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Published in final edited form as: Arch Phys Med Rehabil. 2024 Aug 24;105(12):2262–2268. doi: 10.1016/j.apmr.2024.08.007

Increased Auditory Dual Task Cost during Gait Initiation in Patients Adults with Persistent Concussion Symptoms

Kelsey N Bryk 1,2, Scott Passalugo 1,2, Li-Shan Chou 3, Darcy R Reisman 2,4,5, Jocelyn Hafer 1,2, Jennifer A Semrau 1,2,5, Thomas A Buckley 1,2,5
PMCID: PMC11620944  NIHMSID: NIHMS2018909  PMID: 39187006

Abstract

Objective:

To compare Dual Task Cost (DTC) during Gait Initiation (GI) between a population of patients with Persistent Concussion Symptom (PCS) and age-matched healthy participants.

Design:

Cohort Study.

Setting:

University research center.

Participants:

A cohort sample including 15 PCS (43.9 ± 11.7 y.o., 73.3% Female) and 23 age-matched control (42.1 ± 10.3 y.o., 65.2% Female) participants.

Interventions:

Participants were tested on a single occasion where they performed 5 trials of ST and 5 trials of DT Gait Initiation with 12-camera motion capture and three force plates.

Main Outcome Measures:

The dependent variables of interest were the DTC for the Center of Pressure (COP) displacement and velocity during the Anticipatory Postural Adjustment (APA) phase, the COP-Center of Mass (COP-COM) separation, and the response accuracy during the auditory cognitive tasks.

Results:

There were significant group differences with worse DTC for the PCS participants A/P displacement (PCS: −37.5 ± 22.1% and Control: −9.7 ± 39.2%, p=0.016, d=0.874), APA M/L velocity (PCS: −34.8 ± 28.8% and Control: −17.0 ± 40.21%, p=0.041, d= 0.866), and the peak COP-COM separation (PCS: −7.3% ± 6.7% and Control: 0.6 ± 6.5%, p=0.023, d=1.200). There were no significant group differences in the APA A/P Velocity (PCS: −38.8 + 33.1% and Control: −19.8 + 43.9%, p=0.094), APA M/L Displacement (PCS: −34.8 ± 21.8% and Control: −10.6 ± 25.3%, p=0.313), or cognitive task performance (PCS: −2.7 ± 10.8% and Control: −0.2 ± 4.3%, p=0.321).

Conclusion:

PCS participants had greater (worse) DTC during both the planning and execution of the task with large effect sizes (d>0.80). The PCS participants also utilized a posture-second strategy whereby attentional resources were inappropriately allocated to the cognitive task. These deficits may challenge patient’s ability to complete activities of daily living and limit their functional independence.

Keywords: Mild Traumatic Brain Injury, Balance, Postural Control


Concussions are complex neurological injuries which affect diverse neurophysiological systems resulting in an array of signs and symptoms.16 In collegiate student-athletes, most concussed patients have fairly rapid symptomatic recovery and within a month over 90% will be clinically recovered.1 Conversely, in the general adult population persistent symptoms are far more common and 18–54% were still symptomatic at 3 – 6 months post-injury.7 These ongoing symptoms (e.g., headache, fatigue, vestibular-ocular deficits) are referred to as either post-concussion syndrome or more the contemporary term, persistent concussion symptoms (PCS).8,9 PCS is particularly disruptive in middle aged adults, compared to adolescent/young adult student-athletes, as it likely involves lost or reduced work time with associated lost income, poses challenges to family dynamics and/or parenting children, as well as reduced community engagement and quality of life.7,10,11 While cognitive deficits have been routinely identified in PCS patients, the effect on postural control has received limited attention.1117 Healthy and appropriate postural control is critical to maintain mobility, navigate the community, have functional independence, and maintain a low fall risk profile.

