Rehabilitation for balance and ambulation in a patient with attention impairment due to intracranial hemorrhage. (Case Report).

Patients with central nervous system disorders frequently require physical therapy to improve balance and ambulation. Current physical therapist practice for the management of central nervous system disorders largely emphasizes management of the motor and sensory impairments affecting balance and ambulation. (1 (pp372-381)) However, patients with central nervous system disorders frequently demonstrate cognitive impairments that also affect mobility, especially in the home or community settings and during activities of daily living. (2-4) I believe that unless physical and cognitive impairments are addressed, functional limitations in mobility may persist.

Patients with central nervous system disorders often have impairments in attention. Various definitions and theories of attention exist. In general, attention theories propose that a pool or pools of attentional or information processing resources (attentional capacity) exist that can be allocated to activities at any given time. Different activities draw from these pools in varying amounts. When the information-processing requirements of an activity or activities interfere with each other or exceed the attentional capacity, a decrease in performance results. (5,6)

Using this framework for attention, researchers have demonstrated that postural control and motor tasks require attentional demands, which increase with the complexity of the task. (7-11) Lajoie et al (10) found that when subjects without known attention or balance impairments were asked to respond to an auditory stimulus during a simultaneous motor task (ie, sitting, walking), their reaction times to the auditory stimulus increased with the complexity of the motor task. Andersson et al (7) examined the relationship between mental activity and postural control. In this study, subjects performed a mental task with and separate from 2 balance tasks (standing on a moving platform with eyes open and with eyes closed). Subjects without known attention or balance impairments demonstrated increases in anteroposterior postural sway when each of the balance tasks was performed simultaneously with the mental task compared with anteroposterior postural sway on the balance tasks alone. The accuracy of the subjects' mental task performance decreased when the mental task and the balance tasks were performed simultaneously compared with their accuracy on the mental task when they were sitting. Together, the results of these studies (7,10) suggest that complex balance tasks require attentional resources in people without known problems with attention.

Although research on the effect of impaired attention on balance in patients after acquired brain injury is limited, the results of several studies support a relationship between attention and balance in these patients. When the information processing system of the brain is impaired following brain injury, attentional capacity is decreased. This decreased attentional capacity was demonstrated by Van Zomeren and Deelman, (12) who found that patients with head injury had an increased reaction time during a reaction-time task and that the reaction time was proportional to the duration of coma after injury. Patients with attention impairments after brain injury could be expected to demonstrate decreased performance on a balance task if the attentional requirements at the time of the task exceed the reduced attentional capacity. In one study of subjects at least 3 months after mild traumatic brain injury (ie, subjects who had sustained direct head trauma with subsequent impaired consciousness or amnesia and with the lowest Glasgow Coma Scale scores ranging from 13 to 15 after hospitalization), researchers found that poor performance on the Symbol-Digit Substitution Test (which tests attention and mental speed) was associated with decreased postural stability as measured during quiet standing and weight shifting on a force platform. (13)

The balance tasks performed in these studies tended to be clinical tests of balance rather than "real-life" tasks; therefore, it is difficult to draw definitive conclusions regarding the relationship between attention impairments and balance during functional tasks such as walking across the street at a busy intersection. The studies do suggest, however, that people with impairments in attention tend to demonstrate decreased postural stability, especially during complex mobility tasks that require them to attend to multiple stimuli (eg, walking in the grocery store while carrying a bag of sugar and looking for the next item).

Patients with impaired attention, especially impaired divided attention (see Table for definitions of types of attention), (14) may also be likely to have balance problems due to difficulty performing a task while simultaneously processing and using feedforward information to avoid obstacles. Patients with decreased divided attention, for example, may not notice spills on the floor of the grocery store because they are attending to the search for food items. These patients may be likely to fall after stepping on a wet floor. This possibility is supported by one study that showed that avoiding obstacles places an attentional demand on the information-processing system. In that study, subjects stepped over obstacles with and without performing a secondary task (responding vocally when specific lights were turned on). (15) Both young and older adults without known problems with attention contacted the obstacles more often when their attention was divided between stepping over the obstacles and performing the secondary task. In patients with a limited attentional capacity, the attention required to avoid obstacles while performing a secondary task would be more likely to exceed their attentional capacity. Thus, their ability to process all relevant information simultaneously and produce a rapid, accurate response to avoid obstacles would be decreased. The implications of impairments in attention are especially important when we consider that many patients with central nervous system disorders also have impairments in motor control and balance.

