| | The Immediate Effect of Attentional, Auditory, and a Combined Cue Strategy on Gait During Single and Dual Tasks in Parkinson’s DiseaseAbstract Baker K, Rochester L, Nieuwboer A. The immediate effect of attentional, auditory, and a combined cue strategy on gait during single and dual tasks in Parkinson’s disease. ObjectiveTo compare the effect of rhythmic auditory and attentional cues, and a combination of both cues on gait, in people with Parkinson’s disease (PD) during single and dual tasks. DesignA repeated-measures study requiring participants to perform single and dual-motor tasks under different cueing conditions. SettingHuman movement analysis laboratory. ParticipantsFifteen participants with idiopathic PD and a comparison group of 12 healthy participants. InterventionsThree cueing strategies were compared: a rhythmic auditory cue (walking in time to a metronome beat), an attentional strategy (asked to focus on taking big step), and a combination cue (asked to walk in time to a metronome beat while taking big steps). Main Outcome MeasuresWalking speed, step amplitude, and step frequency. ResultsWalking speed of PD participants improved significantly compared with noncued walking in the single- and dual-task condition with the attentional (P<.001, P=.037) and combination cue strategies (P=.013, P=.028). Step amplitude also increased significantly with the attentional and combination cue strategies in single- (P<.001, P<.001) and dual-task (P<.001, P<.001) conditions. Step frequency was reduced significantly with the attentional strategy (P=.042) in the single and dual tasks (P<.001) and combination cue strategy (P=.009) in the dual task. The rhythmic auditory cue alone did not alter significantly any parameter of gait in the single or dual tasks. ConclusionsThe attentional strategy and the combination of a rhythmic auditory cue with an attentional strategy were equally effective, and improved walking speed and step amplitude significantly during both single and dual tasks. The combination cue, however, may still be a useful alternative in situations of increased attentional demand, or where problems exist with executive function. GAIT DISTURBANCE IN Parkinson’s disease (PD) is characterized by reduced speed and step amplitude, increased stepping frequency and, in some cases, festination and freezing.1 The primary gait deficit in PD, however, has been described as an inability to generate sufficient amplitude of movement.1 Morris et al1 advocate that increasing step amplitude should therefore be the primary goal of therapy intended to normalize gait. Cueing strategies have improved gait in people with PD,2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16 and are argued to bypass the defective basal ganglia by using alternative pathways unaffected by PD to improve motor performance.17 External cues provide temporal or spatial stimuli associated with the initiation and facilitation of a motor activity and can be delivered using different modalities (auditory, visual, somatosensory) that address single parameters of gait, such as step frequency or step amplitude.10 Attentional strategies, such as instructions to increase step length, offer an alternative to external cues; they rely more on cognitive mechanisms of motor control and are internally generated.9, 18, 19, 20, 21 Research has generally focused on using a single cue modality. Visual and attentional strategies appear to have a greater effect on step amplitude and walking speed than do rhythmic auditory cues when they are tested in a laboratory situation with subjects doing simple tasks.1, 6, 9, 18, 19, 20, 21, 22 Not withstanding the benefits of using cues to facilitate gait, their use in facilitating the performance of functional activities and in complex environments has received less attention. People with PD have difficulty performing dual tasks, argued to result from attentional overload and inability to use automatic movement control.23, 24, 25, 26 Morris et al9 found that constant monitoring was required for attentional strategies to retain their effectiveness, which is difficult to do in the real world and during dual-task performance. Canning,22 however, found that attentional strategies were effective during dual tasks when subjects were given explicit instructions to direct their attention to gait. In contrast, rhythmic auditory cues improve gait during dual and multiple tasks involving both motor and cognitive tasks conducted in the home environment,12 possibly because they impose less attentional demand. Deficits in executive function in PD subjects may exacerbate dual-task difficulties because they will have an effect on the appropriate allocation of attention to gait during dual- and multi-tasks.26, 27 Cueing strategies therefore must be effective under dual-task conditions in the context of complex environments where attentional demands increase,12 and must take