BACKGROUND AND PURPOSE
Physical therapy management of individuals with Alzheimer disease (AD) and mobility limitations is complicated by the cognitive impairments that characterize this progressive disease.1,2 Impaired explicit memory, the conscious recollection of facts, ideas, and events, combined with a decreased capacity for explicit learning and error detection, limit the methods by which patients can relearn mobility activities. Physical therapists (PTs) often use explicit verbal instructions, corrective feedback, mental practice, and discovery learning to facilitate improved mobility. Because these methods require patients to remember rules for correct performance and detect errors in performance, they may not be effective to use in individuals with AD, especially those with significantly impaired explicit memory.
A growing body of research suggests that individuals with AD may learn best under conditions that facilitate the use of the implicit memory system.2–4 Implicit learning requires the use of the implicit memory system, which remains relatively intact until the late stages of AD.3,4 Implicit memories are formed with recurrent practice of a task and do not require that the learner develop conscious rules to guide performance.5 When a patient has learned a skill implicitly, a relatively stable change in knowledge or behavior is observed but the patient may not have conscious awareness of either what was learned or specifically how it was learned.
Early research on motor learning in individuals with AD demonstrated that high-repetition, low-variability practice conditions optimized implicit learning of laboratory-based motor tasks, such as mirror tracing tests,6 maze tests,7 tracking tasks,8 serial reaction time task,9 and tossing a beanbag at a target.10 Because these laboratory-based tasks do not simulate the complex functional activities that many patients with AD need to learn or relearn, more recent studies of motor learning in AD have focused on the application of implicit learning principles to the training of individuals with AD in “real-life” functional activities in clinical or naturalistic environments.11,12 Individuals with AD have demonstrated improved performance of sequential instrumental activities of daily living and mobility tasks when trained under implicit learning conditions.11,13
Errorless learning (EL), a learning paradigm based on the implicit learning principles of high-repetition and low-variability practice conditions, is a promising rehabilitation strategy for PTs to use in managing patients with AD.14,15 In the EL paradigm, practice conditions are designed to prevent or minimize inaccurate performance during the learning process. Because individuals with AD may not be able to form conscious rules for correct performance of a task (ie, explicit learning), they are not likely to benefit from making errors during practice or receiving corrective feedback. Instead, repetitive practice without errors may consolidate memory of correct performance within the implicit memory system. Therefore, it is thought that EL conditions may be preferable to trial-and-error learning conditions in individuals with AD.11,16 Because errors are eliminated or reduced in EL training sessions, an additional benefit of EL is that patients are successful throughout the session, which may reduce frustration and increase participation by the patient. Interventions based on the EL paradigm have been effective in teaching individuals with AD to perform sequential instrumental activities of daily living and find the correct route in a residential facility.11,17
Spaced retrieval (SR) is a specific memory training technique that utilizes the implicit learning principle of high-repetition practice to facilitate recall of facts or strategies.18–20 On the basis of the EL paradigm, SR training sessions are designed to promote accurate recall of information over progressively longer time intervals and reduce the likelihood of recall errors. During SR training sessions, a therapist provides the patient with a prompt question or cue and the correct verbal or behavioral response. As the patient successfully recalls the correct response to the prompt question/cue, the therapist systematically increases the recall time interval of future trials. If a patient's response to a prompt question/cue is inaccurate, the therapist decreases the time interval between presentation of the correct information and response by the patient on the next trial. The SR technique has been demonstrated to be effective in teaching individuals with AD to use a calendar as a memory aid for dates and events,21 use a mobile phone,22 and improve feeding and eating behaviors.23 Although primarily used clinically by speech-language pathologists and cognitive therapists, SR may be an effective adjunct to mobility training interventions to facilitate recall of the sequences or strategies of a mobility activity.24
In clinical practice, PTs may encounter barriers to integrating the principles of implicit learning and, more specifically, EL into the physical therapy management of patients with AD. The real-world constraints of clinical practice include limited treatment times, behavioral and neuropsychological symptoms that are common in the later stages of AD, and unpredictable clinical and naturalistic environments. These constraints may limit the feasibility of task training under implicit learning conditions. The purpose of this prospective case series is to describe the application of implicit learning strategies, including high-repetition practice, EL, and SR, to the physical therapy management of individuals with moderate AD.
