Deficits in sustained and divided attention are common following traumatic brain injury (TBI). The frontal and temporal lobes, which are responsible for working memory and attention,1 are common contusion sites after motor vehicle accidents or blunt trauma2 because of their proximity to bony prominences in the skull. Traumatic brain injury frequently results in impairment of cognition and attention. Attention is a complex cognitive process contributing to arousal, alertness, cognitive speed, working memory, and shifting and dividing attention.3 Divided attention is the ability to respond to multiple stimuli simultaneously,4,5 and this ability is important for real-world function.
Dual tasks are tasks that require divided attention; these tasks pair stimuli such as 2 motor tasks or a cognitive task paired with a motor task (eg, walking while talking). Impairments in divided attention have specifically been linked with deficits in functional mobility in neurological populations, including TBI,1,6 acquired brain injury,7 multiple sclerosis,8 and in elderly9 and healthy adults.10 Indeed, when challenged with dual tasks, individuals with Parkinson's disease demonstrate slower walking speed, shorter strides, increased double-support time, and increased stride-to-stride variability.11 Similarly, environments that challenge the ability to perform combined locomotor and attentional tasks can identify residual deficits following a moderate to severe TBI.12
Automaticity indicates that a level of skill has been achieved in performance of a task such that it requires little to no attention from the performer, to the extent that a second task may be performed without degradation in skill of the primary task. Walking or standing balance, which is typically automatic prior to a brain injury, is more attention-demanding following a TBI. Recent evidence suggests that impaired executive function and attention negatively impact walking function in persons with neurologic disorders.11 Indeed, lower cognitive functioning at admission to inpatient rehabilitation has been associated with lower motor scores at discharge in individuals with TBI.13 However, even in the presence of cognitive dysfunction, tasks such as gait and balance can become skilled and more automatic with sufficient practice.7,14 The use of dual-task training (DTT) may promote recovery of automaticity with basic tasks so that attention can be focused on everyday activities such as navigating an environment or carrying on a conversation without thought to the primary task of walking or balancing.
Evidence from other populations, including elderly adults,15 chronic stroke,16 and Parkinson's disease,17 indicates that cognitive-motor DTT programs improve walking speed and ability to dual-task. Recently, a virtual reality program trained cognitive-motor dual tasks in an individual following a concussion (mild TBI) and showed improvements in dynamic and static balance.18 Similarly, DTT improved balance during cognitive activities to a greater extent than mobility training alone in healthy individuals and those with concussion.10,19 Neuropsychological training programs in subacute and chronic severe TBI focusing on either cognitive dual-tasks20 or working memory21 resulted in improvements in reaction times on visual-auditory dual tasks. However, it is unknown whether DTT in individuals with severe TBI has value for improving safe and functional mobility, or when might be the appropriate time to initiate such DTT.
The purpose of this case study was to determine the feasibility and potential value of incorporating cognitive-motor DTT into physical therapy (PT) interventions for an individual with a severe TBI. We speculated that DTT would be a useful addition to activity-dependent recovery and might contribute to both improved performance on dual-task measures and improved automaticity with locomotor tasks. To our knowledge, the case presented herein is the most severe case described in rehabilitation intervention literature and represents the first report of a cognitive-motor training program for severe TBI.
The study was explained to both the subject of the case study and her family, and informed consent was obtained from her parents, who were her legally authorized representatives.
T.K., a 26-year-old woman with no significant medical history, sustained a severe TBI following a high-speed motor vehicle accident. She lost consciousness and was transported to the emergency department where imaging revealed areas of contusion in bilateral temporal fossae, a subarachnoid hemorrhage in right frontal and parietal lobes, and a small right temporal fossa subdural hematoma. In addition, she presented with a left fixed pupil, and nonoperative left-sided clavicle, sacral, and rib fractures. Prior to this accident, T.K. was a healthy, college graduate with no history of head injury or substance abuse. She was physically active and participated in regular exercise and jogging. T.K. spent 25 days in acute care (postinjury days 0–24) where a percutaneous endoscopic gastrostomy was placed and a tracheostomy performed to protect the airway; her stay was complicated by difficulty weaning from the ventilator (Table 1). She was discharged to a long-term acute care center for 21 days (postinjury days 25–45), where she was able to wean from the ventilator and tolerate trach capping.