into consideration cognitive difficulties. Combining a rhythmic auditory cue to prompt step frequency with a spatial cue to normalize step amplitude so to address both the temporal and spatial components of gait in people with PD may provide an alternative to address issues of generalization.12 The external cue may reduce the need for constant monitoring by prompting a person to focus on step amplitude, thus overcoming limitations of executive function and increased attentional requirements. In this exploratory study, we asked the following questions: (1) can people with PD effectively combine a rhythmic auditory cue with an attentional strategy; (2) does the combination cue provide greater benefits than the attentional strategy alone; and (3) can these cues be used to improve gait when performing a dual task? Methods  Participants We used a convenience sample of 15 people with idiopathic PD (PD group) (6 men, 9 women; mean age, 68.83±3.30y) and a control group of 12 healthy participants (5 men, 7 women; mean age, 71.50±2.58y) matched for age (table 1). The Sunderland local research ethics committee in the United Kingdom granted ethical consent for the study, and all participants gave their informed written consent. We used the following criteria to recruit the PD group: diagnosis of idiopathic PD (by a consultant neurologist with a specialist interest in movement disorders), absence of any other neurologic problem, absence of dementia (score >24 on Mini-Mental State Examination [MMSE]),28 absence of any severe comorbidity likely to affect gait, adequate sight and hearing with glasses and hearing aid, if required (determined informally by ensuring that the subject could read the study information sheet and hear the cueing device), independently mobile indoors without a walking aid, no severe dyskinesias (score >2 on the Modified Dyskinesia Scale),29 or prolonged off periods, and age 80 years or less. Participants who scored greater than or equal to 1 on item 3 of the Freezing of Gait Questionnaire (FOGQ)30 were considered to have freezing as a symptom of PD. The control group participants were fit and well, with no severe comorbidity, an MMSE score of 24 or higher, adequate vision and hearing, and aged 80 years or less. Experimental Design We used a repeated-measures experimental design that compared 3 different cue types under single- and dual-task conditions. We controlled order and practice effects by counterbalancing the walking alone and dual-task conditions, and by randomizing the order of cue presentation (fig 1). Primary Outcome Measures We used the GAITRite mata to collect walking speed (in cm/s), step amplitude (in centimeters), and step frequency (in steps/min). Baseline Measures The participants’ demographic data included sex, age, height, and weight. For the PD group, disease, duration, and severity were recorded and scored with the Hoehn and Yahr Scale, which rates disease progression on a scale of 1 to 531; the Unified Parkinson’s Disease Rating Scale, section III (motor examination), which scores the motor signs of PD including speech, facial expression, tremor, rigidity, bradykinesia, balance, and gait32; the FOGQ, which rates the symptom of freezing according to frequency; situations that cause freezing and severity of freeze30; and the Modified Dyskinesia Scale, which scores the symptom of dyskinesia on a scale of 0 to 4 according to interference with motor tasks.29 Cueing Types Three different cue types were compared: 1.Rhythmic auditory cue:Instructions: “As you walk try to step your feet in time to the beat.” 2.Attentional cue strategy, participants had to think about taking big steps:Instructions: “As you walk try to take big steps.” 3.Combination cue-rhythmic auditory cue associated with taking a big step each time the tone is heard:Instructions: “Take a big step in time to the beat.”Rhythmic auditory cues were given using a prototype cueing deviceb that delivered a rhythmic sound set at 10% below preferred stepping frequency. We calculated each participant’s preferred stepping frequency using the mean of 3 repetitions of a 10-meter walk test. The choice of cueing frequency was made to enable the participants to synchronize with the cue during both the single and dual tasks and also to allow time for a larger step. A previous study10 showed improvements in gait at 10% below preferred stepping frequency. Cueing Conditions A functional task was performed with and without cues in which participants walked under 2 different conditions: (1) single task (walking alone), and (2) dual task (walking and carrying a tray on which there were 2 cups of water). This task was chosen to reflect a functional, ecologically valid activity, and has been used in previous studies.22, 24, 26 Single task Participants were seated in a chair, then stood and walked along an 8-m walkway, stopping when they touched a designated point on a table (fig 