The Balance Error Scoring System (BESS) has been routinely utilized to identify postural control deficits;18 however, this test has extensive psychometric limitations (e.g., low sensitivity, poor test-retest reliability) and only assesses the ability to maintain quiet upright stance.1923 In an adult PCS population, BESS scores are within a standard deviation of healthy collegiate student-athletes, suggesting limited discriminatory value.24,25 Conversely, gait studies have consistently identified persistent postural control deficits beyond concussion clinical recovery particularly when a cognitive task is incorporated (termed Dual Task: DT).26,27 In middle aged adult patients with PCS, DT gait is associated with larger decreases in gait speed, shorter step lengths, and decreased cognitive accuracy, broadly considered to be a conservative gait strategy, compared to healthy age matched adults.1217 Furthermore, Dual Task Cost (DTC), the worsening of performance during DT compared to ST trials, can also help elucidate strategies or task priorizations.12 Both acute and chronic brain injured adult patients experience persistent DTC deficits during steady state gait; however, gait initiation (GI), the ability to plan, self-initiate, and control a step during a transitional movement, is a more challenging task to the postural control systems.28

Gait initiation (GI) is a complex movement that occurs when a person transitions from quiet upright stance to steady-state gait.29,30 This transitional movement consists of both locomotor and anticipatory postural adjustments (APA) components with the APA representing the planning and preparation for a step which is likely controlled by the supplementary or premotor area.31,32 During the locomotor component, the most challenging aspect is the peak separation between the center of mass (COM) and center of pressure (COP) which occurs just prior to the heel strike of the swing limb at the end of the single support phase.28 Both the APA COP displacement and COM-COP separation have effectively discriminated patients across a wide range of neurological conditions, including acute and subacute concussion, and these measures have the potential to further elucidate the neurological underpinnings of PCS.29,3238

Impaired DT gait is well documented in adults with PCS ; however, DT GI may provide additional insights postural control in these patients. Therefore, the purpose of this study was to assess DTC during GI in a population of PCS patients compared to age matched healthy participants. We hypothesize PCS participants will have greater DTC (worse performance) in the APA COP displacement and velocity as well as peak COP-COM separation compared to healthy matched participants.

METHODS

Participants

We recruited 38 participants; 15 adults with PCS and 23 healthy control participants from the local community. (Table 1) The inclusion criteria for the adult participants with PCS was a health care provider, external to the research team, referral of a patient being actively treated for PCS following a medically diagnosed concussion/mTBI and with current symptoms at least three months following a diagnosed concussion. The inclusion criteria for both groups was 25 – 65 years old and the control participants were matched based on age (+/− 5 years), sex (self-reported by the participant), height and weight within 10%, and the control participants did not have a diagnosed concussion within the last 12 months. The exclusion criteria for both groups was self-reported history of moderate to severe mTBI, blast-induced mTBI, self-reported neurological disorder, substantial lower body orthopedic injury, uncorrected vision, visual impairment/disorder, or other condition which limited their mobility. Recruitment occurred from Summer 2019 through Fall 2020 and 11 participants (PCS: 2, Control: 9) were assessed during the early COVID pandemic time frame, but there were no significant differences between pre- and during COVID outcomes. All participants provided written and oral informed consent prior to participation as approved by the institution’s IRB.

Table 1.

Participant Demographics and Anthropometrics.

PCS (n=15)
Mean ± SD
Control (n=23)
Mean ± SD
Group Differences
(p-value)
Sex (M/F) 4/11 8/15 0.599
Age (years) Female: 41.3 ± 11.2
Male: 51.0 ± 11.6
Female: 42.3 ± 10.3
Male: 40.2 + 11.1
0.626
Height (m) Female: 163.5 ± 8.6
Male: 177.5 ± 8.3
Female: 165.8 ± 6.7
Male: 174.1 ± 5.8
0.559
Weight (kg) Female: 77.2 ± 16.7
Male: 93.9 ± 16.9
Female: 76.4 ± 21.6
Male: 79.8 ± 11.4
0.601
*Depression Female: 7/11 (63.6%)
Male: 2/4 (50%)
Female: 2/15 (13.3%)
Male: 1/8 (12.5%)
0.002
*Anxiety Female: 8/11 (72.7%)
Male: 2/4 (50%)
Female: 1/15 (6.7%)
Male: 1/8 (12.5%)
0.001
Concussion History Female: 2.2 ± 2.0
Male: 6.5 ± 5.3
Female: 0.3 ± 0.6
Male: 1.0 ± 1.2
0.153
*Rivermead Symptom Score Female: 33.6 ± 12.4
Male: 37.8 ± 18.4
Female: 5.7 ± 5.8
Male: 5.9 ± 5.8
<0.001
*

The PCS participants had a significantly high Rivermead Symptom Score than the Control Participants with a large effect size (p<0.001, Cohen’s d = 2.72) as well higher rates of both self-reported Depression (p=0.002) and Anxiety (p=0.001).