The physical therapy literature offers limited guidance for addressing attention impairments as they relate to mobility. In order to compensate for attention impairments in patients who are easily distracted, some sources recommend decreasing distractions in the environment during physical therapy. (16,17) Others recommend initially decreasing distractions in the environment and then increasing distractions as the patient improves. (18)

The neuropsychology and cognitive rehabilitation literature supports the effectiveness of both compensatory techniques and attention training for the management of attention impairments. (19-24) Compensatory techniques for attention are techniques in which patients use strategies to improve performance on a given task despite continued impairment. Determining which strategy to use for an individual patient depends on the environment in which the patient must function and on the patient's specific combination of cognitive and physical impairments. (19) Examples of compensatory techniques for decreased attention include decreasing the number of distractions in the environment, double-checking work for accuracy, positive reinforcement of attentive behavior, (25) and using self-instructional techniques in which patients repeat statements instructing themselves to focus their attention and then repeat information presented to them subvocally to maintain concentration. (26)

The second type of cognitive rehabilitation for attention is attention training, which uses cognitive exercises to challenge impairments in the 5 types of attention (Table), increasing the demands of the exercises in a controlled manner. (19-22,24) The effectiveness of attention training continues to be a topic of study. Some studies (20-24) demonstrated improvement in attention in subjects with brain injury who received cognitive retraining for attention compared with subjects who did not receive cognitive retraining for attention. These studies, however, differed in the outcome measures of attention that showed improvement--measures of neuropsychological testing for attention, (20-23) measures of attention behavior (ie, attending to a therapy task), (24) or measures of independent living or employment. (21) Overall, the studies support the effectiveness of attention training that: (1) incorporates different levels of complexity and a variety of stimuli and response demands (ie, using different modalities such as visual and auditory stimuli), (19-24) (2) uses training tasks that closely relate to the outcome measure, (21,22) and (3) provides subjects with feedback on performance or results. (20,27)

Although improvement in outcome measures has been shown for subjects with moderate to severe attention impairments, (20,28) no single study has addressed which patients will benefit most from attention training. However, the Cognitive Rehabilitation Committee of the American Congress of Rehabilitation Medicine has issued practice guidelines in a review article that combined the results from several studies. (28) In these practice guidelines, attention training is "recommended during postacute rehabilitation for persons with TBI [traumatic brain injury] or stroke." (28 (p1610)) This guideline was supported by several single studies as well. (18,19) For patients in the acute/inpatient rehabilitation phase, evidence was insufficient to support attention training over more general cognitive rehabilitation and spontaneous recovery. (28,29)

In general, attention training techniques attempt to improve attention by repeated practice. However, theories to provide the rationale for treatment and the process by which treatments bring about improvement are not well delineated. Several theories about the process by which cognitive rehabilitation in general leads to recovery of function have been proposed. One theory suggests that the brain reorganizes, allowing undamaged areas to take over the responsibilities of the damaged areas. (30) Another theory suggests that recovery of function occurs when the brain uses its remaining functional capacities to achieve behavioral goals by different routes. (30)

The purpose of this case report is to describe how cognitive rehabilitation techniques were integrated into an interdisciplinary treatment plan for a patient with a brain injury whose decreased attention and balance limited his ability to ambulate independently in a community environment.

Case Description

Examination

History. The patient was a 16-year-old male with a diagnosis of intracranial hemorrhage secondary to arteriovenous malformation (AVM). His subsequent medical history included placement of a ventriculoperitoneal shunt (VPS) after the initial hemorrhage, repeated intracranial hemorrhage with 2 episodes of generalized seizures 1 month after the initial hemorrhage, embolization of the AVM 2 months after the initial hemorrhage, hydrocephalus causing midline shift and mass effect 4 months after the original hemorrhage with replacement of the original VPS, and gall bladder surgery 8 months after the initial hemorrhage. Because of time constraints in the clinic, results of any diagnostic testing done to determine the specific areas of the brain involved in the hemorrhages were not sought by the therapy team. Six months after the initial hemorrhage, immediately following acute hospitalization and a 6-week stay in an inpatient rehabilitation unit, the patient was admitted for outpatient rehabilitation. In addition to physical therapy services, the patient also received speech-language therapy, occupational therapy, social work, and nursing services. The patient's outpatient rehabilitation program was overseen by a physiatrist.

Prior to the hemorrhage, the patient was a junior in high school with average academic performance and no relevant prior medical history. He spent his leisure time "hanging out with friends" and was a member of his high school football team. The patient and his grandmother reported that following his discharge from the hospital, he demonstrated unsteadiness while walking at home--including one fall. Their goals were improving balance, returning to school, and participating in after-school sports as a line coach for his high school football team (his physician had restricted him from playing football because of the risk of further brain injury).

