 TD controls (aged 9.9� 1.3 years) were included in the study. The children were asked to walk under three conditions: (1) walking at a self-selected speed, (2) walking at a self- selected speed while memorizing and recalling a series of three random numbers and (3) walking at a self-selected speed while listening and identifying commonly experienced sounds. Gait parameters include walking speed, step time and length and step time and length variability as measured with the GAITRite� system. Results: Introduction of a concurrent task led to decreased walking speed and step length and increased step time and step length variability in both groups, but with a significantly prominent effect in children post-TBI. The results also showed that the effect of a concurrent cognitive task on walking depended on the complexity level of the task. Conclusion: When children were asked to perform an additional task while they were walking, this had a negative effect on their gait. One may deduce from these results that control of the rhythmic stepping mechanism at a self-selected walking speed in children is dependant to an extent on their ability to focus attention on their gait. In children post-TBI who usually have an attention deficit anyway, this ability is severely disturbed. Keywords: Concurrent tasks, gait characteristics, traumatic brain injury (TBI) Introduction Many situations in daily activities involve concurrent cognitive and motor tasks. The ability to divide attention and the capacity to process information regarding performance of two or more tasks simul- taneously is essential [1]. For example, walking is a basic daily activity which is often accompanied by various types of concurrent cognitive as well as motor tasks. Since attention is a limited resource it may become overloaded by competing attention demands and subsequently might lead to reduced performance in one or all tasks [2, 3]. Dual-task paradigms are classically used to study involvement of attention in gait control [4]. The paradigms combining gait and cognitive tasks have shown that walking is not purely automatic but requires atten- tion [5–7]. Among healthy adults of all ages as well as among people with a neurological deficit the influence of cognitive activity on gait consistently exhibited a decreased gait velocity and increased gait variability [8–12]. Following severe traumatic brain injury (TBI) children may show deficits in a wide range of cognitive and physical activities. Walking perfor- mance is often characterized by a high level of variability associated with poor balance, as compared Correspondence: Michal Katz-Leurer, Sackler Faculty of Medicine, School of Health Professions, Physical Therapy Department, Tel-Aviv University, Tel-Aviv 69978, Israel. Tel: 972-3-6405432. Fax: 972-3-6409223. E-mail: michalkz@post.tau.ac.il ISSN 0269–9052 print/ISSN 1362–301X online � 2011 Informa UK Ltd. DOI: 10.3109/02699052.2011.572943 to typically-developed controls [13]. As increased walking variability may imply less efficient automatic control, children post-TBI may need more attention to walking and as a result might be more vulnerable to the effect of a concurrent task. In addition to their motor impairments, children with TBI often have deficits in executive function, memory, with increased distractibility or even per- severation, all of which demand an even higher attentive input than normal children during any task performance. Therefore, the addition of a cognitive task to walking may alter gait parameters. Huang et al. [12] found that the effect of a concurrent task on gait was task-related. Comparing the effects of different cognitive tasks (visual iden- tification, auditory identification and memorization) on gait variables in typically developing 5–7-year-old children reveals that the auditory identification task caused the greatest interference in gait speed, cadence and step length, while memorization caused the least interference. It may therefore be hypothesized that a more complex task such as auditory identification would cause significant attention-related gait changes as compared to a memorization task in children post-severe TBI. The aim of this study is to investigate and compare the influence of concurrent cognitive tasks on gait characteristics in children with post-TBI and typically-developed (TD) con- trols. There is little information on the effect of a concurrent task on walking in these children. Since walking is a basic daily activity and is often accom- panied by various types of concurrent tasks, under- standing the effect of a concurrent task on walking should have significant implications for clinicians treating children with post-severe TBI. Methods Subjects Fifteen children post-TBI who were either outpa- tients or former patients of the Alyn Children’s Rehabilitation Hospital in Jerusalem, Israel were engaged in the study. Included were children post- severe closed head injury (Glasgow Coma Scale (GCS) score at admission to the emergency room of �8) [14], at least 1 year post-trauma, aged 7–13 years who were independent ambulators (foot ortho- ses permitted). Excluded were those who had received botulinum toxin for spasticity management or had undergone orthopaedic surgery in the previ- ous 6 months and those who were unable to follow simple instructions. Fifteen TD children matched for age served as controls. The TBI group comprised nine boys and six girls, aged 9.5� 2.2 years. The time since injury was a mean of 3.5 years (range 1.5–7 years); seven of the children were classified as double hemiparesis, eight as hemiparesis. In the TD group there were 10 boys and five girls, aged 9.9�1.3 years. Informed