Patient Description and Selection
Three residents were recruited from the memory care unit or assisted living unit of a senior retirement center. Two nurse managers identified residents who they thought would benefit from physical therapy intervention and who met the inclusion criteria of (1) a diagnosis of probable AD per primary care physician, (2) ability to sit unsupported for 5 minutes, (3) ability to follow a 1-step simple motor command in English, and (4) a decline in mobility in the last 6 months. Persons were excluded if they had a history of any severe cardiopulmonary, musculoskeletal, or other neurological condition that may adversely affect postural stability and ability to participate in therapy sessions, a diagnosis of vascular dementia or chronic dementia other than probable AD, or a history of chronic alcoholism or psychiatric disorder that may affect cognitive function, or were currently participating in a physical rehabilitation program. All study protocols were approved by the institutional review boards of the University of Alabama at Birmingham and the University of South Alabama. Each participant and her legally authorized representative provided written informed consent for participation. The physician for each participant provided a written physician's referral for physical therapy prior to the initial examination.
The PT collected demographic, medical, and social history from the patient, family members, nursing staff, and medical charts kept at the facility. The PT administered the Mini-Mental State Examination (MMSE)25 on the date of the initial examination to assess current cognitive function. The PT also rated each participant on the Functional Assessment Staging Tool26 with the information provided by the nursing staff to classify the level of dementia. Characteristics of each patient are summarized in Table 1.
The initial PT examination and treatment sessions were conducted in each patient's naturalistic setting, which included a private bedroom and bathroom and common areas (ie, hallway and dining room). A naturalistic treatment setting was chosen rather than a private clinic area because familiar settings are thought to decrease stress and behavioral symptoms in individuals with dementia, which may facilitate greater learning.27
Mobility and balance outcome measures were administered to each patient during the initial evaluation and final treatment session. The Timed Up and Go (TUG) Test28 and self-selected walking speed (SSWS) were chosen to objectively measure mobility because (1) the test-retest reliability and minimal detectable change of these measures have been determined in the AD population29 and (2) the measures are feasible when minimal equipment and space are available. The TUG Test was administered and scored using the same procedure as that described by Ries et al.29 Patients were instructed to stand from an armed chair, walk 3 m as quickly and safely as possible, turn around an orange cone placed at the 3-m mark, walk back, and sit down. The TUG Test score was calculated as the mean of the scores from 2 test trials. Self-selected walking speed was measured over a distance of 15 feet, with acceleration and deceleration occurring outside the measured distance. Self-selected walking speed was calculated as the mean speed of 2 test trials. Other mobility and balance outcome measures were administered on the basis of the individual patient's baseline functional status. The clinical decision-making process for selection of these measures is discussed with each individual case.
The PT designed an individualized plan of care that included training of mobility and balance tasks that directly addressed individual patient impairments and activity limitations. The PT selected tasks that were functionally relevant and used objects familiar to the patient in an effort to facilitate active participation by the patient and reliance on implicit memories of prior motor learning.24 Feedback and practice, 2 variables that affect motor learning, were manipulated to facilitate implicit learning and to minimize efforts by the patient to learn the tasks using the impaired explicit memory system. The PT intentionally minimized verbal instruction and did not explicitly state the rules or goals of task performance. No specific terminal feedback was provided to the patient other than general encouragement (ex, “Good job!”). The number of tasks addressed by the plan of care was limited so that each task could be practiced multiple times during each session. The practice schedule was blocked in the same order each session to limit variation and provide a familiar routine for the patients. Rehabilitation strategies that promote EL were incorporated into the task training, when possible (see Table 2).
It was decided prospectively that each patient would receive 12 physical therapy visits over a period of 4 weeks. This visit frequency and duration of episode of care were chosen to simulate the real-world constraint of limited treatment frequency and duration due to third party payment practices. Based on clinical experience, this visit frequency and duration of episode of care are typically reimbursed by third party payers if medical necessity and skilled PT services are adequately documented. On the basis of the training frequency and the number of practice trials reported in published studies of motor learning in AD,8,11 it was decided that 12 visits would be sufficient to provide high-repetition practice to facilitate implicit learning of the intervention tasks. Treatment sessions were to last no longer than 60 minutes to simulate the time constraints in a typical clinical practice. The PT did not seek payment from any party for physical therapy services provided to these patients.
