Long-term locomotor training for gait and balance in a patient with mixed progressive supranuclear palsy and corticobasal degeneration.

Progressive supranuclear palsy (PSP) and corticobasal degeneration (CBD) are neurodegenerarive disorders. In one study, (1) the average annual incidence rate of PSP (new cases per 100,000 person-years) was 5.3 for people aged 50 to 99 years. Progressive supranuclear palsy is almost nonexistent before age 50 years, and its occurrence increases with age and is higher in men. (1) These neurodegenerative disorders are characterized by tau-positive inclusions in neurons and gila. (2) Axial and limb rigidity, supranuclear gaze palsy, balance and gait impairment, and frequent falls are the clinical hallmarks of PSP. (3,4) All of the "tauopathies" (ie, Pick disease, corticobasal degeneration, PSP, argyrophilic grain disease, and frontotemporal dementia with parkinsonism due to a mutation in the microtubule-associated protein tau) involve abnormal accumulation of intracellular tau protein that results in the development and accumulation of inclusions in neurons or glia that render the cells dysfunctional and ultimately cause cell death.

Corticobasal degeneration typically is manifested by asymmetric limb rigidity and apraxia (ie, the core features of "corticobasal syndrome") and other features such as dystonia, myoclonus, alien limb phenomenon, ideomotor apraxia, corticosensory loss, and tremor, (5,6) Some clients have features of both disorders. Postural instability ultimately occurs in both disorders, leading to frequent falls, injuries, and sometimes death due to traumatic brain injury or intracranial hemorrhage. (7,8) In one study of 24 cases of autopsy-proven PSP, (7) median survival time was 5.6 years (range=2-16.6). Onset of falls during the first year predicted a shorter survival time.7 Median survival time after onset of symptoms in a series of 14 cases of autopsyproven CBD was 7.9 years (range=2.5-12.5), and all clients exhibited prominent gait impairment prior to death.8 Gait impairment and the associated falls, therefore, are a major source of morbidity and mortality in people with PSP and CBD. (9,10)

Because no pharmacologic or rehabilitation therapy has been developed that alters the pathophysiology of tan-associated neurodegeneration, management is directed toward problem symptoms. The motor impairments of both disorders are particularly disabling. Pharmacotherapy with carbidopa/levodopa and with dopamine agonists typically is ineffective in managing the disorders; if modest improvement occurs, it is never prolonged. (3,5) Nonpharmacologic therapies such as physical therapy and occupational therapy are potentially useful, with the principal goals being the maintenance of functional ambulation and the reduction of falls and associated injuries.

There is very little published data regarding physical therapy approaches for people with PSP or CBD. Only one case study could be found that studied the effect of locomotor training on the function of people with either disease. This case study (11) showed a decrease in falls and improved balance for a person with PSP after 8 weeks of bodyweight-support treadmill training. Two other case reports of physical therapy intervention for people with PSP were found. (12,13) These reports described programs of strengthening and range-of-motion exercises for the trunk and limbs, coordination and balance activities, gait and transfer training, and fine motor activities. The patients improved in walking ability and safety over the course of therapy, but this improvement was dependent on heavy-weight ambulatory devices or a structured environment. However, 2 of the 3 patients in these case reports required nursing home placement due to deterioration in function within 8 months after discharge from therapy. A study of 24 clients with Parkinson disease (PD)14 demonstrated that bodyweight-support treadmill training improved gait speed after 12 sessions over a 1-month period, but this outcome was not retained at the 4-month follow-up.

Beyond these studies, there is a gap in the literature on the effectiveness of rehabilitation programs for people with parkinsonian disorders such as PSP and CBD. Because the prevalence of these disorders is low, case studies allow researchers and clinicians to present informative data to help others deal with these diseases.

Encouraged by the outcomes in a case study by Suteerawattananon et al (11) of a person with PSP and the availability of a physical therapist-supervised, community exercise class that included locomotor training on treadmills, the first author (TMS) offered an exercise and gait training intervention to a man with parkinsonian-like features who was eventually diagnosed as having mixed PSP and CBD. The present case report describes the longitudinal progression of several functional outcomes during the course of a long-term therapy program of strengthening and stretching exercises combined with locomotor training for this client. The locomotor training was done on a treadmill, with and without body-weight support, with the goals of improving balance and walking performance, as well as reducing falls. The treadmill program was not designed to induce cardiovascular adaptation. The therapy program was provided in both a community setting (a physical therapist-supervised exercise class for people with PD) and a university-based physical therapy clinic setting.