consent was obtained from each partic- ipant and his/her parents before inclusion in the study. The study protocol was approved by the hospital’s institutional ethical committee. Gait assessment Parameters of gait were recorded using a pressure sensitive mat, the ‘Gaitrite1’ system (Gaitrite�, CIR Systems Inc., Clifton, NJ) which is an electronic walkway that automates the collection of spatial and temporal parameters of gait. The validity of the Gaitrite system has been supported by studies in adults [15]. Thorpe et al. [16] recently showed that the Gaitrite� system is a reliable method of measur- ing spatiotemporal gait parameters in children as well. For each test the children were asked to walk along the mat at their regular speed. ‘Stop’ signs were positioned on the floor 2 metres beyond each end of the walkway, providing visual feedback to subjects. Each cycle of walking was �7.66 metres, of which 3.66 metres were on the mat. Each subject completed three sequential cycles of walking for a total of almost 11 metres on the mat. Testing was performed while the children wore comfortable clothes and their regular shoes and orthotics when needed. Distractions in the room were minimized. The investigator and thechild’s parent were present during testing. All temporal and spatial gait parameters were calculated utilizing the software of the Gaitrite system using pre-programmed definitions, calcula- tions and data from the three cycles. Parameters analysed included walking velocity, step length and step length variability, step time and step time variability [16]. Any partial footfalls that did not have a clearly defined beginning and ending or were in contact with the edge of the mat were edited out. Gait variability was expressed as the coefficient of variation (CV) which is SD/mean �100. Procedure After a rest period the children were asked to walk at their regular pace on the Gaitrite, three cycles for each one of the trials: regular walking followed by performing the two different cognitive tasks—the first was to memorize and recall three random numbers one digit each and the second was to identify simple auditory sounds. In a pre-test period children with post-severe TBI were assessed for their ability to memorize and recall three numbers consecutively. It was noticed that the 582 M. Katz-Leurer et al. children could perform the assignment correctly and sequentially only with one digit numbers. So for this study, the children were asked to recall three random numbers of one digit each. In addition, in a pre-test period children with post-severe TBI were asked to identify different sounds. The sounds chosen were clear and simple as commonly experienced by children (such as dog barking, doorbell ringing) and included a total of 15 sounds that the children could identify without mistakes. After three walking cycles with no concurrent task, the children were asked to remember the numbers presented to them and to repeat the numbers over and over in exactly the same order. All the children could perform the task with no mistakes. Then the children were asked to walk while repeating the numbers. Correct and incorrect repetitions of num- bers were counted and the incorrect repetitions out of the total number were recorded. In the second cognitive task the sounds were first projected through a speaker at the far end of the walkway. All of the sounds were less than 2 seconds in duration and the children were asked to identify each as quickly as possible by naming the sound out loud. Then the children were asked to walk while listening and identifying each sound as quickly as possible. The number of sounds that each child identified incorrectly out of the total of 15 possible sounds was recorded. Statistical analysis A preliminary paired t-test was used to assess differences in gait parameters between legs. No significant differences were noted; therefore, the mean value of both legs is presented. The normality of the parameters’ distribution was verified using the Kolmagirove Smirnove test. The values of gait velocity, step time, step length and step time and length variability were summarized using means and standard deviations. To assess differences between groups in the fulfilling of the cognitive assignment—number of cycles achieved in each task, a t-test was performed. To evaluate any different effect of the task on performance quality, a mixed ANOVA model was performed. The between-subject factor is the group factor (TBI vs TD), the within-subject factor is the two cognitive tasks and the interaction term (group� task) and the dependent variable was the percentage error in each assignment. For assessing any differences between the three walking conditions without and with concurrent tasks, a mixed ANOVA model was applied when the dependent variable was the gait parameter. A separate model was built for each parameter. The between-subject factor is the group factor (TBI vs TD), within subject factor (without and with the first and the second concur- rent tasks) and the interaction term (group� task). A p-value< 0.05 was considered statistically signif- icant. All statistical analyses were performed using SPSS v. 17 software packages. Results Cognitive tasks–percentage error Both groups exhibited significantly higher mistakes in the sound recognition assignment. The mean percentage errors between the two cognitive tasks was significantly different between groups; by mean, children post-severe TBI have 31.9% more mistakes compared to the controls (F(1: 28)¼29.6, p<0.01); 23%�5% more mistakes at the memorization assignment (mean of 24.5% among children post-TBI vs 1.5% among the controls) and 39%�6% more at the