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Motor-Cognitive Dual-Task Training in Persons With Neurologic Disorders

A Systematic Review

Fritz, Nora E. PT, DPT, NCS, PhD; Cheek, Fern M. MALS; Nichols-Larsen, Deborah S. PT, PhD

Journal of Neurologic Physical Therapy: July 2015 - Volume 39 - Issue 3 - p 142–153
doi: 10.1097/NPT.0000000000000090
Systematic Review
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Background and Purpose: Deficits in motor-cognitive dual tasks (eg, walking while talking) are common in individuals with neurologic conditions. This review was conducted to determine the effectiveness of motor-cognitive dual-task training (DTT) compared with usual care on mobility and cognition in individuals with neurologic disorders.

Methods: Databases searched were Biosis, CINAHL, ERIC, PsychInfo, EBSCO Psychological & Behavioral, PubMed, Scopus, and Web of Knowledge. Eligibility criteria were studies of adults with neurologic disorders that included DTT, and outcomes of gait or balance were included. Fourteen studies met inclusion criteria. Participants were subjects with brain injury, Parkinson disease (PD), and Alzheimer disease (AD). Intervention protocols included cued walking, cognitive tasks paired with gait, balance, and strength training and virtual reality or gaming. Quality of the included trials was evaluated with a standardized rating scale of clinical relevance.

Results: Results show that DTT improves single-task gait velocity and stride length in subjects with PD and AD, dual-task gait velocity and stride length in subjects with PD, AD, and brain injury, and may improve balance and cognition in those with PD and AD. The inclusion criteria of the studies reviewed limited the diagnostic groups included.

Discussion and Conclusions: While the range of training protocols and outcome assessments in available studies limited comparison of the results across studies motor-cognitive dual-task deficits in individuals with neurologic disorders appears to be amenable to training. Improvement of dual-task ability in individuals with neurologic disorders holds potential for improving gait, balance, and cognition.

Video Abstract available for additional insights from the authors (Supplemental Digital Content, http://links.lww.com/JNPT/A104).

Kennedy Krieger Institute, Johns Hopkins University, Baltimore, Maryland.

Correspondence: Nora E. Fritz, PT, DPT, NCS, PhD, Kennedy Krieger Institute, Johns Hopkins University, Baltimore, MD 21205 (fritzn@kennedykrieger.org).

This project was supported by Award Number Grant 8TL1TR000091-05 from the National Center for Advancing Translational Sciences. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Center for Advancing Translational Sciences of the National Institutes of Health.

An earlier version of this work was published to OhioLink as part of Dr Fritz's doctoral thesis.

The authors declare no conflict of interest.

Supplemental digital content is available for this article. Direct URL citation appears in the printed text and is provided in the HTML and PDF versions of this article on the journal's Web site (www.jnpt.org).

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INTRODUCTION

Impairments in both mobility and cognition are common in many neurologic conditions, making previously automatic movements more attention demanding.1 Divided attention, the ability to respond to multiple stimuli simultaneously,2,3 is frequently affected more than other domains (eg, sustained attention).4 Divided attention is necessary to successfully perform 2 tasks concurrently (ie, dual tasks), such as a cognitive and a motor task (eg, walking and talking). Deficits in divided attention and dual-task (DT) ability seem linked to impairments in functional mobility in traumatic brain injury,5,6 acquired brain injury,7 multiple sclerosis (MS),8,9 Parkinson disease (PD),10,11 stroke,12 and Alzheimer disease (AD).13

The addition of a cognitive task to mobility tasks to gait or balance has been shown to amplify gait variability in individuals with neurologic disorders. Indeed, under DT conditions, individuals with PD10 and MS8 significantly increased swing and stride time variability, compared with controls. During balance DTs, individuals with MS demonstrated greater postural sway14 and sway velocity variability15 compared with controls. Impairments in divided attention may prevent individuals from allotting appropriate attentional resources to balance and gait, reduce adaptability to challenging environments such as obstacles and uneven paths, and may contribute to fall risk in PD,10 AD,13 and MS.16

Despite documented deterioration in gait and balance under DT conditions, there are few intervention studies that address this deficit. Available studies are marked by variability of training type and duration. Case studies in mild17 and severe traumatic brain injury,18 utilizing dual-task training (DTT), have reported improvements in balance,17 gait speed,18 and DT tolerance.17,18 Similarly, DTT improved balance during cognitive activities to a greater extent than mobility training alone in healthy individuals.19 The purpose of this systematic review was to examine the literature to determine the effectiveness of DTT on mobility and cognition compared with usual care in individuals with neurologic disorders.