The patient was a 90-year-old woman who resided in the memory care unit. She had fallen 1 month prior to the initial examination. A staff member found the patient on the floor in a narrow space between her bed and wall. Her medical history included placement of a demand pacemaker and long-standing hypertension, which was recently uncontrolled and required a change in her antihypertensive medications.
The patient's son resided locally and took her to church every Sunday. He reported that she had recently become unsteady when walking in the church. His goal for the patient was to improve her ability to walk through the busy church. The nursing staff reported that the participant was independent in all activities of daily living (ADL). She ambulated independently without an assistive device throughout the memory care unit. During the initial interview with the patient, she demonstrated limited recall of recent life events, reported no problems with mobility, and did not recollect any previous falls.
Clinical Impression and Examination
Given the patient's impaired declarative memory as reflected in the patient interview, task-training interventions to improve mobility using implicit learning strategies were warranted. Further clinical examination was conducted to identify underlying impairments and specific mobility limitations that would be addressed by the plan of care.
The patient scored 14 of 30 on the MMSE and was alert and oriented to self and place. She was inconsistently able to follow a multiple-step motor command. The patient was able to roll independently in all directions on her bed. Supine to sit and sit to stand were independent when performed as distinct transitions. However, when the patient was asked to get out of bed, she quickly transitioned from supine to standing positions, requiring contact guard assistance due to excessive postural sway in initial standing. Sit to stand from the bedside chair and toilet was independent, although it was noted that the patient positioned her legs against the chair for support as she stood.
The patient ambulated independently in her room without the use of an assistive device, but she was observed to hold onto the wall or bed when she walked in the narrow area between her bed and wall. She maintained her balance while performing ADL at her sink, but she was observed to have a wide base of support (BOS). The patient ambulated independently from her bedroom to the dining room without signs of exertion. However, she stopped walking when a cognitive task (ie, conversing with the PT or other residents) was introduced.
On initial examination, the patient's SSWS was 1.38 m/s, which was significantly faster than norms for the mild-moderate AD population.29 Her score on the TUG Test was 12.94 seconds, slightly less than the cutoff score of 13.5 seconds, which is predictive of high fall risk in community-dwelling older adults.33 The Berg Balance Scale (BBS)34 was administered to objectively measure the patient's static and dynamic standing balance at baseline and after the intervention. The BBS is a valid and reliable measure that evaluates 14 mobility and balance tasks that are relevant to the participant's daily life.34,35 The patient scored a 41 of 56 on the BBS, indicating a minimal risk for falls.36 During administration of the BBS, she had difficulty standing with her feet together, was unable to stand in a tandem position, and required physical assistance to regain her balance when placing her foot on a stool.
Clinical Impression and Intervention
The patient's impaired static and dynamic standing balance was most evident in mobility tasks that required a narrow BOS or attention to a concurrent cognitive task. Therefore, mobility and balance intervention tasks were selected that could be performed under dual-task conditions and challenged the patient's balance by requiring a narrow BOS. During task training, the PT used modeling, feed-forward instruction, and concurrent tactile cues. The PT decided to use the EL-based strategy of SR to teach the patient to slow the transition from supine to standing, as the patient consistently demonstrated postural instability upon initial standing. The patient successfully completed a short verbal recall screening test, indicating that she was an appropriate candidate for the use of SR.19 Because no specific protocol for SR training has been demonstrated to be most effective, the PT created a protocol for this patient based on successful approaches described in the literature and consideration of time constraints in PT practice.19,20,37 Spaced retrieval training sessions lasted approximately 30 minutes. The PT asked the patient, “What should you do before you get out of bed?” The patient was instructed to verbally respond, “Sit for a little bit.” Time intervals between verbal recall tests were systematically increased after each successful trial. Time intervals were 5, 10, 20, 40, 60, 90, 120, 150, and 180 seconds. After 3 minutes, subsequent intervals increased by 1 minute. After 6 minutes, subsequent intervals increased by 2 minutes. When the patient responded incorrectly, the time interval of the next trial was reduced to that of the previous successful trial. When the patient was able to verbalize the correct response 24 hours after the last SR session, the PT transitioned the training sessions to include practicing the associated motor task of a supine-to-stand transfer with prolonged sitting of at least 30 seconds.