sound recognition assign- ment as compared to the TD group (mean of 46.3% among children post-TBI vs 6.7% among the con- trols) there was a significant group*assignment interaction effect (F(1: 28)¼ 9.45, p< 0.01), as chil- dren post-TBI exhibited larger differences between assignments (TBI; 20%�16%, TD 5%�7%) (Table I). Baseline differences between groups Gait parameters during all three gait conditions are presented in Table II. In the regular walking test, only the step length was significantly different between groups; children with post-severe TBI walked with a smaller step length as compared with TD controls (mean of 59.1� 10.1 cm vs 66.1�6.1 cm, respectively, t28¼ 2.34. p¼ 0.02). Gait parameters during cognitive assignments In the repeated model, significant differences were noted between groups in all assessed gait parameters. Children post-TBI exhibit significant slower gait velocity, significant shorter step length and signifi- cantly larger step length and step time variability. Table I. Number of cycles and percentage of errors in task performance by groups. Task Numbers Sounds TBI TD TBI TD No. of cycles 11.0� 4.3 16.6� 2.6 17.6� 2.6 14.7�2.0 % of error 24.5� 22.9 1.5� 3.2 46.3� 22.9 6.7�5.3 Values are mean�SD. Effect of concurrent cognitive tasks on gait 583 There were significant differences in gait param- eters between assignments in both groups. Gait velocity Gait velocity was significantly different between trials (F2;50¼38.1, p< 0.01). After bonferroni adjustment for multiple compression it was noted that walking velocity was significantly faster at usual walking and it decreased by a mean of 23.8� 3.9 cm s�1 at the number assignment (mem- orization) and by 37.0�5.1 cm s�1 at the sound (auditory) assignment. In addition, a significant difference was noted between dual task conditions; during the sound assignment children walked signif- icantly slower as compared to the walking velocity during the number assignment (by a mean of 13.1� 3.7 cm s�1, p< 0.01). Additionally, there was a significant group-assignment interaction effect; gait velocity decreased for both groups in the dual task conditions, but significantly more among children post-TBI. In the number assign- ment, gait velocity decreased by 36.5� 6.9 cm s�1 among children post-TBI as compared to 8.3� 3.6 cm s�1 among TD children (p< 0.01). In the sound assignment walking velocity decreased by 48.7� 7.9 cm s�1 among children post-TBI as compared to 25.3� 6.5 cm s�1 among TD children (p¼0.03). Step time Step time was significantly different between trials (F2;50¼ 23.42, p<0.01). Mean step time was sig- nificantly increased in the dual task conditions as compared to baseline; it increased by a mean of 0.10� 0.02 seconds in the number assignment and by 0.10� 0.01 seconds in the sound assignment. No significant difference was noted between dual task conditions. A significant group-assignment interac- tion effect was noted also for the step time param- eters. Step time increased during dual task conditions in both groups but significantly more among children post TBI. In the number assign- ment, step time increased among children post-TBI by 0.17�0.15 seconds as compared to 0.03� 0.04 seconds among TD children (p< 0.01). In the sound assignment, step time increased by 0.16� 0.10 seconds among childrenpost-TBI as compared to an increase of 0.05� 0.03 seconds among TD children (p<0.01). Step length In addition, step length was significantly different between trials (F2;50¼ 13.9, p<0.01). Step length was significantly shorter at the sound assignment. It was shorter by a mean of 9.48� 2.2 cm as compared to the baseline value and by 5.9� 1.1 cm as com- pared to number assignment. Step length and step time variability Step length and step time variability were signifi- cantly higher among children post-TBI across the assignments, with no significant difference between the assignments (step length variability, mean between groups difference 12.2� 2.2, F1;25¼ 8.3, p< 0.01, step time variability mean between groups difference 7.9� 2.6, F1;25¼ 9.2, p< 0.01). Discussion The present study examined the effects of concur- rent cognitive tasks on gait performance in children post-TBI in comparison to TD controls. There was a negative effect on walking performance when the children did a concurrent task and this effect was task-dependant. During the auditory assignment, the performance error rate was significantly higher as compared to the memorization assignment and the effect on walking was more detrimental: walking speed decreased and step time increased significantly in the auditory assignment in both groups but with a Table II. Gait parameters in children post-TBI and TD controls in usual walking and in the two dual task conditions. Usual walking Dual task- numbers Dual task- sounds ^p-value #p-valueTBI TD *p-value TBI TD TBI TD Velocity 1.2�0.3 1.3� 0.1 0.15 0.8� 0.2 1.3� 0.2 0.7� 0.1 1.1� 0.2 <0.01 <0.01 Step length 59.1�10.1 66.1� 6.1 0.02 51.2� 11.1 65.4� 5.7 43.9� 11.7 58.7� 8.0 <0.01 0.58 Step length variability 9.3�9.1 8.2� 10.2 0.27 13.4� 14.6 5.4� 3.0 24.0� 17.0 8.4� 5.7 0.12 0.53 Step time 0.45�0.07 0.48� 0.05 0.55 0.60� 0.11 0.51� 0.07 0.61� 0.09 0.53� 0.06 <0.01 <0.01 Step time variability 11.5�15.4 6.8� 7.6 0.23 13.6� 10.1 6.8� 4.8 16.2� 7.8 8.6� 9.2 0.15 0.80 *p-value between groups at usual walking (t-test). ^p-value within subjects (usual walking, numbers, sounds) (Repeated measure ANOVA). #p-value interaction effect group and manipulation (Repeated measure ANOVA). 