Physical therapy tests and measures. Observational gait analysis was performed as the patient walked more than 30.5 m (100 ft) at a self-selected pace in a nondistracting environment. He had right knee hyperextension in approximately 30% of his steps during the right stance phase and a positive Trendelenburg sign bilaterally. No losses of balance were noted during this gait analysis. (Unless otherwise noted, a loss of balance refers to postural instability requiring stepping or upper-extremity balance strategies or physical assistance from another person to prevent a fall.) When the patient walked for 61 m (200 ft) in a more distracting environment (an area of the clinic with other people, equipment and furniture placed around the room, and pictures on the walls), he was distracted 4 times, as evidenced by head turning and gazing toward the distraction, followed by losses of balance requiring stepping responses to prevent a fall. The losses of balance decreased to 1 to 2 incidents over a 61-m (200-ft) distance when verbal and tactile cues were provided to help focus the patient's attention on upcoming obstacles (eg, a change in surface from tile to carpeting). The patient also frequently stopped walking when conversation was initiated. The tendency to "stop walking when talking" in elderly people has been shown to correlate with a higher incidence of falls. (31) In instances when he did not stop walking while carrying on a conversation, the patient often lost his balance. The patient required standby assistance when walking in familiar, indoor settings and contact guard assistance when walking in more distracting environments, such as outside and at church, because of frequent loss of balance.

On balance assessment in standing, the patient had decreased balance compared with the level of balance that would be expected in a typical person of his age. The patient was unable to perform tandem gait, losing his balance laterally with each step (19 steps over 6.1 m [20 ft] total) and requiring physical assistance with each step to recover balance and prevent falls. Several studies have investigated the relationship between tandem gait speed and impaired postural control and gait (32,33); however, the patient was not even able to perform the activity. The patient was unable to maintain one-legged stance or tandem stance bilaterally for longer than 2 seconds. In a study of 184 subjects without balance deficits between 20 and 79 years of age, all subjects under 40 years of age (n=62) were able to maintain one-legged stance for 30 seconds. (34) Together, the results of these tests indicated a balance impairment.

Manual muscle testing also was performed to help determine whether weakness was playing a role in the patient's losses of balance during gait. The manual muscle tests were performed as described by Kendall et al35 and ranged from 3-/5 to 4+/5 bilaterally in the hip, knee, and ankle musculature, with increased time required (4-5 seconds) for full muscle activation with all manual muscle testing. Wadsworth et al (36) found that the intrarater reliability of data obtained with manual muscle testing for various upper- and lower-extremity muscles was good, with test-retest reliability coefficients ranging from .63 to .98 (P<.05) and with the paired t test revealing no significant test-retest mean differences between manual muscle tests (P>.05). Manual muscle testing has some content validity in that it measures the ability of the muscles to generate torque. (37) Its predictive validity, however, has been debated in the literature. (38)

The appropriateness of manual muscle testing in patients with brain lesions also has been debated in the literature. (38,39) Some of the arguments against the use of manual muscle testing in these patients include: (1) spastic antagonists may be opposing the muscles being tested, (2) muscles may be stronger when acting in a mass pattern than in the muscle test, and (3) apparent weakness in muscles may actually be due to sensory impairments. (39) However, in this case, the patient had minimal hypertonicity in his lower extremities, no tendency to move in mass patterns on observation, and intact sensation. As measured by the Modified Ashworth Scale, his lower-extremity muscle tone was normal, except for a score of 1+ in both ankle plantar flexors and knee flexors.

Bohannon and Smith (40) reported good interrater reliability for the Modified Ashworth Scale when they found that 2 raters agreed on 86.7% of their ratings of elbow flexor spasticity and that these ratings were significantly correlated (P<.001). Blackburn et al (41) found that the intrarater reliability for the Modified Ashworth Scale was acceptable, with 73.3% agreement, when used on the lower extremities of subjects with stroke. The Modified Ashworth Scale may have face validity, because it appears to measure spasticity by assigning a grade to resistance felt on passive stretching. (40) Further studies examining both reliability and validity are needed before a determination of the Modified Ashworth Scale's validity can be made. The patient's bilateral lower-extremity range of motion was normal on goniometric measurement during active and passive movement, and he performed the isolated movements required in active range of motion testing without difficulty (ie, no mass patterns were observed). Active and passive range of motion were measured with a universal goniometer as described by Norkin and White. (42) Intratester reliability of goniometric measurements of lower-extremity passive range of motion has been found to be good, with intraclass correlation coefficients (ICCs) of .91 and .99 for knee extension and flexion, respectively, (43) and ICCs of .86 and .90 for ankle plantar flexion and dorsiflexion, respectively. (44) Limited studies of the validity of goniometric measurements are available, although Gogia et al (45) found good validity (ICC=.98-.99) when goniometric measurements of the knee were compared with measurements of the joint angle of a roentgenogram. Sensation was tested as described by Schmitz (46) and found to be intact to light touch, position sense, and kinesthesia in both lower extremities. Therefore, the main arguments against using manual muscle testing in patients with brain lesions are not applicable to this patient's case.