T.K. was treated with divalproex sodium (Depakote) for seizures initially but was weaned because of abnormal liver laboratory values and subsequently placed on sertraline hydrochloride, quetiapine (Seroquel), and trazodone for behavioral stabilization and mood control. T.K.'s only other medications were for pain management of the nonoperative fractures (fentanyl, oxycodone), deep vein thrombosis prophylaxis (enoxaparin [Lovenox]), and stool softeners (senna, docusate sodium). Unfortunately, both acute and long-term acute stays occurred outside our medical system, so common prognostic variables (ie, length of coma, Glasgow Coma Scale, intracranial pressure, and pupillary size22) were unknown. However, positive prognosis is associated with a number of other variables, including the number of years of education,23,24 younger age,25 high socioeconomic status, and no prior history of head injury or substance abuse,24 all of which were true for T.K.
T.K. presented to the inpatient rehabilitation center for intense physical, occupational, and speech therapy on postinjury day 46. Her cognitive function was categorized as Rancho IV on the Rancho Los Amigos Level of Cognitive Function scale with left cranial nerve III palsy and no weight-bearing restrictions. The Rancho Los Amigos scale is used with the TBI population to assess overall level of cognition (see Table, Supplemental Digital Content 2, which outlines the Rancho Los Amigos Levels of Cognitive Function, http://links.lww.com/JNPT/A32).26 During evaluation, T.K.'s agitation, restlessness, perseveration, and occasional aggression limited formal assessment of pain and strength. Strength was, therefore, assessed through functional activity; T.K. was able to toe walk (but struggled to keep her left heel off the ground), squat and rise (with assistance), march (with decreased left hip flexion), side step (with reduced left step lengths), achieve quadruped, perform single-leg stance bilaterally, kneel (with bilateral upper extremity support), and half-kneel (but unable to maintain right knee up position). In summary, T.K. presented with mild left-sided weakness and motor delays. T.K.'s sitting balance was rated as “fair,” and she was able to safely maintain unsupported sitting for static but not dynamic activities. Her standing balance was “poor”, requiring both upper extremity assistance and physical assistance of 1 other person for static and dynamic tasks. T.K. scored 9/56 on the Berg Balance Scale, indicating a high fall risk. Transfers from bed to wheelchair/tub/toilet required moderate assistance of 2 persons. Bed mobility required minimal assistance. T.K. required 100% assistance for wheelchair mobility. Walking required moderate assistance of 2 persons for safety. Gait deviations included a Trendelenburg gait pattern (with lean to the left on left swing phase), decreased left step length, and left leg dysmetria during swing phase. T.K. was able to ascend and descend 4 steps with a hand rail and moderate assistance of 1 person using a step-to pattern (Table 2). T.K.'s physical impairments were complicated by her level of cognition and poor short-term memory. While she was able to follow simple motor commands, she required minimal assistance for multistep directions for activities of daily living and maximal cueing to provide verbal responses. Throughout the evaluation, she was impulsive, agitated, perseverative, and easily distracted.
Taken together, T.K.'s main impairments were left-sided weakness and incoordination, poor balance, and reduced cognition and attention to task, which led to functional limitations in gait and mobility. Based on this examination, T.K.'s estimated length of stay was 2 to 3 weeks with a discharge plan of returning home with her family. Physical therapy goals were (1) ambulatory transfers with stand-by assistance and no device to bed, toilet, car, and on/off floor; (2) walk with no device and stand-by assistance of family on smooth and uneven surfaces 1000 feet, 3 times per day with no loss of balance; and (3) ascend/descend 1 flight of stairs with 1 railing, no device, and contact-guard assistance of a family member. Accordingly, the PT plan of care included family education as well as balance, gait, and stair training.