584 M. Katz-Leurer et al. significantly prominent effect among children post-TBI. The interference effects of concurrent cognitive tasks on locomotor performance has been assessed and described before among children as well as among adults [12, 17, 18]. It has been suggested that the outcome of dividing attention between two concurrent tasks depends on the type and level of difficulty of the tasks and on the priority given to each task [3, 4]. Since attention resources are limited, two tasks will compete for resources if they are carried out at the same time. They may interfere with each other when the total amount of resources demanded exceeds those available. In the present study, the auditory assignment caused greater interference than the memorization assignment. It might be that memorizing a set of three numbers is a simple memory task which requires short-term learning and recall as compared to the sound recognition assignment which involves identification, recall of existing knowledge and naming capabilities. The auditory assignment is clearly more demanding and requires more attention resources [4, 5, 18]. In previous studies, the negative effect on locomotor speed while performing second- ary tasks involving processing of sensory stimuli was higher than for those involving other types of cognitive processing. Specifically, it has been noted that an auditory identification task produced greatest interference effects on gait than other concurring tasks [12]. One may claim that the lower effect of the concurrent cognitive task on gait characteristics in TD children is due to the fact that the cognitive task was too simple for them. It has been suggested before that it is essential to adjust the task difficulties to the individual’s capacity [19]. However, it has also been noted that even with a very light overall load on the cognitive system a difference between patients with brain damage and healthy controls could be detected [20]. In this study the memorization and the auditory assignments were adjusted to the capabilities of children post-severe TBI. By doing so one may reduce any significant baseline differ- ences between groups, but it is argued that any reduced ability in performance is the result of the demand to combine performances. One of the most frequent cognitive limitations among children post-TBI is an attention distur- bance. Performing dual tasks demands splitting attention simultaneously between two tasks and each assignment might be too difficult to perform in those whose attention ability is reduced. It has been well established that when combining cognitive and walking tasks, the walking requires attention [21] and dual tasking is sensitive enough to distin- guish between patients post-concussion from control subjects [22, 23]. The interactions between concur- rent tasks cannot be automatically generalized and should be assessed in different conditions and modalities. This may imply that the attention needed for motor and cognitive activities are not necessarily always competitive and interruptive. Step variability increases when step velocity decreases [24]. Therefore, the dual-task related increase in step length variability shown in this study could also be explained by the dual-task related decrease in step velocity. However, the results of this study show that the decrease in step velocity while performing the memorization task did not modify step variability. During the auditory assignment the mean step time was the same as for the memorization assignment, but step variability increased significantly in both groups, more so in the children post-TBI. This suggests that the increase in step variability was task-specific, in contrast to step time. These findings have clinical implications for the physiotherapist. Firstly, therapists use a lot of verbal instructions and feedback during the actual treat- ment. Therefore, a child post-severe TBI who is practicing a new and higher level of motor perfor- mance will benefit more from instructions or feed- back given before or after performing the task. On the other hand, if the child needs further refinement of an achieved motor skill and the therapist indeed wants to challenge the child, the therapist can provide concurrent feedback or add a secondary cognitive task. Another clinical implication is related to the finding that step variability increases during dual task performance. It has been noted before that step variability is associated with balance performance among children post-TBI [13], a higher step variability being associated with poor balance. Possible, the therapist should work on improving balance as much as possible before progressing to higher motor skills. However, Silsupadol et al. [25] described two adults patients who received balance training under dual task conditions. Benefits were maintained over 3 months, whereas they were not evident in a patient who trained under a single task balance training programme. The question of whether training under dual task conditions is more effective in improving gait after the patient has progressed in the single task performance needs further investigation. The therapist might instruct the family of a child post-TBI to avoid cognitive tasks in the early stages of motor training. Dual tasking and adding cognitive activities while walking should, however, be intro- duced as an effort to improve the child’s ability to perform dual tasks in a safe and functional manner. Effect of concurrent cognitive tasks on gait 585 Declaration of Interest: The authors report no conflicts of interest.The authors alone are responsible for the content and writing of the paper. References 1. Schmidt RA. Motor control and learning: A behavioral emphasis. 2nd ed. Champaign, IL: Human Kinetics Publishers; 1988. 2. 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