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METHODS

Data Sources and Searches

The search terms “nervous system disease(s) or neurologic disorder(s)” with “rehabilitation or intervention” and “dual task(s) or divided attention OR multi task(s)” were applied to the title, abstract, or index term fields. These search terms were directed to the following databases: Biosis, CINAHL, Cochrane, ERIC, PsychInfo, EBSCO Psychological & Behavioral, PubMed, Scopus, and Web of Knowledge. All databases were searched from their inception until January 19, 2014. Two investigators independently screened the titles of the publications identified; if a title potentially met the inclusion criteria, or if there was inadequate information to make a decision, a copy of the article was obtained. In addition, the reference lists of retrieved articles were searched for potential studies that may have been overlooked or absent from databases.

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Study Selection

Figure 1 outlines the number of references considered at each state of the selection process before confirming the included trials. A total of 14 identified studies20–33 were eligible for inclusion; excluded study details are shown in Figure 1. Inclusion was restricted to studies of adults (>18 years old) with a central neurologic disorder diagnosis, who received motor-cognitive DTT, and were assessed on outcomes of mobility (ie, gait and balance) or mobility and one domain of cognition. Because of the paucity of training studies, repeated-measures designs were included along with randomized controlled trials (RCTs).

Figure 1

Figure 1

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Data Extraction and Quality Assessment

Data were independently extracted from the included trials by 2 authors and recorded on a standardized spreadsheet that included sample sizes, trial settings, population characteristics, intervention details, and study results. In one trial,33 there was insufficient information on outcomes and study population; the authors were contacted, but we did not receive a response. As the included studies focused on motor-cognitive DTT, the primary outcome of interest was mobility, including single- and dual-task gait velocity and stride length (ie, one temporal and one spatial measure) or balance, whereas the secondary outcome of interest was cognitive performance. All outcomes were assessed at the conclusion of training and compared with either usual care (exercise or null—no treatment) or baseline (in the case of repeated-measures designs). Because of the wide variation in study outcomes, cognitive and balance measures were not limited to one outcome measure alone; rather all measures used were assessed. The methodological quality of each study was independently evaluated, using the 5 criteria recommended by the Cochrane Back Review Group.34 This scale evaluates criteria relevant to physical therapy practice and is suitable for the evaluation of neurologic clinical trials (Table 1). Presently, there are no established cutoff scores for high- and low-quality studies with this tool.

Table 1

Table 1

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Data Synthesis and Analysis

Two independent raters synthesized the data in a standardized table, including study design, participant characteristics, intervention, comparison interventions (if present), and all outcome measures (Table 2). Because more than 30 different outcome measures were utilized as primary and secondary outcomes, we analyzed the effectiveness of DTT on single-task gait, dual-task gait, balance, and cognition to better examine the results across studies. In studies presenting full data, raw data were extracted to derive standardized mean differences in the case of RCTs and mean change in the case of repeated-measures trials as well as 95% confidence intervals for report in a forest plot.

Table 2-a

Table 2-a

Table 2-b

Table 2-b

Table 2-c

Table 2-c

Table 2-d

Table 2-d

Table 2-e

Table 2-e

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RESULTS

Study Characteristics (Table 2)