The following outcome measures were used to identify functional deficits and monitor progress in mobility, balance, divided attention, and dual-task ability.
The Functional Independence Measures (FIM) assesses level of assistance required for physical and cognitive independence in the areas of self-care, locomotion, mobility, sphincter control, communication, and social cognition.27,28 The FIM is reliable in detecting changes in independence over time and valid for predicting burden of care in TBI.28
Walking speed was assessed using the 10-m walk test, which is reliable29 and valid30 in severe TBI. The time to ascend and descend 10 stairs was recorded as a measure of functional mobility.
The Berg Balance Scale is composed of 14 items, each rated 0 to 4 for a maximal score of 56, which reliably measures static and dynamic balance during functional tasks in individuals with brain injury.31 A score of fewer than 45 predicts fallers with 85% sensitivity and specificity.32
The Walking While Talking Test (WWTT), a test of cognitive-motor dual-task ability, was administered as described by Verghese et al33; the participant is timed while walking 40 feet with a 180° turn at the midpoint under 3 conditions: comfortable walking speed, comfortable walking speed while reciting the alphabet (WWT-simple), and comfortable walking speed while reciting every other letter of the alphabet (WWT-complex). A cutoff of 20 seconds for the WWT-simple, and 33 seconds for the WWT-complex, predicts elderly fallers with a specificity of 89% and 96%, respectively.33 While only 44% of individuals with acquired brain injury were able to accurately perform the WWT-complex in a small pilot study7 (vs 87% for the WWT-simple), only the WWT-complex elicited a dual-task cost, suggesting that the rote tasks such as recital of the alphabet may not be sufficiently challenging for ambulatory individuals with brain injury.7 Reliability and validity of the WWTT have not been established in persons with TBI.
The Trail Making Test A and B measures cognitive divided attention and visual tracking34; Part A requires the patient to connect 25 numbered circles, in order, as quickly as possible without picking up their pencil. Part B requires the patient to connect the 25 circles, now labeled with numbers (1–13) and letters (A-L) in an alternating fashion (1-A, 2-B, 3-C, etc)34 The Trail Making Test is one of the most commonly administered neuropsychological examinations and is a sensitive measurement of divided attention in persons with TBI.35 Although disease-specific norms have not been identified, normative data for healthy women aged 25 to 34 years with 12 to 19 years of education are 23.3 ± 8.0 for Part A and 52.8 ± 20.4 for Part B.36
Recovery following TBI is highly variable. Despite the severity of T.K.'s injury, she had many positive prognostic indicators, including age, education, and medical history. However, poorer prognosis is associated with increased severity of injury, which is determined by length of posttraumatic amnesia (PTA). Posttraumatic amnesia represents an interval of confusion during which the patient is likely to have behavioral disturbances as well as amnesia to ongoing events24 and serves as an acute predictor of TBI outcome. Posttraumatic amnesia duration of more than 24 hours is classified as severe TBI, while PTA duration of more than 4 weeks indicates a very severe TBI. Long-term outcomes indicate that patients with more than 3 weeks of PTA generally experience residual cognitive deficits, in particular poor concentration and difficulty dividing attention at 1 year postinjury.24 T.K.'s progress toward clearance of PTA was monitored in an orientation group setting using the Orientation Log, a 10-item scale that evaluates place, time, and situation domains.37 This setting and procedure reliably measure the duration of PTA.38,39 T.K. cleared PTA on postinjury day 60, indicating a very severe brain injury.24 Despite the severity of her injury, T.K.'s prognosis with intensive therapy was considered to be fair for achieving functional ambulation and self-care with supervision because of her age, education, and medical history.