Occupational therapy and speech-language pathology tests and measures. The assessments of the occupational therapist and the speech-language pathologist indicated that the patient's primary cognitive impairment was decreased attention, including decreased sustained attention, divided attention, alternating attention, and selective attention. The occupational therapist and the speech-language pathologist based their assessments of the patient's attention on testing and on observation of his behavior. To test for attention impairment, the speech-language pathologist administered portions of the Word Sequences Subtest of the Detroit Tests of Learning Aptitude. (47) The Word Sequences Subtest consists of 30 series of unrelated words from 3 to 8 words long, which are read to the subject. The subject then repeats each series of words back to the tester. In this case, the speech-language pathologist read only 17 of the 30 series of words to the patient, with the series ranging from 3 to 7 words long. Although the patient demonstrated an attention impairment based on the judgment of the speech-language pathologist, specific data from this ad hoc version of the Word Sequences Subtest cannot be shown to be reliable or valid. The occupational therapist administered a revised version of the Trail Making Test, Part B. The Trail Making Test, Part B, is a test that measures attention as well as other abilities such as visual tracking. (48,49) In this test, 25 circles are spread over a page and labeled with numbers (1-13) and letters (A-L). The subject draws a line to connect the circles in order, alternating between numbers and letters (ie, 1, A, 2, B, 3, C, and so on). (48) The test that the occupational therapist administered in this case consisted of 22 circles placed along the perimeter of a larger circle and labeled with numbers (1-11) and letters (A-K) in random order. The patient then drew a line connecting the circles in order, alternating between letters and numbers. There are no reliability or validity studies available for this test. When observed, the patient demonstrated behavior consistent with an attention impairment. He attended to a given task for no more than 1 to 2 minutes at a time, required frequent redirection to the task, was easily distracted by his environment, and had difficulty shifting from one task to another. He also demonstrated impairments in auditory comprehension (understanding spoken information) when answering questions about a story that was read to him and impaired organization skills when organizing a shopping list; however, these impairments were judged to be secondary to his attention deficits. For example, the patient had difficulty answering questions about a story because he was unable to attend to the story while it was being read to him.

The patient also demonstrated mild impairment in visual perception, which is the ability to attend to appropriate visual stimuli and to integrate and interpret them. (50) Testing for visual perception was done by the occupational therapist with the Motor-Free Visual Perception Test (MVPT). (51) The MVPT had good test-retest reliability (r=.81), (51) and it was found to demonstrate construct validity when subjects' scores on the MVPT had higher correlations with their visual-motor test scores than with their achievement and intelligence scores. (51) Because vision plays a role in maintaining postural stability, (52) this mild visual impairment may have contributed to the patient's balance impairment. However, because it was a mild impairment, it was probably not a major factor in the patient's frequent losses of balance during gait.

Evaluation

Based on examination results, the interdisciplinary treatment team hypothesized that the factors contributing to the patient's losses of balance were his impairments in balance, attention, strength, and vision. We believed that the combined attentional requirements of walking, maintaining balance, and interacting visually and verbally with the environment exceeded his capacity and resulted in decreased performance. This hypothesis was supported by the observations that the patient had more frequent losses of balance while walking in distracting environments, that he frequently diverted his attention to a distraction (eg, turning his head to look at the distraction) immediately before losing his balance, and that his losses of balance that required a stepping response were less frequent when verbal cues were provided to focus his attention on upcoming obstacles. Although the patient's lower-extremity weakness and visual-perceptual impairment may have been factors in his decreased stability, we did not believe that they contributed to his frequent losses of balance as much as his balance and attention impairments. By discharge, the patient would need to maintain his balance during complex ambulation tasks (eg, carrying a book bag and talking) in the presence of multiple distractions in order to return to school and the community. Ambulating safely with distractions in a community environment became the primary goal of physical therapy.

The patient was seen in an interdisciplinary, day rehabilitation setting 3 hours per visit, 3 times per week, for 11 weeks of treatment. The patient engaged in one 50-minute physical therapy session per visit for all but 4 visits, when he was seen for a 2-hour session. The 4 longer treatment sessions were scheduled when more time was required for interventions such as family training and community outings. The remainder of the time (1-2 hours per visit) was divided between sessions with the occupational therapist and the speech-language pathologist. The patient was seen by the social worker for 1-hour sessions once every 1 to 3 weeks. The treatment course was interrupted after 10 weeks of treatment for approximately 2 weeks when the patient was hospitalized and recovering from gall bladder surgery. The frequency of 3 times per week was chosen in order to provide services intensive enough to facilitate improvement while still allowing the patient enough time outside of therapy to practice the skills learned in therapy. The duration was chosen to allow time for improvement adequate for resumption of previous activities and to coordinate with re-entry to school at the beginning of a semester.