Case Description

Historical Features

The client had been a practicing dentist for 40 years and, during that time, worked with several types of metallic compounds, including gold, silver, amalgam, and mercury. He was right-handed and initially began experiencing changes in gait and limb coordination around 60 years of age. This was particularly notable when he was playing cuffing, with unsteadiness on the ice and struggling to curl as he aimed with the skip's broom. Over subsequent years, he began falling, particularly in the forward direction. By age 65 years, he also noted changes in his speech, with difficulty manipulating his tongue and lips. Others described his speech as "slurred." By age 68 years, he had fallen numerous times, sustaining many bruises and lacerations, and he reported occasionally choking on liquids. By age 70 years, his limb dyspraxia was increasing such that he could no longer button buttons, tie shoes, or perform other activities requiring fine motor dexterity. At age 71 years, he began exhibiting mild emotional lability and apathy. His cognition was viewed as preserved by himself and his family, with no significant features of memory, language, visuospatial, or executive dysfunction. Also absent were tremors, sialorrhea, dyskinesia, paresthesias, bladder and bowel incontinence, muscle twitching, and cramps. His medical history was otherwise remarkably benign. He used no prescription medications. There was no significant history of tobacco or alcohol use. There was no family history of any neurodegenerative disorder.

Neurologic Examination 

Initial neurologic examination (age 66 years) was notable, with a score of 32/38 on the Kokmen Short Test of Mental Status (15) with mild difficulties in attention, calculation, construction, and recall. His extraocular movements (vertical and horizontal saccades and pursuits) were essentially normal. He had moderately severe apraxia and rigidity in the left upper extremity, less so on the right side than on the left side, with corticosensory loss on the left side as well. He had moderate constructional dyspraxia in drawing complex figures. Increased tone (velocity-dependent resistance to stretch that a muscle exhibits) also was present in the lower extremities, but axial tone was normal. Alternating motion rates of the limbs were decreased, more so on the left side than on the right side. Deep tendon reflexes were brisk, but Babinski and Hoffman signs were absent. The palmomental reflex was present bilaterally. His stance was wide-based, and his stride was short with decreased arm swing, which was greater on the left side. A Romberg sign was present, and the pull test was positive. There was no tremor, myoclonus, dystonia, alien limb phenomenon, or mirror movements.

Ancillary Test Results

His initial assessment on neuropsychological testing demonstrated set maintenance problems, impaired working memory, impaired divided and sustained attention, and perseveration. Complex reasoning in a novel setting also was mildly impaired, but performance on all tests of language, visuospatial functioning, and delayed recall was normal. Magnetic resonance imaging and fluorodeoxyglucose positron emission tomography showed abnormalities in the parietofrontal cortex, which were maximal on the right side. All laboratory tests for treatable causes of cognitive impairment and motor dysfunction were negative or normal.

Assessment and Longitudinal Course

The constellation of features and findings initially was considered most consistent with CBD, albeit atypical. Longitudinal evaluations at yearly intervals over the subsequent years have demonstrated mild progression in his asymmetric rigidity and apraxia, spastic dysarthria, apraxia of speech, and prominent gait impairment. At each evaluation, the client and his family reported that he had frequent falls; on one occasion, a fall resulted in a deep laceration on his elbow that exposed the olecranon, requiring sutures. Cognition and behavior changed minimally. His axial muscle tone and extraocular movements remained intact until age 72 years when mild saccadic pursuits on vertical extraocular movement testing were evident and his eye-brink frequency decreased significantly. At age 72 years, a diagnosis of mixed CBD and PSP best characterized his symptoms and clinical findings.