Of the 14 included studies, 3 were RCTs20–22 and 11 were repeated-measures designs.23,33 All studies were conducted in an outpatient setting. The experimental group's sample size—median (interquartile range)—was 14 (5.5), age of 69.5 (11.5) years, and a male-to-female ratio of 9 (2.5):7 (11.5). In studies with control groups, the sample size was 12 (6.3), age 72.3 (11.1) years, and a male-to-female ratio of 8.5 (3):8.5 (10.5). Seven studies enrolled greater than 20 total subjects.20,21,25–29,32 Among the 14 studies, 12 different DTT protocols were described; 3 used single sessions of cueing23,24,29 to improve gait parameters during DT gait, 7 described multisession training including various cognitive tasks paired with gait20,22,28,30,31 or balance/strength tasks,25,26 4 employed virtual reality (VR) or gaming,21,27,32,33 and 4 combined DTT with additional therapies (balance20,33 or aerobic exercise).25,26 More than 35 outcome measures were used to assess the effect of DTT, including more than 7 different tasks to assess DT gait. Table 2 outlines the DT protocols and outcome measures; here, we describe the effect of DTT on the primary outcome measures of mobility (gait and/or balance) and secondary outcome measure of cognition.

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Effect of DTT on Single-Task Gait

Spatiotemporal gait parameters (eg, velocity and stride length) were measured using 3D motion capture, 2D kinematics, and the GAITRite electronic walkway.

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Parkinson Disease

Compared with both null controls and controls participating in general exercise, individuals with PD who had DTT demonstrated significantly increased single-task gait speed and stride length,23,24,32 which were maintained at follow-up. Gait endurance also improved after training with a significant improvement on the 6-Minute Walk Test.32 In test-retest designs, individuals demonstrated improvements in walking speed,28,29,31 step length,29 step amplitude,31 and cadence.31

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Alzheimer Disease

Measures of single-task gait were reported in only one study in individuals with AD; Coehlo et al26 reported significant improvements in stride length (between-group difference 5 cm) with an effect size of 2.07 (95% confidence interval, 1.08-2.93) (Figure 2) compared with null controls.

Figure 2

Figure 2

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Brain Injury

Single-task gait was not assessed in either of the studies including individuals with brain injury.

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Effect of DTT on Balance

Although one study assessed center of pressure (COP) during the Sensory Organization Test (SOT),21 others analyzed COP measures in various single-task and DT conditions,25,33 while another25 utilized the Berg Balance Scale (BBS) to examine static and dynamic balance.

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Parkinson Disease

Yen et al21 demonstrated a significant improvement on conditions 5 and 6 (eyes closed on an unstable surface and eyes open on an unstable surface with visual surround) of the SOT in the treatment groups over the null control group, but no differences between the 2 treatment groups (VR vs conventional balance training). Mirelman et al32 measured balance indirectly with the Four Square Step Test and noted significant improvements after training that were maintained at follow-up. Conversely, Rochester et al31 measured balance with tandem stance time and found no significant improvement after training.

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Alzheimer Disease

de Andrade et al25 measured balance with the BBS, and demonstrated a large effect size of 1.67 (Figure 2) compared with the null control group (between-group difference 4.9 points). Anterior-posterior and medial-lateral COP measures were recorded in quiet stance, with the intervention group demonstrating a reduction in sway whereas controls had increased sway.

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Brain Injury

Although measured, values for quiet stance were not reported by Sveistrup et al33 and queries to the author received no response. Improvements on the Community Balance and Mobility Scale were reported for both the conventional exercise group and VR exercise group33; however, 2 of the 4 null control participants also demonstrated large improvements on the Community Balance and Mobility Scale, and no statistics were reported.

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Effect of DTT on Cognition

Several studies measured the effect of DTT on domains of cognition including memory, processing speed, and attention.

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Parkinson Disease

After cognitively challenging VR training, Mirelman et al32 reported significant improvements on the Trail Making Test, which evaluates mental flexibility and processing speed, and participants made 31% fewer errors on a serial subtraction task compared with baseline.32

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Alzheimer Disease

After DTT, large improvements on the Frontal Assessment Battery were noted by de Andrade et al25 and Coehlo et al26 (effect sizes of 1.96 and 3.07, respectively)(Figure 2), compared with a null control group (between-group differences 3.9 points and 6 points, respectively). Conversely, Schwenk et al20 found no significant differences in cognition as measured by the Trail Making Test after training, compared with a general exercise control group.

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Brain Injury

Evans et al22 reported no significant treatment effect on cognitive performance after DTT (effect size −0.59) with the Memory Span and Tracking Task (between-group difference −4.75 points) or the TEA Telephone Search while Counting task (a dual-task) compared with a null control group.