ASSESSMENT OF READINESS TO INITIATE DTT
T.K. received PT services 60 to 90 minutes per day, 5 to 6 days per week for a total of 26 days. Prebaseline treatment occurred over 12 days (postinjury days 46–57) and included standard PT (see Table, Supplemental Digital Content 3, which outlines examples of standard PT, available at: http://links.lww.com/JNPT/A33). There is a paucity of evidence indicating the ability of individuals with TBI to benefit from DTT while in PTA, or during the period that the Rancho level of cognitive function is categorized as “confused” (Rancho IV-VI). Therefore, we assessed T.K. performing a dual-task activity (ie, walking while answering an orientation question) once a week to determine her ability to participate in training. With cognitive function classified as Rancho V on postinjury day 51, T.K. demonstrated inability to continue walking while talking and therefore we deemed that she was inappropriate for DTT. However, with cognitive function classified as Rancho V/evolving Rancho VI on postinjury day 57, T.K. was deemed ready for DTT because she was able to continue walking while answering orientation questions, although she was frequently incorrect, easily distracted, and required verbal cues to continue walking. Collection of baseline outcome measures occurred the following day (day 58) and baseline phase A began (Table 1), despite the fact that T.K. had not yet cleared PTA.
This case study included 2 phases; a 7-day baseline period (phase A) and a 7-day dual-task intervention period (phase B) (Table 1). Outcome measures were assessed prior to phase A, between phases and following phase B. The 7-day duration of each phase was determined by the estimated length of stay for T.K.
Phase A (Postinjury Days 58–64)
Phase A was a continuation of the standard PT care provided prebaseline (see Table, Supplemental Digital Content 3, http://links.lww.com/JNPT/A33) with progressions matching T.K.'s functional improvements. In terms of Gentile's Taxonomy, the standard PT interventions represented closed environment body stability and transport activities with and without intertrial variability, with no manipulation,40 while progression included open environments. Phase A served as a baseline period at a time when T.K. was able to participate in, and might receive benefit from, DTT. However, DTT was not utilized during the baseline period. T.K. cleared PTA on postinjury day 60, or day 2 of phase A.
Phase B (Postinjury Days 65–71)
Phase B included standard PT (see Table, Supplemental Digital Content 3, http://links.lww.com/JNPT/A33) supplemented with a directed intervention of DTT for 7 days. Dual-task training occurred for an average of 15 minutes out of each 30-minute session yielding at least 180 total minutes of DTT over 7 days. Interventions included motor-motor and cognitive-motor dual tasks (see Table, Supplemental Digital Content 4, which describes the DTT program, http://links.lww.com/JNPT/A34) that represented an increase in complexity on Gentile's Taxonomy by including manipulation to both open and closed environments during body stability and transport activities.
As independent mobility increased, T.K. demonstrated multiple gait abnormalities including step asymmetry, slow self-selected speed, poor arm swing, decreased push-off, and reduced left knee extension during heel strike. These deviations did not improve with verbal cueing, and T.K. remained fearful of walking at a normal or near-normal pace. Thus, body-weight–supported treadmill training was used to increase motor demands (ie, higher velocity) without risking injury or falls. The goal of treadmill training was to attain long-duration bouts of stepping without gait deviation and physical or verbal assistance. Four sessions of treadmill training occurred during phase B of the study. During each treadmill session, T.K. walked an average of 20 minutes with stepping bouts of approximately 4 to 5 minutes. We adjusted body weight support (BWS) until gait deviations for asymmetry were minimized and then increased treadmill speed to challenge locomotion. Speed was 3.0 to 3.5 mph for the first 2 sessions progressing to 4.0 mph by session 4. T.K. required BWS during the first 2 sessions and only the safety harness was in place for sessions 3 and 4. The BWS harness system at our facility (LiteGait; Mobility Research, Tempe, AZ) does not report percentage of BWS. During all sessions, T.K.'s heart rate and blood pressure were monitored and remained within an expected, safe range. In accordance with other phase B sessions, cognitive tasks (see Table, Supplemental Digital Content 4) such as addition, subtraction, and synthesis of lists were paired with treadmill walking in the same manner as overground walking. However, these tasks were added only after T.K. was able to maintain a steady speed on the treadmill without assistance and comprised only 60 to 90 seconds of each stepping bout. Despite the greater demands of treadmill training, T.K. participated in dual tasks during all sessions.