Physical Therapist Examination and Evaluation

This client was referred in 2003 (at 70 years of age) to a university physical therapy program clinic after initially being recruited for a research exercise program for people with PD. At that time, the client was formally diagnosed with atypical CBD by a neurologist specializing in this rare disease at the Mayo Clinic. At the time of his initial visit for physical therapy intervention, he lived at home with his wife, who performed all household chores and helped the client with basic activities of daily living and instrumental activities of daily living. He relied on family members for community transportation. He no longer participated in recreational activities such as golf due to his impaired balance and apraxia. He chose to discontinue working with patients in his dental practice due to impaired balance and speech difficulties but continued to work 3 hours per week at the dental office performing bookkeeping and paperwork. The client also attended church and a social group once a week. A chronological index of his disease progression is shown in Table 1.

On initial examination, the client's sensation and kinesthesia were intact bilaterally, and passive range of motion and muscle strength (forcegenerating capacity) for all 4 extremities were within functional limits. Vestibular testing was not performed. The client did not report dizziness. The client walked without an assistive device and was unsteady, exhibiting a wide base of support and short steps. He was unable to perform a secondary cognitive task while walking. He could not negotiate stairs without using both of his hands on the rails, and he was independent but unsafe in transitional movements. Although his speech was dysarthric, he was able to communicate verbally.

Functional tests of balance and walking performance were administered every 2 months, beginning in February 2003, at the university clinic. Informed consent was obtained from the client to be photographed and videotaped when he came in for his first session. Testing was done by a team of 3 physical therapists who were experienced in administering the tests. The same therapist collected the same outcome measurements. The order of the outcome measures was rotated every session and included: 6-Minute Walk Test (6-MWT), (16) comfortable and fast gait speeds, (17) Berg Balance Scale (BBS), (18,19) Timed "Up & Go" Test (TUG), (20) forward functional reach (FFR), (21) backward functional reach (BFR), (21) right functional reach (RFR), (21) left functional reach (LFR), (21) and the Sharpened Romberg Test (SRT). (22) These tests were chosen because they are reliable and valid measures of balance and gait function in various populations of older adults. Using a cutoff score of 50, the BBS has a sensitivity of 85% for predicting future falls. (23) The FFR test used in people with PD has a low sensitivity of 30% in predicting future fails. (24) It was clear the client had numerous falls; thus, the balance measures were used to measure responsiveness of the intervention. High intrarater reliability has been reported for most of these measures in people with PD. (25) The lateral reach tests were added 1 year into the follow-up when asymmetrical limb apraxia became more apparent on the left side. The reliability and validity of data obtained with these measures has been documented for people with PD. (25-27) The client did not use a walker for the first 2 testing sessions, but thereafter he used a Do lomite 4-wheeled walker * for ambulation tests. He walked with the examiner, following to the side of and behind him, to ensure safety on the ambulation tests.

Community-based Group Exercise Intervention

Throughout the 2.5-year intervention period, the client participated in a physical therapist-designed exercise group for people with PD at a YMCA. His program was not altered from that of the other participants with the exception that he was closely supervised. This group met for 1 hour twice weekly, with a physical therapist or an occupational therapist always present during the sessions. The exercise session started with 20 minutes of lower-extremity and trunk stretching and a few lower-extremity strengthening exercises on a floor mat, followed by 10 minutes of upright balance and strengthening exercises and treadmill walking. On the Life Fitness treadmill (9500HR or 95Ti) ([dagger]) used at the YMCA program, the client walked backward for 10 minutes at a speed of 1.6 km/h holding on to the side rails and walked forward for 10 minutes at a speed of 2.25 km/h using unilateral arm support (Fig. 1). These speeds were as fast as the client could safely walk. The client started in the group in February 2003 (at age 70 years) and continued throughout the 2.5-year follow-up period. He rarely missed a group session.

[FIGURE 1 OMITTED]

University-based Individual Physical Therapy Intervention

Table 2 outlines the sequence of individual physical therapy interventions at the university clinic concurrent with the exercise group intervention. The individual treatment sessions were added, as available, throughout the 2.5-year period to increase the intensity of interventions addressing the client's postural instability. Figure 2 shows the treadmill and body-weight-support harness at the university clinic. The client's physical therapy intervention sessions at the university clinic in 2003 consisted of balance training, strengthening and stretching exercises, transitional movement practice, gait training, stair training, and safety education. These 14 sessions lasted 60 minutes each.

[FIGURE 2 OMITTED]

Each 2004 physical therapy intervention session at the clinic involved 40 minutes of treadmill training with the body-weight-support system. The client's falls while upright in all 4 directions indicated he was not aware of his limits of stability. Balance activities in 4 directions without the use of hand support provided movement control training. Speeds were increased to challenge him.