Intervention.

To address the patient's losses of balance resulting from distraction, the patient's physical therapy plan of care was designed to include attention training and compensatory techniques for attention within the context of gait and balance training. Initially, the use of several compensatory techniques enabled the patient to ambulate with fewer losses of balance. For instance, a quiet, nondistracting environment was provided for the patient to practice ambulation and balance tasks such as walking or reaching overhead for objects. In addition, if I detected signs of distraction--such as the patient turning his head to a stimulus or initiating discussion about an irrelevant topic--I provided verbal or tactile cues to refocus his attention on the task. During the first 2 physical therapy sessions, while using these compensatory techniques, the frequency of loss of balance decreased from 4 events to 1 or 2 over 61 m (200 ft) of ambulation in a nondistracting environment. Initially, the patient's family was also instructed to cue the patient to refocus his attention on his balance and ambulation as needed outside of therapy.

After the patient walked in this nondistracting environment without loss of balance during the first 2 physical therapy sessions, physical therapy tasks progressed to include attention training. According to the theory that balance tasks of increasing complexity require increasing amounts of attention, (10) attention training was implemented by gradually increasing the complexity of ambulation tasks and balance exercises while manipulating the environment to increase attention demand. The 3 aspects of effective attention training noted earlier were integrated into this modified approach: (1) training tasks that closely relate to the desired outcome (ambulation in all environments without falls) were chosen, (21,22) (2) different levels of complexity and multimodal stimuli and response demands were incorporated into treatment activities, (19-24) and (3) feedback was provided. (20,27)

The first aspect of an effective attention training program was incorporated by choosing training tasks that were closely related to the desired outcome. Ambulation and balance exercises as well as environmental modifications were tailored to patient-specific criteria. This patient's goal was to return to school; therefore, environmental factors such as conversational distractions and crowds were introduced to simulate tasks such as walking in the school corridors. Ambulation exercises such as walking around obstacles and carrying books while walking also were emphasized because this would be the most physically challenging aspect of returning to school (eg, compared with sitting at a desk). In another patient, other modifications may have been made based on that patient's goals (such as walking while reading if the patient were a mail carrier).

The second aspect of an effective attention training program was incorporated by creating a structured framework of treatment activities that required different levels of complexity and multimodal stimuli and response demands. The level of complexity was adjusted by making balance and ambulation tasks more challenging to increase the attention required to perform the tasks. Environmental modifications also were made to augment both the amount of attention and the level of attention (Table) required to perform the treatment tasks. Further, the progressions in ambulation tasks and the environmental modifications incorporated varied stimulus and response demands. For example, during the course of treatment, the patient received auditory, visual, and tactile stimuli. He also produced varied responses, including verbal and motor responses. These progressions increased the demands of the attention system and, thus, were hypothesized to bring about an improvement in balance, ambulation, and attention. The following environmental modifications were introduced and progressed as indicated:

* Increasing auditory input during ambulation: Initially, irrelevant auditory stimuli were introduced, such as people conversing or the radio playing near the patient, to increase the selective and sustained attention required by the patient to focus on ambulation and prevent a loss of balance. Once the patient walked in the presence of a variety of irrelevant auditory distractions without loss of balance, he received auditory input relevant to him, such as conversation directed to the patient as he walked. The complexity of this conversation was increased as he progressed. That is, once the patient responded to a simple greeting in a quiet environment without loss of balance (after approximately 2 weeks of outpatient physical therapy), conversation was expanded to include complex questions about school. These relevant auditory stimuli required the patient to use alternating attention to switch his focus as needed between walking and talking and to use divided attention to attend simultaneously to auditory input and ambulation in order to prevent a loss of balance.

* Increasing the number of obstacles in the environment during ambulation: The patient ambulated in increasingly cluttered environments. In less-cluttered environments, the emphasis was on selective attention--the patient had to decide what stimuli to focus on intermittently. In more-cluttered environments, the emphasis was on divided attention--the patient had to attend constantly to avoiding obstacles and to planning his route as he walked. For example, after 2 physical therapy sessions, the patient could walk in an open gym without loss of balance (using selective attention to avoid obstacles); he then progressed to walking in a kitchen or dining room with several tables, chairs, countertops, appliances, objects on the floor, and narrow walkways (using divided attention to plan his route and avoid obstacles).