2). Dual task Participants were seated in a chair, stood, collected a tray with 2 cups of water placed on it from a table beside the chair, walked along the 8-m walkway carrying the tray and stopped when they placed the tray on a designated point on a table (see fig 2). The water levels in the cups and the positions of the cups on the tray were standardized. Experimental Protocol All testing took place in the human movement analysis laboratory at Northumbria University. Testing lasted approximately 45 minutes, during which the PD group was in the on phase of the medication cycle (1h after medication intake), confirmed through the use of a visual analog scale with which the participants rated their current status on a scale of from “on” to severely “off.” Participants performed 10 trials in both the single- and dual-task conditions (see fig 1), with the order of the tasks being counterbalanced. Three noncued baseline trials (B1) preceded the cueing trials (see fig 1), with a final noncued baseline trial performed after the cueing trials so as to examine the short-term carry-over effects of cue use. Participants performed 2 trials with each cue type in a randomized order. For each trial, participants walked a distance of 8m over a GAITRite mat, which recorded these gait parameters: walking speed, step frequency, and step amplitude, which measures the distance from the center of the heel on 1 foot to the center of the heel of the opposite foot. The mat was positioned in the middle section of the walkway to record the most stable phase of each walk and reduce the effects of acceleration and deceleration. The GAITRite system is a flexible electronic walkway that provides an automated means of measuring the spatial and temporal parameters of gait by using a carpet embedded with sensors that detect footfalls. It has been shown to provide valid and reliable data.33, 34, 35 The carpet is 457cm long, with an active (data recording) area of 366cm, at a data sampling rate of 32.2 to 38.4Hz. Data Analysis We used SPSSc to analyze the data, which were examined for distribution using the Shapiro-Wilk W test. All data were normally distributed and therefore we used parametric statistics for analysis. We used a mixed-design, repeated-measures analysis of variance to compare walking speed, step amplitude, and step frequency for the effect of participant type (PD, control), cue type (auditory, attentional, combination), and task type (single, dual task). We described the data as the mean values for each trial type. In addition, we calculated the interference effect on gait of a dual task with and without cues. This was expressed as the mean percentage difference between single and dual tasks for each trial type, as shown in the equation: For walking speed and step amplitude, a negative response indicates reduced performance during the dual-task condition and a positive response indicates improved performance; this is reversed for step frequency. We used pairwise comparisons with Bonferroni adjustments to identify significant differences between trials. Two-tailed tests with a P value of .05 or less were considered statistically significant. Results PD and control participants were matched for height (P=.67) and sex, however, there was a small but significant difference between the ages of the groups (P=.045), with the control participants being a mean of 2.67 years older than the PD subjects. There was no significant difference in scores on the MMSE (P=.37), with all participants scoring above the cutoff of 24, which indicates an absence of dementia. The mean duration of the PD group’s disease was 6.15±3.16 years; Hoehn and Yahr ratings are presented in table 1 and indicate mild-to-moderate disease severity. Comparison of PD and Control Group There was a significant main effect of participant type in walking speed (F=25.65, P<.001), step amplitude (F=29.13, P<.001), and step frequency (F=4.18, P=.046), with the PD group walking consistently slower, with smaller steps, and a reduced step frequency across all conditions. There was no interaction effect of participant type and cue type between the 2 groups, which suggests that although PD participants walked away more slowly and with smaller steps, they responded in a similar way to cue types and conditions. Therefore, the following description of the results will only refer to the PD group unless otherwise stated. Table 2 lists the values for the controls for comparison purposes. Comparison of Cue Modality There was a significant main effect of cue type for all parameters (walking speed, F=48.70, P<.001; step amplitude, F=232.60, P<.001; step frequency, F=44.21, P<.001), which indicates that cue modalities differed significantly from each other. Figure 3 shows the changes in each parameter relative to the noncued B1 trial (expressed as the percentage mean difference). For walking speed and step amplitude, a negative value