The interventions, specific implicit learning strategies incorporated into the interventions, and rules for progression for this patient are summarized in Table 3.
Patient 1 participated in all 12 planned treatment sessions. Functional outcome measures were administered again during the final session and are reported in Table 6. Her score on the BBS was 50 of 56. The increase in BBS score from baseline was 9 points, which is greater than the reported minimal detectable change of 7.4 points.35 Her scores on the TUG Test and SSWS did not change significantly from baseline. Initially, the patient was unable to verbalize that she was to “sit for a little bit” before rising to stand from supine on a 5-second recall test. By the fourth session, she could verbally recall this correct response 24 hours after the presentation of the information, but she did not spontaneously perform the associated motor task (ie, sit on the edge of the bed before standing). On the sixth session, she consistently demonstrated correct performance of both verbal recall and motor performance. On subsequent visits, she was able to verbally recall the correct response without prompting but did not spontaneously perform the transition correctly.
The patient was an 89-year-old woman who resided in the memory care unit. The nursing staff reported that she had fallen several times over the past several months after being hospitalized with pneumonia. Her medical history included osteoporosis, severe kyphoscoliotic deformity, coronary artery disease, hypertension, anxiety, and severe bilateral hearing loss. She wore bilateral hearing aids. She was prescribed an anxiolytic due to occasional episodes of anxiety and agitation.
The patient was widowed and had no family in the area. The staff reported that she ambulated independently with a wheeled walker from her bedroom to the dining room for meals 3 times per day but rarely left her room otherwise. The patient was reportedly independent in all ADL. During the initial patient interview, she denied any history of falls but stated that she always used a walker for standing and walking.
Clinical Impression and Examination
Like patient 1, this patient demonstrated significant impairments in declarative memory, suggesting that she would benefit from the use of implicit learning strategies. Based on her history of anxiety and agitation, there was some concern that the patient would not participate actively in the examination because of its unfamiliar nature.
The patient scored 12 of 30 on the MMSE and was alert and oriented to self and her state of residence only. The patient had a severe hearing impairment that was still evident with the use of hearing aids. She became anxious when she could not understand verbal instructions. The patient was able to follow a motor command with written instructions. She had a severe fixed thoracic kyphosis but was able to achieve a horizontal visual gaze by actively extending the cervical spine. The patient was able to roll in all directions on her bed and transitioned supine to and from sitting independently. She required multiple attempts to transition from sit to stand. During stand to sit, she did not use her upper extremities for support, and the descent was uncontrolled. Although the patient grimaced upon sitting, she verbally denied pain during the transition.
The patient ambulated independently with a front-wheeled walker. On initial examination, the patient's SSWS was 0.70 m/s, and her TUG Test score was 17.39 seconds. The patient performed both tests with a front-wheeled walker. Both SSWS and TUG Test score indicated a high fall risk.33,38 The Performance-Oriented Mobility Assessment (POMA)39 was also administered to measure the patient's performance in gait and balance. Given the patient's severe hearing loss and history of osteoporosis, it was decided that the POMA was more appropriate than the BBS to use with this patient. The POMA requires fewer verbal cues than the BBS and does not require the patient to pick an object off the floor, which could potentially injure the osteoporotic spine if performed incorrectly. The patient scored 8 of 16 on the balance section (POMA-b) and 9 of 12 on the gait section (POMA-g). The patient performed the gait section with a front-wheeled walker. Her combined score (POMA-total) was 17 of 28, indicative of high fall risk.39 During administration of the POMA, she lost her balance in a posterior direction upon mild external perturbation (ie, sternal nudge) in static standing, demonstrating an inefficient motor ankle strategy.