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Effect of DTT on Ability to Dual Task

The most commonly assessed outcome measure across studies was ability to DT during gait, although several examined ability to DT during quiet stance.

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Parkinson Disease

Compared with null controls, individuals with PD had significantly improved DT gait speed and stride length,23,24,32 maintained at follow-up.32 In test-retest designs, there were also significant improvements in DT gait speed and28–31 stride length,29,30 maintained at follow-up.30 Interestingly, Yogev-Seligmann et al28 reported improvements in gait speed and stride time variability during an untrained DT, suggesting that transfer of training might be possible.

Training effects in DT gait were noted even after short-term training programs. A single 30-minute session of DT training23,24 and three 30-minute sessions of DT training30 resulted in significant increases in stride length and gait velocity that were maintained at a delayed retention.

Yen et al21 reported improvements in DT balance during conditions 5 and 6 of the SOT in both the VR group and the conventional balance group, whereas individuals in the control group declined in these conditions.

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Alzheimer Disease

A common measure of DT ability during gait is the calculation of dual-task cost (DTC), which determines the specific effect of the secondary task on the primary task of walking.

DTC = [(dual task − single task)/single task] × 100

After DTT, individuals with AD demonstrated significantly reduced DTC for both velocity and stride length compared with the control group, where DTC was unchanged.20 This held true for DT walking when the secondary task was addition or subtraction.20 Similarly, Coehlo et al26 reported significant improvements in DT stride length with an effect size of 1.62 (between-group difference 6 cm) (Figure 2).

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Brain Injury

Gait outcomes were not reported by Sveistrup et al33; however, Evans et al22 reported significant improvements in DT gait speed with an effect size of 1.52 (between-group difference 6.11 seconds) (Figure 2).

A meta-analysis was not undertaken because of heterogeneity among the identified studies. The trials included variable treatments, disparate disability levels, methodological heterogeneity of the DT training protocols, and vastly variable treatment duration (range = 30 minutes to 24 hours). Given this variability, it was not possible to conduct a meaningful meta-analysis.35 The mean changes (for repeated-measures trials), mean differences (for clinical trials), treatment effect sizes, and associated 95% confidence intervals for the individual trials are presented by outcome assessment and comparative treatment in Figure 2. Effect sizes more than 0 indicate an outcome favoring the DTT group, whereas effect sizes less than 0 indicate an outcome favoring the comparison group.

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DISCUSSION

The primary goal of this systematic review was to examine the evidence, supporting efficacy of motor-cognitive DT interventions for individuals with neurologic conditions. This review found that physical therapy interventions, regardless of the method, targeting DTT resulted in improvements in single and DT walking and modest improvements in balance and cognition.

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Effectiveness and Clinical Recommendations

A formal analysis of frequency, duration, and intensity of DT therapies was not undertaken as these characteristics were either highly variable or not included. In studies demonstrating large effect sizes in Figure 2, the frequency, intensity, and duration of therapies ranged from a single 30-minute training session23,24 to 3 hours per week for 16 weeks.25,26 Thus, generalization of these results to the clinic is challenging. There were only 3 small RCTs in this review;20–22 the majority of the studies were repeated-measures design studies, which precluded the use of the PEDro scale,36 a common assessment for RCTs. The clinical rating scale was included to measure the clinical usefulness across studies.

Small sample sizes, heterogeneity of the interventions, and the outcome measures used further limit the generalization of the results. Within diagnoses, differences in the disease status of those enrolled further complicated the comparison of individuals with similar functional levels. Twelve different DT interventions were presented across the 14 studies. Thus, clinical recommendation of a single DTT protocol is challenging. Many of the interventions lacked control groups and evaluator blinding, potentially biasing the results toward a benefit with DTT. It is clear that further research is needed to standardize both DTT protocols and outcome measures sensitive to change because of such programs in neurologic diagnoses.