* Changing the characteristics of the walking surfaces: As the patient transitioned from walking on tile to walking on less-even surfaces such as carpet, he had to attend to the differences in walking surface (selective attention) and adjust his walking to accommodate the change. When the patient initially began treatment, he frequently had a loss of balance. This required both a stepping strategy and an upper-extremity strategy when crossing a threshold between tile and carpet if he was not visually attending to the change in surface. Once the patient consistently negotiated a threshold between tile and carpet in a nondistracting environment without loss of balance (after approximately 3 weeks of outpatient physical therapy), he practiced negotiating larger changes in surface with more environmental distractions (eg, negotiating threshold between sidewalk and grass surface outside).

* Adding motion to the environment: Adding motion to the environment made the patient attend both to the state of his immediate environment and to changes in the environment as they occurred or before they occurred (selective attention, alternating attention, and divided attention). Examples of tasks that were used to integrate motion into the patient's environment included introducing external perturbations (eg, another person bumping into the patient), walking in a crowd of people, and using escalators. As the complexity of the situation increased (eg, from bumping into the patient in an open gym without other people in the room to bumping into the patient in a crowded mall), the emphasis shifted from selective attention and alternating attention to divided attention where the patient had to focus on walking and distractions at the same time. Small external perturbations were introduced after 1 week of physical therapy, when the patient was able to maintain balance while walking in open, nondistracting areas without a loss of balance. Motion in the environment was progressively increased as the patient improved. For example, the patient used escalators in a distracting environment (a bookstore) during a physical therapy session after 10 weeks of physical therapy.

These techniques for increasing attention demands by modifying the environment were introduced and progressed concurrently. Progression occurred when the patient performed a given task without loss of balance. In addition, practice of each activity occurred in variable patterns; that is, the treatment activities were alternated within each therapy session. As a result, the time frame for each progression is approximate because the patient's ability to respond to each environmental modification depended on other variables in the environment. For example, although the patient was able to respond to a simple greeting during ambulation in an open, nondistracting environment without loss of balance after 2 weeks of physical therapy, his performance tended to decrease if he was in a more-cluttered environment. Therefore, specific time frames are difficult to determine. Throughout the patient's 11 weeks of physical therapy, these environmental modifications were progressed and combined (eg, walking in a cluttered environment over uneven surfaces while having a discussion about physics) to continue to increase the attentional demands of the activity.

Within the context of attention training, exercises were progressed. As the environmental modifications increased the attention demands, the balance exercises increased in difficulty to augment their attention demand. Balance exercises the patient performed included Romberg stance with eyes open and closed, tandem walking, single-limb stance, tandem stance, side-stepping, braiding, kicking a ball in sitting and standing positions, standing exercises with one foot on a foam roller, and hopping on one foot. The balance exercises were made more difficult by decreasing sensory input (ie, performing the exercises with eyes closed) (9) and by decreasing the base of support such as during performance of tandem stance or single leg stance. (10) For example, once the patient kicked a ball in a sitting position without loss of balance requiring upper-extremity balance response, he progressed to kicking a ball in a standing position.

Ambulation tasks were also progressed. As the environmental modifications increased the attention demands, the complexity of the ambulation tasks also were increased by adding components that required simultaneous manipulation of an object or a change in the variables of ambulation. The first component added to the patient's ambulation was carrying a book bag, because he would have to carry it to each of his classes when he returned to school. Once the patient ambulated 30.5 m (100 ft) while carrying his book bag without loss of balance, other components were added to the task--the weight of the book bag was increased, speed was increased (as if he was late for class), and directions were changed suddenly. Increasing the complexity of the ambulation task demanded additional attention in order to maintain balance and to perform the task.

When the patient responded to the challenges in the clinic without a loss of balance, community ambulation was introduced. In this environment, all of these demands were present in various combinations. As in the clinic, the community environments were introduced progressively, depending on their attention and balance demands. For instance, a quiet library had fewer attention demands than a crowded, noisy grocery store.

The third aspect of an effective attention training program was incorporated by providing the patient with feedback to maximize his learning and retention. I provided extrinsic feedback, which outlined specific knowledge of results (eg, "You lost your balance 3 times during that last walk.") and knowledge of performance (eg, "Just before you lost your balance, you turned your head toward that distraction."). As the patient progressed, he verbalized aspects of his intrinsic feedback as well. For example, after a walking and talking task, he stated, "When I started talking, I had to take a step to catch my balance." This intrinsic feedback was augmented by additional extrinsic feedback as needed (eg, "You also had to use your arms on the wall to keep from falling."). I provided the extrinsic feedback as both summary feedback and bandwidth feedback. Summary feedback is defined as a summary of knowledge of results or performance over multiple trials after the trials are completed. (53) The number of trials in the summary increased as the patient's skill in the given activity improved. Bandwidth feedback is defined as feedback that is given if performance falls outside of a predetermined acceptable range. (53,54) Bandwidth feedback was provided by giving the patient immediate feedback if he appeared in danger of falling according to the judgment of the therapist. By using both summary and bandwidth feedback, the feedback was decreased as the patient improved to minimize dependency on extrinsic feedback and maximize retention. (53-56)

The program addressing the patient's ambulation, attention, and balance in physical therapy sessions was part of a larger interdisciplinary plan of care. In addition to the interventions described above, the patient's physical therapy plan of care included the following elements: (1) cardiovascular endurance training on a stationary bicycle and a treadmill, (2) patient and family instruction about the patient's impairments, his functional limitations, and techniques for providing him with safe care, and (3) instruction in a home exercise program for trunk and lower-extremity strengthening.