Performance on divided attention tests (WWTT and Trail Making Test) in phase B indicated modest improvement when compared that in phase A (Table 3). T.K. required fewer cues and had fewer errors and faster completion times for these tests.
T.K. showed clear improvements in functional tasks (Table 3 and Figure 1A). She had a 3-fold greater rate of change in walking speed during phase B than during phase A (0.35 m/s vs 0.1 m/s, respectively). T.K.'s time to descend stairs was markedly reduced after DTT (7.49 s) but only modestly reduced during the baseline phase (2.66 s) (Table 3 and Figure 1B).
Throughout her treatment (day 46–71), T.K. demonstrated improvements on the FIM (Table 2) and Berg Balance Scale as expected with intensive multidisciplinary therapy. The majority of improvement in balance and FIM scores occurred prior to phase A (Table 3) and paralleled T.K.'s increased activity tolerance. Treadmill walking was a successful addition to T.K.'s locomotor training; after 2 sessions, T.K. was able to achieve full arm swing and improved gait mechanics without cueing while walking at 3.5 mph. During the fourth and final treadmill walking session, T.K. was able to achieve symmetrical stride lengths.
Cognitive-motor DTT programs may be effective in ameliorating attentional deficits during mobility in populations of mild TBI18 and other neurological populations.15–19 Longitudinal evidence indicates that individuals with severe TBI with greater than 3 weeks of PTA often have residual cognitive deficits in the areas of concentration and ability to divide attention24; thus, we anticipated that T.K. may benefit from cognitive-motor DTT. Although the DTT intervention itself is not unique, its application to severe TBI is novel and allowed us to target specific attentional deficits that may have been inhibiting safe mobility and to focus upon rehabilitation of both divided attention and mobility impairment with challenging customized tasks.
To our knowledge, this case represents the only report of cognitive-motor DTT in a person with severe TBI. T.K.'s PTA of 60 days far exceeds that of previously reported cognitive-cognitive dual-task interventions in severe TBI (7–30 days20,21). While prior work exploring DTT in TBI has targeted subjects in the outpatient arena, the DTT intervention described was successfully administered within an inpatient rehabilitation setting over a short, clinically feasible duration of 7 days. Other studies targeting cognitive improvements20,21 included 24 to 64 hours of DTT while our study and that of Rábago and Wilson,18 which also targeted mobility and balance in mild TBI, required markedly shorter durations (3 and 6 hours, respectively) to achieve gains. This short duration may highlight the importance of task specificity in DTT.
T.K.'s overall improvements illustrate the feasibility of supplementing standard PT with DTT in persons with severe TBI. T.K.'s mobility continually improved through the baseline phase when no DTT was provided, which is consistent with expected recovery observed with intensive multidisciplinary therapy. However, the change in walking speed during the dual-task phase of 0.35 m/s was considerably larger than the minimal clinically important difference of 0.16 m/s established in populations with subacute stroke.41 Of greater importance is the relationship of increased walking speed to community ambulation. Only after phase B did T.K. surpass 0.8 m/s to achieve speeds sufficient for community ambulation.42
T.K. demonstrated greater gains in time to descend stairs than to ascend stairs during the dual-task phase. This outcome is perhaps due to several factors, including improved eccentric control, left-sided attention, and automaticity. Both walking and stair descent are considered automatic movements, and objective improvement in these activities suggests a positive relationship between DTT and functional mobility.11,14 Interestingly, while many of T.K.'s FIM scores plateau after day 58 (beginning of phase A), the acquisition of a walking speed sufficient for community ambulation occurs well beyond this point. Thus, program evaluation for DTT after TBI must be carefully considered. It appears that objective outcome measures such as walking speed and dual-task measures (WWTT) may prove to be more sensitive indicators of gains and treatment efficacy than measures focused on burden of care.