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Cognition

Prior studies of DT have discussed the contributions of cognition to DT deficits in PD,10,37 healthy elderly,38,39 elderly adults with cognitive impairment,40 and MS.8 This review yielded mixed results on the effect of DTT on cognition. Although several studies reported improvements,25,26 others reported no improvement20 or declines.22 Mirelman et al32 also reported a relationship between the change in the Trail Making Test score and DT gait speed. Taken together, these results suggest the importance of selecting cognitive outcome measures that are within the domain trained and further exploring the relationships between these cognitive measures and changes in mobility measures.

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TRAINING IN OTHER POPULATIONS

Elderly Adults

DT deficits similar to those of neurologic conditions have been described in elderly adults.39 After DTT for 10 to 12 weeks, the healthy elderly demonstrated improvements in cognition on the Stroop test,41 reaction time on a lower extremity motor task,42,43 Community Balance and Mobility Scale,43 and reduced fear of falling.42 In elderly adults with a history of falls, DTT for 6 weeks resulted in greater improvement in memory performance compared with controls who received only walking training.44 In elderly adults with balance impairment, 4 weeks of DTT produced improvements in cognition on the Stroop45 and both single and DT walking.45,46 Interestingly, variable training (ie, instructions to prioritize either the motor or cognitive task) was more effective for improvement of mobility and cognitive outcomes under DT conditions than fixed-priority or single-task conditions,45 and only those who experienced variable training maintained the gains in DT performance at a 12-week follow-up, whereas those who experienced fixed-priority training showed initial benefit that was not maintained at follow-up.45 This variable-priority effect has been noted in cognitive-cognitive DT training programs of healthy adults, where individuals trained with variable-priority instructions learned tasks faster and performed better than those who received fixed-priority instructions.47

A systematic review exploring the use of DTs to identify elderly fallers was inconclusive,48 but suggested that DTs may have added benefit in the assessment of fall prediction and should be studied further. Moreover, in an exploration of gait, falls, and cognition, Segev-Jacubovski et al49 concluded that combining motor and cognitive therapies should be included in clinical practice to improve mobility and reduce safety in older adults.

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Stroke

Individuals with chronic stroke have demonstrated improvements in mobility and cognitive outcomes after DTT. After a 4-week motor-motor DTT program, Yang et al50 reported significant improvements in single and DT walking compared with a null control.

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Limitations

Despite documented DT deficits, there is a paucity of motor-cognitive DTT data for many neurologic disorders. Indeed, many populations are not represented in the DTT data, most notably stroke, MS, and Huntington disease, which have known cognitive and motor deficits. Although several case studies17,18 examined DTT in individuals with neurologic deficits, there is a deficiency of RCTs in this area. Thus, we included repeated-measures designs, several of which lacked control groups. The results of these studies should be interpreted with caution, as changes over time could be due to the passage of time. To date, DTT has been formally investigated in AD,20,25,26 PD,21,23,24,27–32 and brain injury.22,33 Many of these studies provide weak evidence because of lack of blinding and small sample sizes. Studies that did not present raw data were excluded from Figure 2, further challenging generalization of these results.

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CONCLUSIONS

Although motor-cognitive interference has been well described in many neurologic populations, training studies the met the inclusion criteria were limited to PD, AD, and brain injury. Furthermore, limitations in the reviewed studies make generalizing results of this review into evidence-based recommendations difficult. Although DTT seems to be safe and effective for improving spatiotemporal measures of DT gait in individuals with PD, AD, and brain injury, more research is needed to define the specific DT interventions that are most effective and to better assess whether some interventions are more appropriate than others for a specific diagnostic group.

In conclusion, this first review to examine the outcomes of DTT across neurologic disorders suggests that DTT may improve spatiotemporal measures (velocity, step length) of single-task gait in PD and AD and DT gait in PD, AD, and brain injury, and may have a modest impact on balance and cognition in PD and AD. Future studies including larger sample sizes and greater standardization of DT protocols (eg, intensity, frequency, and duration) and outcome measures would greatly assist in the determination of the efficacy of such interventions in neurologic populations. Improvement of DT ability in individuals with neurologic disorders holds potential for improving gait, balance, and cognition that may impact independence and fall risk.

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Keywords:

balance; cognition; dual-task training; gait speed; neurologic disorders; rehabilitation

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© 2015 Neurology Section, APTA