Clinical Impression and Intervention
Specific mobility and balance tasks were selected for intervention to improve the patient's motor ankle strategy in response to perturbation, controlled descent of the stand to sit transition, and gait speed. Poor eccentric control of the stand-to-sit transition was a primary concern due to both increased fall risk and increased risk of vertebral fracture in this patient with osteoporosis. Given a hearing impairment that limited the effectiveness of verbal instruction, the PT used modeling, concurrent tactile cues, and hand-over-hand guidance to promote correct performance and implicit learning of the tasks. The PT decided to use an SR strategy to teach the patient to use her upper extremities for support during the stand-to-sit transition. The PT developed an SR training protocol similar to the one used with patient 1. Although the patient successfully completed the SR screening test when the prompt question and correct response were provided to her in a written format, she demonstrated agitation during the SR intervention on the second treatment session. At that time, the PT decided to replace the SR strategy with modeling and hand-over-hand guidance, as these were better tolerated by the patient. The mobility and balance tasks, specific implicit learning strategies incorporated into the task training, and rules for progression are summarized in Table 4.
Patient 2 participated in each of the 12 planned treatment sessions over 4 weeks, although 2 sessions were rescheduled because of the patient's refusal to participate. Functional outcome measures were administered during the final session and are reported in Table 6. Her score on the POMA-total increased from a 17/28 on initial evaluation to a 21/28 because of an increase of 4 points on the POMA-b. This change was 1 point less than the reported minimal detectable change of 5 points for the POMA-total.40 Her score on the TUG Test and SSWS did not change significantly. During the final session, the patient was observed to spontaneously place her hands on her bedside chair during the stand-to-sit transition on 3 of 3 trials. Descent was controlled, and the patient did not grimace upon sitting.
The patient was a 95-year-old woman who resided in the assisted living unit. Although she had no history of falls, the nursing staff reported that the patient had recently demonstrated increased shuffling and slower gait, and shortness of breath when walking to the dining room. Her medical history included hypothyroidism, urge incontinence, and hypertension.
The patient was widowed and had 1 daughter who agreed with the nursing staff that her mother's mobility had recently declined. The daughter's goal for the patient was to maintain her ability to walk independently. The nursing staff stated that the patient ambulated independently in her room without a device but used a 4-wheeled walker to ambulate to the dining room for meals 3 times per day. The patient required assistance for dressing and bathing but occasionally refused to participate in assisted ADL.
Clinical Impression and Examination
As with the first 2 patients, this patient also demonstrated significant impairments in declarative memory, suggesting that she would benefit from the use of implicit learning strategies. Based on her history of refusal to participate in assisted ADL, there was some concern that the patient would not participate actively in the PT examination.
The patient scored 11 of 30 on the MMSE and was alert and oriented to self and season of the year only. The patient was able to follow a motor command consistently. She demonstrated impairments in expressive language, occasionally having word-finding difficulty. The patient was able to roll in all directions on her bed. Transitions of supine to and from sit, and sit to and from stand, were independent when she used her upper extremities for support.
The patient ambulated independently in her bedroom without a device with short step lengths noted bilaterally. Neither swing foot passed the toe of the stance foot, although both feet cleared the floor during swing phase. The patient ambulated independently in the common hallway with a 4-wheeled walker. No significant differences in the gait pattern were noted with the use of a walker. On initial examination, the patient's SSWS with the use of a walker was 0.52 m/s. The patient's score on the TUG Test without the use of an assistive device was 18.61 seconds. Her TUG Test score and SSWS indicated a high fall risk.33,38 The BBS was selected as a measure of static and dynamic balance. Her score on the BBS was 28 of 56, indicating a high fall risk.36 During administration of the BBS, she was noted to have difficulty with tasks that required a narrow BOS. She required physical assistance to keep from falling while attempting to place foot on a stool or stand in a tandem position.
Clinical Impression and Intervention
It was hypothesized that the patient's static and dynamic standing balance impairments contributed to decreased gait speed and short step length. Her difficulty maintaining a narrow BOS and single-limb stance was thought to result in a prolonged double-stance time in gait. Therefore, mobility and balance tasks were selected which addressed these impairments. The PT used feed-forward and concurrent verbal instruction to promote implicit learning of the tasks. The mobility and balance tasks, specific implicit learning strategies incorporated into the task-training, and rules for progression for Patient 3 are summarized in Table 5.
Patient 3 participated in 10 of the 12 scheduled treatment sessions over 4 weeks, with a progressive decline in active participation noted throughout the episode of care. Treatment sessions were structured on the basis of the patient's willingness to participate in a particular task. At times, engaging the patient in verbal reminiscence of an early life event was effective in increasing the patient's participation in a motor task. Functional outcome measures were administered during the last 2 sessions and are reported in Table 6. Her BBS score improved, although the 5-point change from baseline was less than the minimal detectable change of 7.4 points reported for the BBS.35 Her TUG Test score and SSWS did not change significantly.