Instrumentation

The GI trials were collected along a 10-m walkway and the participants were outfitted with 46 retroreflective markers creating a 15-segment full body kinematic model consistent with a six degree of freedom model. The kinematic data was collected at 120 Hz using a Qualisys 12-camera motion capture system (Qualisys, Gothenburg, Sweden). Ground reaction forces were recorded at 1200 Hz using 3 adjacent force plates (AMTI Inc, Watertown, MA, USA). Auditory stimuli were presented using the Blue Tiger Elite Bluetooth headset (Blue Tiger USA, Stafford, TX, USA), a wireless headset with an attached microphone that was placed directly in front of the participant’s mouth.

Procedures

To confirm the presence of post-concussion related symptoms in PCS patients, each participant completed the Rivermead Post-Concussion Symptoms Questionnaire (RPSQ); a total symptom score ranges from 0 – 64, with a higher value indicating more severe symptoms.39 To ensure all inclusion and exclusion criteria were met, participants also completed a reliable health history questionnaire (ICC: 0.92) to self-report information regarding concussion history, lower body injury history, as well as general health questions including prior medically diagnosed history of anxiety or depression.40

Prior to performing the GI task, participants completed a ST cognitive assessment, the auditory Stroop test which been used in concussion related DT gait studies4144 and is reliable during DT gait (e.g., Cronbach alpha :0.94, ICC: 0.94 (95% CI: 0.83 – 0.98).41 The auditory Stroop test consisted of 4 auditory stimuli: the words “High” and “Low”, each spoken in either a high or low pitch and the participant had to verbally identify the pitch of the word regardless of the word spoken. The order of auditory stimuli was pseudo-randomized for each trial (to ensure that all 4 auditory stimuli were presented an equal amount), and this order was kept consistent for all participants.

For the GI trials, the participants began each trial standing barefoot and comfortably with their feet about shoulder width apart and the foot position was marked on the force plate and each trial started from the same position. The initial swing limb was self-selected and five trials of both ST and DT with the same initial swing limb were collected.29,30,33,36 The ST GI trials consisted of the participant initiating movement in response to a verbal cue and walking forward for at least five meters. During the DT trials, participants performed the same motor task while simultaneously performing the auditory Stroop task and initiated movement in response to the first verbal challenge. Participants were not given instructions to prioritize either motor or cognitive performance, but to complete the tasks to the best of their ability.

Data Analysis

Gait initiation is classically divided in three sections based on 4 landmarks.29,33 (Figure 1) The APA phase, a primary outcome measure is this study, was defined as the displacement and velocity between movement imitation and the most lateral movement of the COP. Specifically, movement initiation was determined first by the change in COP displacement and confirmed by changes in the vertical ground reaction force with a threshold of 2 standard deviations away from the mean of the first 0.5 seconds of the trial.29 The COP is then shifted posteriorly and laterally towards the initial swing limb and the maximum lateral movement (closest point to the initial swing limb) represents the GI APA phase. As the heel leaves the ground, the COP then shifts from the initial swing to initial stance limb which represents the Transitional Phase which ends with COP under the initial stance limb and in single support. Finally, the Locomotor Phase is represented by the anterior displacement of the COP under the initial stance limb and ending when the foot leaves the ground. As the purpose of this study was to investigate movement planning and dynamic balance, the outcome measures were the A/P and M/L displacement and mean velocities of the COP during the APA phase.29,33,35,36

Figure 1. Gait Initiation Exemplar.

Figure 1.

In this example, the right foot was the initial swing limb.

The COP-COM resultant displacement is calculated at the peak which occurs just prior to the heel strike of the initial swing limb.28 The single outcome measure is the resultant peak displacement between the COM and COP during the initial step. (Figure 1)

The cognitive outcome of interest was the mean percentage correct on the Auditory Stroop test.