The home program exercises were performed for 15 repetitions each and consisted of single-plane antigravity active range of motion exercises for the trunk flexors and each major muscle group of the lower extremities. They were performed in supine, side-lying, sitting, and standing positions. After 9 weeks of treatment, these exercises were progressed to include resistance from a There-Band. * Compensatory techniques for balance and attention were introduced in which the patient and his family were initially instructed in decreasing distractions during ambulation and in providing verbal and tactile cues to help him focus attention on ambulation. As the patient progressed, he and his family were instructed in how to increase environmental distractions during ambulation at home to maximize carryover of progress in physical therapy sessions. For example, once the patient began to work on community ambulation in physical therapy, he was encouraged to accompany his family members on trips into the community, such as to the grocery store or a shopping mall. The patient's grandmother attended therapy sessions frequently and was kept informed of the patient's progress and abilities. She and the patient reported that he carried out his home program. The patient's occupational therapist and speech-language pathologist also managed the patient's attention impairments (as well as other impairments listed in "Occupational Therapy and Speech-Language Pathology Tests and Measures"). Cognitive rehabilitation techniques used in occupational therapy and speech-language pathology to address the patient's attention impairments are outlined in the Figure.

Figure.

Cognitive rehabilitation techniques used in occupational therapy and speech-language pathology to address the patient's attention impairments.

Attention training

* Performing computer exercises aimed at increasing attention

* Practicing shifting attention across 3 tasks

* Performing tasks in the presence of distractions

* Performing tasks requiring prolonged attention such as reading an article

Compensatory techniques

* Double-checking written and verbal information

* Using external cues (eg, timer) to focus attention

* Giving the patient a timeframe or deadline

* Identifying and decreasing distractions

* Reading aloud (eg, when reading directions)

* Providing verbal cues for redirection when the patient became distracted

* Using checklists

Outcome

At the time of the physical therapy discharge examination, the patient had improved in all areas of impairment. I observed no significant gait deviations in clinic or community environments. The patient ambulated in community environments, negotiating uneven surfaces and escalators without loss of balance. The patient also ambulated in a crowded environment carrying a book bag and engaging in conversation without slowing down or stopping and without loss of balance. This ability to walk and talk simultaneously marked a change from the initial examination and indicated a lower chance of falls. (31) The patient demonstrated improved balance on both tandem gait and one-legged stance when compared with the initial testing. He performed tandem gait for 6.1 m (20 ft) independently in approximately 20 seconds without loss of balance and with appropriate balance responses. The patient performed this test faster than people who had not fallen and who participated in a study by Gunter et al. (33) In this study, a group of people who had not fallen performed tandem gait faster than a group of people who had fallen. (33) The patient performed right and left one-legged stance for 30 seconds each without loss of balance, which is within normal limits for adults younger than 40 years of age. (34) The patient also performed age-appropriate activities such as running, jumping, and skipping without loss of balance. The patient's lower-extremity manual muscle tests ranged from 4/5 to 5/5 bilaterally. Muscle tone as measured by the Modified Ashworth Scale was normal throughout the lower extremities.

The occupational therapist and the speech-language pathologist were unable to perform formal retesting of cognition at the time of discharge because the patient was discharged suddenly for financial and personal reasons. However, the patient demonstrated functional improvement in areas affected by attention. At the time of discharge, the patient engaged in written tasks and schoolwork for up to an hour in the presence of distractions. He also used strategies to increase attention independently, such as double-checking work and reading instructions aloud.

One month after discharge from physical therapy, the patient and his grandmother reported that he had successfully returned to school, navigating crowded hall-ways between classes without loss of balance or unsteadiness. They also reported that he attended full days of classes and was a line coach for his high school football team.

Discussion

This treatment approach was consistent with the framework of transfer-appropriate processing. According to the concept of transfer-appropriate processing, maximum learning occurs when the processing requirements of the practice conditions are similar to the processing requirements of the transfer test. (57) Therefore, in this case, learning would occur if the processing requirements of the therapy activities were similar to the processing requirements of walking in school. The treatment approach described in this case report applied the concept of transfer-appropriate processing in 3 ways.