Previous studies reported difficulty with participation in the WWT-complex; however, we did not encounter this problem.7 All parts of the WWTT were easily and quickly administered, even during periods when PTA had not fully resolved. Unfortunately, we did not record the time to complete the complex cognitive task in sitting, which would have allowed for the calculation of dual-task cost. However, based on our experience, WWTT could be applied clinically to gain objective measures of dual-task ability in individuals with severe TBI. While T.K. also demonstrated improvements on the Trail Making Test, it is important to note that this pen-and-paper test does not measure improvements in functional mobility or real-world dual-task situations.
The motor and cognitive tasks utilized throughout the progression of this program were dictated by T.K.'s functional gains and level of cognition. Her attention to task, memory, and agitation all served as guides for treatment progression, particularly for the secondary cognitive tasks. As T.K.'s attention improved, we were able to introduce more cognitively challenging secondary tasks. If a task was introduced that caused frustration or severe detriment in the primary task, it was abandoned for an easier task. Increasing secondary task difficulty mirrored T.K.'s improvement in ability to dual task throughout phase B.
Several factors beyond the addition of DTT may have contributed to the positive outcomes seen in T.K. Indeed, intensive multidisciplinary therapy alone may account for the improvements in walking speed and dual-task measures. In addition, the use of treadmill training as a progression of gait training may be challenged; it has been used in TBI populations to improve both cardiorespiratory capacity and spatiotemporal characteristics of unsupported overground walking.43 In this case, it allowed us to modulate speed in a safe environment. All treadmill training occurred during phase B of the study and may have contributed to the observed gains in walking speed. Finally, T.K. was started on amantadine on postinjury day 65, the same day that phase B began. In TBI, amantadine can be used off-label to improve sustained and divided attention, increase arousal, and reduce impulsivity. Whether this drug contributed to the observed functional improvements is unclear because other mood-stabilizing drugs, including quetiapine44 and sertraline,45 were prescribed during phase A to reduce agitation and improve cognition and alertness.
The ability of individuals who have not cleared PTA to benefit from DTT is also an important consideration. With PTA, patients may be unable to retain training effects within or between treatments. For T.K., about 33% of phase A (2 days) occurred with PTA. Thus, the lower rate of recovery during this phase may be due in part to PTA. However, because T.K.'s impairments in attention to task were contributing to her mobility, we felt that a program of DTT may be beneficial. These limitations represent the true conditions encountered in the clinic and the best interests of the patient, without regard to the experimental design. Overall, these clinical modifications alone, or in combination with the dual-task intervention, were associated with greater gains in phase B than were seen in phase A.
This case study provides support for the feasibility and possible benefits of DTT in addition to standard PT for an individual with severe TBI. Clinically meaningful improvements were found in functional mobility and ability to dual task as measured by the WWTT. Specific improvements seen in the intervention phase cannot be solely attributed to DTT, but this training did not disrupt the progression of recovery. Indeed, gains in locomotion and attention with the addition of DTT outpaced those seen with standard PT 2- to 3-fold. The results of this case study are encouraging and support the need for studies with larger sample sizes to identify the optimal time to initiate DTT following TBI, further examine whether gains in functional mobility and cognition can be enhanced with DTT in severe TBI, and explore the transfer of DTT to real-world dual-task demands.
We thank Sara Rismiller, MPT, NCS, for her mentorship and assistance in data collection, Dr Meredith Wilhelm for her thoughtful manuscript edits, and all of the providers on the traumatic brain injury service at Dodd Hall Inpatient Rehabilitation Hospital for their support.
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balance; divided attention; dual-task; dual-task training; gait speed; severe traumatic brain injury; Walking While Talking Test (WWTT)