The dual task cost (DTC) was calculated for each variable and is the outcome measure of interest. The DTC is the percentage that represents the reduced motor task performance which occurs when a cognitive task is added to movement and is calculated as (((DT Outcome – ST Outcome)/ST Outcome) * 100). A negative value reflects greater DTC (worse performance), a positive value reflects better performance during the DT, and a value of zero reflects no difference between ST and DT performance.

Statistical Analysis

Descriptive statistics were calculated for participant’s demographic and anthropometric measures and compared between groups with an independent samples t-test (continuous variables) or chi-square analysis (categorical variables). Additionally, the ST and DT outcomes are presented with means and standard deviations, but not further analyzed. (Table 2) Because both self-reported Depression and Anxiety differed between groups, they were included in the analysis as co-variates. (Table 1) All outcome measures were assessed for normality using an Anderson-Darling test and the DTC for APA A/P Displacement and Velocity, APA M/L Velocity were not normally distributed while APA M/L Displacement, resultant COP-COM separation, and Auditory Stroop Test were normally distributed. The Dual Task Cost (DTC) was compared between groups with either a Wilcoxon Test (not normally distributed) or a one-way ANOVA (normally distributed). Cohen’s d effect sizes were calculated on all outcome measures and were interpreted as small (<0.20), medium (0.20 – 0.79), or large (>0.80). Statistical significance was set a priori at α level of 0.05. A small sample size of males, particularly in the PCS group, precludes subsequent analysis of sex differences.

Table 2.

Descriptive Data for ST and DT Outcome Measures.

ST PCS
Mean + SD
(95% CI)
DT PCS
Mean + SD
95% CI
ST Control
Mean + SD
95% CI
DT Control
Mean + SD
95% CI
APA A/P Displacement (cm) 3.83 ± 1.73 (2.87 – 4.78) 2.26 ± 1.07 (1.67 – 2.85) 3.86 ± 1.11 (3.37 – 4.34) 3.37 ± 1.56 (2.70 – 4.05)
APA M/L Displacement (cm) 3.54 ± 0.91 (3.04 – 4.05) 2.35 ± 1.1 (1.75 – 2.94) 3.96 ± 1.62 (3.26 – 4.66) 3.45 ± 1.48 (2.81 + 4.09)
APA A/P Velocity (cm/sec) 18.6 ± 10.5 (12.8 – 24.4) 9.8 ± 4.3 (7.4 – 12.2) 17.0 ± 6.8 (14.0 – 19.9) 12.1 ± 4.6 (10.1 – 14.1)
APA M/L Velocity (cm/sec) 16.3 ± 2.6 (14.8 – 17.7) 9.9 ± 4.4 (7.5 – 12.3) 17.6 ± 9.3 (13.5 – 21.6) 13.8 ± 7.8 (10.5 – 17.2)
COP-COM Separation (cm) 22.2 ± 2.3 (20.9 – 23.5) 20.6 ± 2.8 (19.0 – 22.2) 22.4 ± 2.6 (21.3 – 23.5) 22.5 ± 2.3 (21.5 – 23.5)
Auditory Stroop Performance (%) 97.4 ± 4.6 (94.8 – 100) 94.9 ± 11.6 (88.5 – 101.3) 97.6 ± 5.7 (95.0 – 100) 97.1 ± 3.8 (95.5 – 98.9)

RESULTS

Motor Task Performance

There were significant group differences with greater (worse) DTC for the PCS participants for the APA A/P displacement (PCS: −37.5 ± 22.1% and Control: −9.7 ± 39.2%, z=2.390, p=0.016, d=0.874) (Figure 2) and slower APA M/L velocity (PCS: −34.8 ± 28.8% and Control: −17.0 ± 40.21%, z=2.031, p=0.041, d= 0.866). (Figure 3) There was also a significant group difference in the peak COP-COM separation with greater (worse) DTC for the PCS participants (PCS: −7.3% ± 6.7% and Control: 0.6 ± 6.5%, F=5.787, p=0.023, d=1.200). (Figure 4)

Figure 2. APA Phase A/P Displacement by Task.

Figure 2.