The client trained by walking in each of 4 directions on a Marquette Series 2000 treadmill ([double dagger]) supported by a Biodex Offset Unweighting System ([section]) set to unweight 10% of body weight. The sequence of walking direction (forward, backward, left, and right) was randomly determined at each session. To optimize the locomotion training, verbal or tactile feedback was given for proper upright posture while walking. The treadmill had a support bar in front of and to both sides of the client. He was instructed to use the bars to catch his balance, if needed, but to let his arms hang free as often as possible. The treadmill surface was set at a 0% grade, and the speed was increased until the client felt that he was at a safe comfortable pace. The walking time for each direction varied based on client tolerance. On average, the client was walking forward and backward for approximately 6 minutes in each direction at a speed of 2.3 km/h and 1.6 km/h, respectively. Walking sideways was much more difficult for the client. He achieved 6 minutes each way at 1.0 km/h. His heart rate varied from 80 to 120 bpm during sessions. Between walking in each direction, the client took standing rests on the treadmill.

Outcomes

Fall frequency declined over the 3 years from 2 falls per month to 1 fall per month. When graphed, the line of best fit equals y=-0.03x + 2.2. Figures 3 and 4 show longitudinal performance on a balance test and 2 walking tests, with a line of best fit calculated to indicate trends toward improvement or decline in test performance. The key for Figures 3 and 4 is given in Table 2 and indicates when the frequency and type of intervention changed. Figure 3 depicts the results of the functional reach tests in the 4 directions. For the first year, just FFR and BFR were tested. Starting February 2004, RFR and LFR were added to testing. Limits of stability in the forward direction (FFR) and to the right side (RFR) improved over time. Limits of stability in the backward direction (BFR) remained constant, whereas reach to the left side (LFR) decreased and then reached a plateau.

[FIGURES 3-4 OMITTED]

The coefficient of variation for the 4 reaching measures ranged from 17% to 25%. The coefficient of variation is an index of measurement variability, useful for comparing the relative stability of different clinical assessments. (28) The BBS test results showed essentially no change, with the slope of the line of best fit equaling y=0.07x + 31 (mean=31, SD=5, range=21-37) with a coefficient of variation of 15%. Figure 4 shows a decline in both gait speed and 6-MWT results. The mean difference over time between the client's mean comfortable and fast gait speeds was 0.16 m/s. The coefficient of variation was 10% for gait speed and 15% for the 6-MWT. Data collected on the TUG demonstrated the same decline as the data for gait speed and the 6-MWT. The client's mean TUG score was 25 seconds (SD=4). Over the follow-up period, TUG scores ranged from 21 seconds initially to 27 seconds at the end. The coefficient of variation for the walking tests and the TUG ranged from 10% to 15%.

Discussion

Most of the client's symptoms were consistent with underlying CBD, although the early and prominent gait impairment and frequent falls are far more suggestive of PSP, and thus our classification of this case as mixed CBD and PSP. The client's duration of symptoms (9 years, as of 2006) already exceeds the median survival time reported by people with CBD and PSP. He not only remains alive, but is ambulatory with a reasonable quality of life.

In this case report, we have shown functional outcomes throughout a 2.5-year physical therapy intervention period in an individual with CBD and PSP. The degree of variability in the outcome measurements over time (coefficients of variation ranging from 10% to 25%) make interpretation of the longitudinal data challenging. Thus, we chose a line of best fit through the data points to illustrate trends in test performance over time. In light of this client's chronic progressive neurological disorder, we believe that even graphic trends with a relatively flat line of best fit suggest treatment effectiveness. We have interpreted the stable or slightly positive trends for the BBS and the functional reach tests as support for this client's maintenance of balance function over a time period when decline could be expected. This maintenance or slightly improved balance function, coupled with the observed reduction in fall frequency, certainly is a positive outcome for this client.