indicates that gait performance is reduced with the cue, compared with the noncued trial; a positive response indicates that walking improves with the cue. A negative value for step frequency indicates an improvement. Walking speed During the single-task condition, the attentional cue type resulted in a significant increase in speed compared with baseline (P<.001) of 10.68cm/s, which represents a 9.5% improvement compared with noncued gait. The combination cue type was equally effective (P=.013), but showed no further increase from the addition of the rhythmic auditory cue (fig 3A). The auditory cue reduced speed during single-task gait but this change was not significant. In the dual-task condition, there were similar significant increases for attentional (P=.037) and combination (P=.028) cue types, with an increase in speed of approximately 8.5 to 10cm/s. The auditory cue type increased speed by about 2%, which was not significant. Step amplitude During the single-task condition, there was a significant increase in step amplitude of approximately 10cm, representing a 15% increase, for the attentional and combination cue types (P<.001, P<.001) (fig 3B), with no differences between them. Although the auditory cue caused a small increase in step amplitude, it was not significant. The same response was seen in the dual-task condition, with significant increases in step amplitude of 9 to 10cm, an improvement of 15% to 17% for the attentional and combination cue types (P<.001, P<.001), and a small nonsignificant increase for the auditory cue type. Step frequency During the single-task condition, only the attentional cue type caused a significant (P=.042) reduction in step frequency of 6.15 steps/min or 6% (fig 3C). The combination and auditory cue types caused a slightly smaller reduction of about 5 steps/min, which was not significant. In the dual-task condition; however, both the attentional and combination cue types caused significant reductions of 6%, to 10 steps/min—a decrease of about 6% to 10% (P<.001, P=.009). The auditory cue type again caused a nonsignificant reduction of about 5 steps/min. Interference Effect on Gait There was a significant main effect of task type on walking speed and step amplitude (F=5.47, P=.023; F=11.49, P=.001), with dual-task performance always being significantly reduced compared with single-task performance (see table 2). This was not so with step frequency, where there was no significant difference between single and dual tasks. There was no significant interaction effect of task type (single, dual task) by cue type, indicating that the pattern of response during cued and noncued trials for each condition (single, dual task) was the same for all gait variables (speed, step amplitude, step frequency). Cues reduced the interference between a single and a dual task in speed, step amplitude, and step frequency when compared with noncued trials (see table 2, interference effect), which was approximately a 7% to 9.5% reduction in all parameters; however, the reduction was not significant. Do Cues Normalize Gait to Control Levels? To see if gait parameters of the PD group were normalized to control values in the single and dual tasks, we compared each cue modality for the PD group with the controls’ baseline values (walking at preferred speed without cues in the single and dual tasks) (see table 2). Walking speed was normalized with the attentional (P=.13) and combination (P=.183) cue types to the level of the control group at baseline in the dual-task condition only. Step amplitude, however, was normalized in both the single- and dual-task conditions with the attentional (P=.566, P=.063) and combination (P=.707, P=.175) cue types. Step frequency did not differ significantly from control subjects and this did not change with cues. Immediate Carry-Over Effects of Cueing When cues were removed in the final (B2) noncued trial (see fig 3), a small improvement remained in all gait parameters in the single and dual tasks. This was significant for step amplitude in the dual task, which remained increased compared with B1 (P=.038) and indeed, was normalized to control values. Discussion Our main findings in this study were that subjects could use an attentional strategy to increase step amplitude during both a single and a dual task and this strategy also normalized walking speed. In addition, they could combine a rhythmic auditory cue with an attentional strategy during single and dual tasks and this was as effective as the attentional strategy alone, but not more so. The attentional strategy and the combination cue resulted in large improvements in both walking speed (≈10% improvement) and step amplitude (≈15% improvement), considerably higher than the 1.03cm/s improvement in walking speed and 2cm improvement in step amplitude suggested to have a clinical effect above the normal variance in gait of people with PD.36 The rhythmic