There was a significant difference in DTC (p=0.016, d=0.874) between groups. The PCS group displacement decreased by 1.5 cm (ST: 3.8 ± 1.7 cm and DT: 2.3 ± 1.1 cm) while the Control group displacement decreased by 0.5 cm (ST: 3.9 ± 1.1 cm and DT: 3.4 ± 1.6 cm).

Figure 3. APA M/L Velocity by Group.

Figure 3.

There was a significant difference in DTC (p=0.041, d= 0.866) between the groups. The PCS group decreased APA M/L velocity by 6.4 cm/sec (ST: 16.3 ± 2.6 cm/sec and DT: 9.9 ± 4.4 cm/sec) while the control group decreased by 3.8 cm/sec (ST: 17.6 ± 9.3 cm/sec and DT: 13.8 ± 7.8 cm/sec).

Figure 4. Peak COP-COM Separation by Task.

Figure 4.

There was a significant difference in DTC (p=0.023, d=1.200) between groups. The PCS group decreased COP-COM separation by 1.6 cm (ST: 22.2 ± 2.3 cm and DT: 20.6 ± 2.8 cm) while the control group increased by 0.1 cm (ST: 22.4 ± 2.6 cm and DT: 22.5 ± 2.3 cm).

There were no significant DTC group differences in the APA A/P Velocity (PCS: −38.8 ± 33.1% and Control: −19.8 ± 43.9%, z=1.668, p=0.094, d=0.489) or APA M/L Displacement (PCS: −34.8 ± 21.8% and Control: −10.6 ± 25.3%, F=1.055, p=0.313, d=1.024).

The ST and DT outcomes are provided as Means and Standard Deviations are presented in Table 2.

Cognitive Performance

There was no group difference in DTC for the Auditory Stroop task (PCS: −2.7 ± 10.8% and Control: −0.2 ± 4.3%, F= 1.012, p=0.321, d=0.304).

DISCUSSION

Impairments in dynamic postural control are present in adults with PCS across a variety of gait related tasks,1215,45 and herein we assessed postural control during the inherently unstable transitional GI task to further elucidate motor planning and execution. The primary finding of this study was increased DTC (worse performance) in PCS participants during components of both the task planning (APA phase) and execution (COP-COM separation). The large effect size (>0.80) suggest that PCS patients have meaningful underlying motor planning deficits when an auditory cognitive task is incorporated.

Gait initiation challenges the postural control systems to maintain dynamic balance while planning and executing a transition from quiet upright stance to rhythmic locomotion.29,30,33,34 The APA phase COP displacement and velocity is the primary mechanism for initial step momentum with reductions being considered a motor planning deficit46 and have been observed across diverse neuropathological patients.29,30,3237 Herein, the PCS participants posterior COP displacement and lateral velocity were reduced by 34 – 38% when a cognitive challenge was incorporated thus limiting the necessary momentum to safely initiate gait;47,48 however cognitive performance DTC did not differ between groups. This suggests the PCS participants used a “posture-second” strategy whereby the cognitive performance was prioritized at the expense of motor performance.49 The adoption of a posture-second strategy is dependent upon the individual’s motor and cognitive capacity as well as the perceived complexity of the motor and cognitive challenges.50,51 As auditory Stroop DT challenges involve a competition for limited postural and cognitive attentional resources, the PCS participant’s posture-second strategy may reduce their ability to respond to perturbations and elevate their fall risk.50,52 Auditory processing is highly common during activities of daily living (e.g., engaging in a conversation, interpreting auditory environmental cues) and these impairments may also underlie the recent report of elevated fall risk in individuals with prior history of head injury.53 This finding suggests that health care providers treating PCS patients may need to incorporate DT challenges as well as integrating fall risk reduction strategies into rehabilitation programs.