The trend for declines in measurements of walking performance (gait speed, 6-MWT, TUG) is not as encouraging, especially because a main focus of the intervention was task-specific for walking. The progressive nature of the client's disorder and the effects of normal aging on walking performance are both likely factors contributing to these declines. However, these declines in performance on walking tests should not overshadow the fact that the client maintained independence with household ambulation with a 4-wheeled walker and maintained community ambulation with supervision and the walker. In addition, our client and his wife sought out the exercise program, and his readiness to exercise was evident from the start. The client reported that he was an active exerciser before his disease began, although he was not actively exercising when he entered the program. We believe that the motivation of our client and his wife to continue treadmill training and exercise on a regular basis was an important factor in maintaining his functional ambulation status.

No other literature was found with similar long-term data on the effects of rehabilitation intervention on the progression of the condition of people with these diseases. Minimal clinical differences on these tests for this population would help clinicians interpret the changes made with individual clients. In a case report by Suteerawattananon et al (11) of an 8-week intervention with bodyweight-support treadmill training, the client with PSP showed improvement in balance and gait and a decrease in falls. The difference between the present case report and the outcomes reported by Suteerawattananon et al may be explained by the difference in diagnosis, individualized therapy versus group therapy, or the length of the intervention between the 2 cases. In the present case, the question of whether the addition of weekly body-weight-support treadmill training in the university clinic enhanced the client's performance beyond the twice-weekly exercise program cannot be supported by the data. There were no clear trends suggesting an association between intermittent changes in intervention intensity and changes in functional performance over the follow-up period.

The decrease in this client's functional reach to the left side, but not the other directions, may be due to the fact that his left extremities, especially his left arm, demonstrated more apraxic movements than the right extremities. The last 2 measurement sessions demonstrated that his reach to the left side had plateaued around 10 cm compared with approximately 17 cm on the right side. This overall asymmetry in his left and right limits of stability is different from the left and right limits of stability of other people his age.25 Although we were not able to quantify the seriousness of the client's falls, most falls reported in 2003 and early 2004 caused nosebleeds, injuries requiting stitches, the simultaneous fall of a nearby person, or damage to nearby objects. His wife reported that most of his falls later in 2004 and in 2005 involved reaching from a sitting position for an object (eg, remote control) and usually did not involve injury. Thus, we believe that there was not only a decrease in fall frequency over the intervention period, but also a decrease in fall severity. In addition to treadmill training and exercise, undocumented cueing regarding safety was done in physical therapy intervention sessions and by family members. How this feedback affected the fall outcomes cannot be separated out from the effects of the exercise protocol.

The client continued to participate in the exercise group and treadmill training at the YMCA after the time of our reported follow-up. Based on the gait speed decline observed in our data, especially the decreasing distinction between fast and comfortable speeds, a decision was made to increase the treadmill speed for forward and backward walking without adding variability in the incline. As of January 2007, the client continued to show improvement in that he was walking backward on the treadmill at 1.6 km/h and forward on the treadmill at 3.20 km/h using only one upper extremity for support. He also continued to maintain his previous level of ambulation in his home and the community with the 4-wheeled walker. His falls since the last measurement period averaged one fall per month. Any declines in balance (as measured by falls, BBS, or functional reach tests in 4 directions) also would support the need for increasing intervention related to this problem.

Physical therapy intervention, as described here, appears to have contributed to maintenance of balance function and a slowed decline in walking performance for this client with mixed features of CBD and PSP. We suggest that physical therapists continue to support decision making regarding interventions with functional outcome measures. Another option to support maintenance of function would be referral to a personal trainer or other supervising exercise personnel, with intermittent physical therapy reassessments. It is worth noting that the community-based exercise group was led by a physical therapist with the assistance of an occupational therapist. The intangible effect of additional therapeutic information from the skilled professionals needs to be considered when exercise groups for people with balance disorders are lead by nontherapists.

Summary

Current medical interventions for clients with CBD and PSP have not been able to slow the progression of these diseases. This case demonstrates how a physical therapist-designed intervention, including exercise and locomotor training on a treadmill, may have contributed to maintenance of balance function and slowing of decline in walking function for a highly motivated client with CBD and PSP. The case also shows the value of functional outcome measures to validate and progress treatment interventions. We chose to use outcome measures (functional reach tests, TUG, gait speed) similar to those used in Suteerawattananon and colleagues' case study of a client with PSP (11) because of the lack of longitudinal outcomes with these diseases. The reach in 4 directions of the client in the present case report demonstrated the most positive change. The TUG, 6-MWT, and gait speed measurements demonstrated similar declines in this client, suggesting that only one of these measures might be necessary. The case highlights the evolving physical therapy role in providing ongoing intervention for people with chronic, progressive disorders.