auditory cue, when delivered on its own at 10% below preferred stepping frequency, improved step amplitude but the improvement was not significant. Effect of Cue Modality During Walking (single task) As expected, the attentional strategy resulted in significant improvements in walking speed, step amplitude, and step frequency in the single task, normalizing gait parameters of the PD group. This supports previous findings that people with PD can effectively modify their gait pattern during a single task when given appropriate instruction to do so.9, 18, 19, 20, 21, 22 Our main purpose in this study was to determine whether people with PD could combine a rhythmic auditory cue with an attentional strategy, and to see if the combination was as, or more, effective as the attentional strategy. Our results show that participants successfully combined the cue types and it was equally effective in normalizing walking speed and step amplitude, but it was not superior. This is in contrast to results of a previous study14 that investigated the effect of combining a rhythmic auditory cue at 25% above preferred stepping frequency with a visual cue (stripes on the floor) and found that the significant improvement in step amplitude with the visual cue alone was lost when the cue types were combined. We suggest that the attentional demand of using 2 different external cue types together resulted in gait interference. Interestingly, we did not find this, which suggests there was no increased attentional demand when this combination of cues was used. The combined cues did not provide additional benefit over the use of the attentional strategy alone. The choice of a cueing frequency of 10% below preferred stepping rate might be important here. While the rhythmic auditory cue caused a small increase in step amplitude and a small reduction in both walking speed and step frequency, none of these changes reached significance. We chose this cue frequency because subjects had to synchronize with the cue during a dual task as well as while walking alone; therefore, safety was a consideration. When rhythmic auditory cues are delivered at baseline or higher, there are improvements in walking speed,12 but not in step amplitude.1, 3, 5, 14 Although the effect of the combination cue was not greater than the attentional strategy alone, the effect of increased cueing frequency to baseline or above may be that it results in additional benefits. The effect of cue frequency on the combination cue and the identification of the optimal cue frequency for dual-task activity therefore require investigation. Effect of Cue Modality During a Dual Task A range of secondary tasks have been used in dual-task studies that include secondary cognitive or motor tasks.9, 22, 26, 37 We chose a task that was both functional and familiar to the participants and therefore had greater ecologic validity. O’Shea et al25 suggested there is a critical level of task complexity that must be met for interference to occur. The relatively simple dual-motor task we used resulted in a significant deterioration in walking speed and step amplitude in the PD group during the noncued baseline trials and therefore it can be said to have reached a critical level of difficulty. This also agrees with previous studies that have reported an interference effect on gait of a secondary motor task.23, 24, 25, 26, 38 Furthermore, none of the cue strategies significantly increased gait interference, which indicates that subjects could attend to both the task and the cue without further deterioration in gait, suggesting the cues did not increase attentional demands further. The attentional strategy resulted in significantly improved walking speed and step amplitude and normalized gait in the PD group in the dual task. Previous studies have reported reduced effectiveness of attentional strategies during dual tasks because constant vigilance is required.9 Canning22 found that when participants were asked to direct attention to a specific aspect of gait, attentional strategies were effective during a tray-carrying task similar to the task in our study. Importantly, however, the measurement of gait by Morris et al9 was covert and the participants perceived no need to remain vigilant to the attentional strategy, which perhaps is more reflective of a functional situation. In the present study, participants knew that their gait was being measured, which may have heightened their arousal and made it more likely that they continued to use the attentional strategy during the dual task. The effect of executive dysfunction on cue use during dual tasks is unknown. It is possible, however, that the combination cue may provide a prompt that a person simply responds to by directing attention to gait without the need for constant vigilance. This method might be a practical alternative for patients who find attentional strategies difficult to use in