Once the movement is planned and initiated, the transition from quiet stance to rhythmic locomotion includes a destabilizing transition which requires dynamic balance.28 The peak displacement between the COP and COM quantifies this instability and reduced displacements suggest a conservative posture control strategy.26 This strategy may be utilized by the patient to preserve stability and reduce demand on the neuromuscular system or mechanically to reduce the momentum generated during the APA phase of GI.5456 While control participants maintained consistent separation displacements, the PCS participants reduced COP-COM separation by >7% with a large effect size (d=1.20) when the auditory cognitive task was added. (Figure 4) Previous studies of GI in concussion and PCS populations have focused on COP displacement and initial stepping characteristics,33,35,36,38 however reduced COP-COM separation has been noted during both ST and DT steady state gait tasks acutely and for up to a month post-injury.26 The posture-second strategy during the APA phase reduces the forward momentum during the locomotor phase and therefore the PCS patients may restrict their COP-COM separation to minimize threats to their dynamic balance. The underlying mechanism remains to be elucidated, but a reduced COP-COM moment arm lessens the neuromuscular challenges to the postural control system thus potentially resulting in a more conservative strategy. Subsequent studies should incorporate assessment of participants lower extremity strength to further elucidate this relationship.57

One key aspect of this study was the focus on the DTC as opposed to either ST or DT performance independently. In middle-aged adults with PCS, ST gait did not successfully discriminate between groups in several studies15,58 and herein both groups performed similarly during ST trials. (Table 2) Conversely, both DT gait and more challenging ST motor tasks (e.g., turning, obstacle avoidance) have identified reduced postural control in PCS patients.13,45 The focus on DTC is particularly important as increased (worsening) DTC may predict cognitive decline and future falls59,60 and elevated fall risk has been identified in patients with prior brain injury,53 thus the clear need for specific DT postural control rehabilitation for individuals with persistent brain injury related symptoms.

Study Limitations

The participants in this study had a wide range of symptom duration (110 – 1,315 days) and symptom burden (Rivermead: 15 – 63); however, these ranges are common in PCS studies1317 but limits extrapolation of the study. As is also common amongst PCS studies in the general public,1217 pre-injury performance data is not available; however both groups’ single task motor and cognitive performance were generally consistent with prior GI studies and the PCS participants DT performance was similar to aging and neuropathological populations.29,30,3336 The specific diagnostic criteria for PCS remains controversial (i.e., was removed from DSM-IV for lack of diagnostic specificity)61 and PCS-like symptoms are commonplace in healthy young adults.62 The inclusion criteria for this study was persistent symptoms for at least three months as documented by a health care provider which was supported by the participant’s high Rivermead scores; nonetheless, the lack of a recognized and consistent PCS diagnostic criteria is a limitation. Consistent with gait findings in adults with PCS,4144 the auditory Stroop task identified DTC deficits; however, other cognitive (e.g., working memory, visual Stroop) or non-cognitive (e.g., motor-motor tasks) tasks could further elucidate neurological deficits. We were unable to analyze potential sex differences given the limited enrollment of men, particularly in the PCS group, and this should be explored further in subsequent studies. Finally, 11 participants were assessed during the early phases of the COVID-19 pandemic (2 PCS and 9 control) but task performance was similar between those assessed pre-COVID and during COVID; however, this limited participant enrollment.

CONCLUSIONS

The primary finding of this study was increased (worse) DTC during GI in PCS patients with large effect sizes. Specifically, deficits were noted during both the planning and execution of the task suggestive of a conservative strategy to reduce dynamic balance challenges when an auditory cognitive challenge was included. Furthermore, the PCS participants demonstrated an apparent posture-second strategy whereby attentional resources were inappropriately allocated to the cognitive task. These deficits may reduce the functional independence and quality of life of PCS patients and may be incorporated into rehabilitation programs.

Funding Sources

This project was funded, in part, by a grant from NIH/NINDS (1R0303NS104371).

Suppliers List:

Force plates: AMTI, Inc. Watertown, MA, USA

Motion Capture Cameras: Qualisys, Gothenburg, Sweden

Auditory Tasks: Blue Tiger USA, Stafford, TX., USA

Supported in part by a research grant from the National Institute of Neurological Disorders and Stroke of the National Institutes of Health (grant number NIH/NINDS R03NS104371).

List of Abbreviations

APA

Anticipatory Postural Adjustment

BESS

Balance Error Scoring System

COM

Center of Mass

COP

Center of Pressure

DT

Dual Task

DTC

Dual Task Cost

PCS

Persistent Concussion Symptoms

Footnotes

Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

The study was conducted within the Department of Kinesiology and the Biomechanics and Movement Science program at the University of Delaware.

Disclosures: none.

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