Dr Steffen provided concept/idea/project design and data analysis. All authors provided writing and data collection. A special thanks to Will Cates, Ben Maschke, Beth Geboy, and Antoinette Spector, who assisted with data collection and treatment while they were physical therapist students at Concordia University Wisconsin, and to Lina La Licata for clerical support and Paul Wangerin for statistical support.

This work was presented at the World Parkinson Congress; February 22-26, 2006; Washington, DC.

This article was submitted June 16, 2006, and was accepted March 12, 2007.

DOI: 10.2522/ptj.20060166

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* Dolomite Home Care Products Inc, 50 Shields Ct, Markham, Ontario, Canada L3R 9T5.

([dagger]) Life Fitness, 5100 River Rd, Schiller Park, IL 60176.

([double dagger]) General Electric Medical Services, 3000 N Gradview Blvd, Waukesha, WI 53188.

[section] Biodex Medical Systems Inc, 20 Ramsay Rd, Shirley, NY 11967-4704.

TM Steffen, PT, PhD, is Professor, Program in Physical Therapy, Concordia University Wisconsin, 12800 N Lake Shore Dr, Mequon, WI 53097 (USA). Address all correspondence to Dr Steffen at: [e-mail].

BF Boeve, MD, Division of Behavioral Neurology, Department of Neurology, and Alzheimer's Disease Research Center, Mayo Clinic, Rochester, Minn.

LA Mollinger-Riemann, PT, MS, is Assistant Professor, Program in Physical Therapy, Concordia University Wisconsin.

CM Petersen, PT, DPT, is Assistant Professor, Program in Physical Therapy, Concordia University Wisconsin.

[Steffen TM, Boeve BF, MollingerRiemann LA, Petersen CM. Longterm locomotor training for gait and balance in a patient with mixed progressive supranuclear palsy and corticobasal degeneration. Phys Ther. 2007;87: 1078-1087.]

Table 1.
Chronology of Significant Events for the Client With Progressive
Supranuclear Palsy (PSP) and Corticobasal Degeneration (CBD)

Date            Significant Events

June 25, 1933   Date of birth
1959            Began clinical practice as a dentist
1997            Balance and speech became noticeably impaired
April 1997      Diagnosis of CBD by neurologist
December 1997   Stopped driving automobile
1998            Carbidopa/levodopa prescribed to manage balance
                  impairment
1999            First fall
1999            Stopped working with patients due to speech and
                  communicationproblems
1999            Carbidopa/levodopa discontinued
June 2000       Diagnosis of CBD confirmed at the Mayo Clinic
2001            Falls became an increasing problem
2005            Neurologist suspected mixed PSP and CBD

Table 2.
Sequence of Physical Therapy Interventions for Client With Progressive
Supranuclear Palsy (PSP) and Corticobasal Degeneration (CBD)

Date             Key for Vertical      Physical Therapy Interventions
                 Lines in Figures 3
                 and 4
January 2003                           Joined physical therapist-
                                         directed exercise group for
                                         people with Parkinson disease
                                         (1 hour per session, 2X/wk,
                                         began functional testing)
February 2003                          Participated in 14-wk
                                         rehabilitation program at the
                                         university physical therapy
                                         clinic

April 2003       - - - - - - - -       Started use of 4-wheel walker

May 2003                               University physical therapy
                                         clinic ended for 2003; client
                                         continued 2X/wk with exercise
                                         group
February 2004                          University physical therapy
                                         clinic resumed; client
                                         continued 2X/wk with
                                         exercise group

March 2004       - . - . -  . -        Began body-weight-supported
                                         treadmill training at the
                                         university physical
                                         therapy clinic

July 2004        . . . . . . . . .     University physical therapy
                                         clinic ended for 2004;
                                         client continued 2X/wk with
                                         exercise group

January 2005     - - - - - - -         University physical therapy
                                         clinic resumed

July 2005        - . . - . . - . . -   University physical therapy
                                         clinic ended for 2005; client
                                         continued 2X/wk with exercise
                                         group