a functional setting because of distractions in the environment, or problems with executive function. The rhythmic auditory cue improved gait during the dual task, but this was not significant. This is in contrast to results of previous studies by our group, where there were significant increases in step amplitude with rhythmic auditory cues during dual and multitask performances in the home.12 This, however, may have been the result of the cue frequency we used, as discussed previously. The present study tested the immediate response to cues and also showed a short-term carryover effect on step amplitude in the dual task. A period of training with rhythmic auditory cues has been shown to improve walking performance.2, 7, 22, 39, 40, 41, 42 Retention of the effect of an attentional strategy that instructs subjects to increase step size depends on disease severity, with more severe subjects reverting back to baseline measures despite significant improvements made at the time of training with the strategy.19 This may be the result of increased executive and attentional dysfunction that is seen in more severe disease stages, which may make it less likely that subjects will remember to use the strategy they have been taught if they are not prompted to do so. This may be a promising role for strategies such as the combination cue, which has the external element to aid its use in more functional settings. The effect sizes seen here with the attentional strategy and the combination cue suggest a potential for further improvement with training; the question remains whether the effects of either cue type can be sustained. Study Limitations This study involved a small sample of PD and control participants, which limits the ability to generalize its results to a wider population. There was a small but significant difference in the ages of the 2 groups, with the controls being just over 2 years older. This fact may reduce the differences between the groups inasmuch as walking speed and step amplitude are known to be reduced with normal aging, as does dual-task ability; this, in addition to the small number of people studied, should lead to a cautious interpretation of the data. The small number of people with PD also prevented further subgroup analysis, for example, discriminating freezers from nonfreezers. Although no participants experienced freezing during the phase of the walk that was analyzed, freezing may still be a factor that alters response to cues. The testing environment of the laboratory also reduces transfer of these findings. A more complex dual task would have made it possible for us to more fully evaluate the attentional cost of the cueing strategies because the task we used does not necessarily transfer to more complex tasks such as crossing a busy street. All participants were tested in the on phase of their medication and little is known about the effects of cues on gait in the off medication phase. A planned further study will involve a larger sample in the home environment, which should address these issues. This study presents the effect of cues on mean gait values. There is increasing evidence that variability of gait parameters also needs to be investigated to fully evaluate the attentional cost of cues.43 Conclusions This study has extended the findings of previous work by demonstrating that an attentional strategy and a combination cue strategy were equally effective in improving walking speed and step amplitude during both single and dual tasks. The combination cue strategy appears to offer an effective and practical alternative for managing gait deficits in Parkinson’s disease, in addition to the use of rhythmic auditory cues or attentional strategies alone. Perhaps it has potential for use in situations of increased attentional demand, or where there are problems of executive dysfunction. Supplier Acknowledgment We thank David Burns, MD, and his team for their help and support with recruitment of subjects for the study. References 1. 1Morris ME, Iansek R, Matyas T, Summers JL. The pathogenesis of gait hypokinesia in Parkinson’s disease. 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a School of Health, Community and Education Studies, Northumbria University, Newcastle, UK b Faculty of Movement and Rehabilitation Sciences, Katholieke Universiteit, Leuven, Belgium.  Reprint requests to Katherine Baker, BSc, School of Health, Community and Education Studies, Northumbria University, Rm H110, Coach Lane Campus East, Coach Ln, Newcastle upon Tyne, NE7 7XA, UK
Supported by the Association of Physiotherapists Interested in Neurology, UK. 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 author(s) or upon any organization with which the author(s) is/are associated. PII: S0003-9993(07)01454-2 doi:10.1016/j.apmr.2007.07.026 © 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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