The implicit learning principle of high-repetition practice proved to be the most feasible to integrate into the plan of care for all 3 patients. Addressing the mobility limitations most meaningful to the patient and caregivers and limiting the number of tasks addressed in each session allowed for higher-repetition practice of each task. Selecting functionally relevant tasks that incorporate strengthening and balance components may limit the number of interventions that a PT needs to address in a treatment session, thereby allowing more time for high-repetition practice. For example, patient 1 performed step-ups on her bathroom scale that incorporated hip and knee extensor strengthening and single-limb stance into a single task that was functionally relevant for the patient. She seemed to enjoy watching how the numbers displayed on the scale fluctuated between steps, potentially increasing her compliance with the high-repetition practice.
Applying the EL paradigm was not always feasible, as some mobility and balance tasks were more readily trained under EL conditions than others, depending on the characteristics of the task. The discrete task of the stand-to sit-transition practiced by patient 2 was more easily modified to practice under EL conditions than the continuous task of walking with increased step length practiced by patient 3. Tasks that were already being performed by the patients in their daily routine, such as the supine-to-stand transition practiced by patient 1, were performed under EL conditions during the treatment sessions. However, the patient also performed the task with errors throughout the remainder of the day when no caregivers were present, potentially negating the effect of the EL practice during the treatment sessions. It seems that discrete tasks and sequential tasks with discrete steps that are not practiced outside of therapy sessions in “error-full” conditions are most applicable for training under EL conditions.
Although the EL-based technique of SR has received little attention in the physical therapy literature, the outcomes from this case series suggest that SR may be effective in teaching patients with AD new mobility strategies. By the fourth session, patient 1 was able to successfully recall that she should sit on the edge of bed during the supine-to-stand transition after a 24-hour delay in practice. Performing the desired strategy resulted in improved stability upon initial standing. However, her spontaneous performance of this strategy during the supine-to-stand transition remained inconsistent throughout the episode of care. Training the patient's caregivers to practice the technique throughout the day may have increased her learning of the desired mobility strategy. Research suggests that caregiver participation in SR training and carry-over into the patient's daily routine may be a key component to the success of the SR technique.41,42 Unfortunately, caregiver participation was not feasible in the case of patient 1, as caregiver staffing of the memory care unit was inconsistent throughout the episode of care. Further research is needed to determine to what extent mobility skills can be relearned by individuals in various stages of AD using SR techniques.
Although intervention effectiveness cannot be determined in a case series, it is worthy to note that all patients improved their performance on objective measures of balance, although only one exceeded the minimal detectable change for either the BBS or POMA. No significant clinical change was observed in any patients on the TUG Test or SSWS. Given that individuals with AD are not able to transfer learning of 1 task to another, it may be that the TUG Test and SSWS measures are not sensitive to the motor learning that occurred in these patients. For example, on the final treatment session, patient 2 consistently used her upper extremities for support when performing the sit to and from stand transitions in her bedside chair. However, she did not use this mobility strategy during testing on the same day when performing the TUG Test with a different chair in a hallway.
To date, few studies in the physical therapy literature have attempted to bridge the gap between motor learning and cognitive rehabilitation research on AD and the physical therapy management of this patient population. The heterogeneity of the AD population in the domains of cognitive, physical, and behavioral function makes it difficult to generalize the research findings of well-controlled studies with stringent inclusion criteria to individual patients often encountered in clinical practice. The patients described in this case series would likely be excluded from many AD studies on the basis of their medical comorbidities, behavioral symptoms, or disease severity. However, this case series demonstrates that it is feasible to apply the knowledge gained from these studies of implicit learning to the physical therapy management of complex patients in the moderate to moderately severe stages of AD. Limitations of this case series should be acknowledged and include a small sample size, lack of neuropsychological testing to confirm the diagnosis of AD, and an unblinded assessor. Further research on the effectiveness of EL, SR, and other rehabilitation strategies that facilitate implicit learning of mobility skills in patients with AD is needed to promote optimal physical therapy outcomes in this patient population.
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© 2014 The Section on Geriatrics of the American Physical Therapy Association.