First, the described treatment approach required the patient to perform progressively more challenging balance and ambulation exercises in the presence of distractions. The processing requirements of this approach were hypothesized to be more similar to those of walking in school than to those when performing the ambulation and balance exercises alone. That is, both the treatment activities and walking in school required the patient to use attentional capacity for maintaining balance and for interacting with the environment simultaneously.

Second, both the practice conditions and the transfer test conditions (walking in school) were variable. Just as the conditions in school varied during each school day (eg, walking in an empty hallway before school versus walking up and down stairs between classes), the ambulation and balance exercises and of the attention training varied within each therapy session. Furthermore, in several studies variable and random practice conditions promoted improved performance on transfer tests and increased retention. (58,59) According to the transfer-appropriate processing framework, the variable and random practice conditions required the patient to regenerate the appropriate movement pattern for each trial rather than simply repeating or revising the previous movement pattern as with blocked practice.

Third, the practice conditions in this treatment approach incorporated knowledge of results in a pattern that maximized transfer-appropriate processing. In the transfer test (walking in school), the patient would not know the results from external sources. The patient would only receive knowledge of results by self-monitoring his balance. Therefore, practice conditions were structured to develop the patient's use of internal knowledge of results and minimize the amount of summary and bandwidth feedback given to the patient. In addition, this pattern of minimizing extrinsic feedback likely maximized the patient's retention. In a study in which subjects received bandwidth feedback on a ballistic timing task (goal=200 milliseconds), subjects in the 0% bandwidth group received feedback on each trial, whereas subjects in the 5% and 10% bandwidth groups received feedback only if their performance fell outside of their respective goal bandwidth (between 190 and 210 milliseconds for the 5% bandwidth group and between 180 and 220 milliseconds for the 10% bandwidth group). The subjects who received feedback in a 10% bandwidth (and, therefore, at the lowest frequency) performed just as accurately and more consistently on retention tests than the subjects who received more frequent feedback. (54)

This case report cannot identify how the patient's improvement came about. The patient's improved performance may have resulted from more automatic performance of walking and thus lowering the attention demand of the task. Alternately, improved attentional capacity may have resulted in improved ability to attend to both walking and interaction with the environment. This case report also cannot show that this method of addressing attention in the context of balance and gait training is effective in improving attention, balance, or ambulation. Other factors were involved in this patient's recovery. Other interventions, such as strength training, occupational therapy, and speech therapy, were applied simultaneously. The patient likely experienced some degree of spontaneous recovery as well. By structuring the patient's treatment plan to conform to the framework of transfer-appropriate processing, however, I hypothesize that the carryover of motor and attention skills learned in therapy into the patient's activities in school and the community was maximized.

Attention-related balance impairments in people with brain injuries may limit independence and safety during community ambulation. Physical therapists need to determine effective techniques to address attention as it relates to balance and ambulation in order to maximize patient recovery. In this case, the patient demonstrated impairments in attention along with physical impairments. Although no research on the relationship among balance, ambulation, and attention in subjects with this patient's diagnosis is available, other studies on subjects without impairments, (7,8,10) subjects with lower-extremity amputations, (9) and elderly people (8,11) suggest that balance does require attention and that a decrease in attention in patients with traumatic brain injury may be associated with decreased postural stability. (13) This case report outlines one method of addressing the patient's attention impairments in the context of balance and gait training. Continued research is needed to determine the interaction between balance and attention in patients with brain injury and to determine optimal evaluation and treatment variables for patients with decreased balance related to attention impairments.

Table.

Definitions of the Five Categories of Attention (14)

Type of
Attention     Definition

Focused       The ability to process and respond to specific
                information or input.
Sustained     The ability to perform an activity continuously
                over a period of time.
Selective     The ability to perform an activity in the
                presence of distracting stimuli, including
                ignoring irrelevant information.
Alternating   The ability to shift the focus of attention
                beween multiple stimuli.
Divided       The ability to respond to multiple stimuli
                simultaneously.

* The Hygenic Corporation, 1245 Home Ave, Akron, OH 44310.

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RS Tappan, PT, is a physical therapist at the Rehabilitation Institute of Chicago, Chicago, Ill. She was a physical therapist at CRS Rehabilitation Specialists, Skokie, Ill, when this case report was written. Address all correspondence to Ms Tappan at 4704 N Rockwell St, Chicago, IL 60625 (USA) ([e-mail]).

The author acknowledges the support of Alisa RG Halfman, MHS, CCC-SLP; Dena Kolosieke, OTR/L, MS; Ethan Stoller; and Georgia Tappan for their consultation (including review of manuscript before submission) on this project. The author also acknowledges the support of Beth Connelly, PT, MPT, who was a student at Northwestern University and participated in the treatment of this patient as part of her internship at CRS Rehabilitation Specialists.