HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Full Text (PDF) All Versions of this Article: ptj.20070302v1 88/12/1460    most recent Submit a response Alert me when this article is cited Alert me when Rapid Responses are posted Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Zampieri, C. Articles by Di Fabio, R. P Search for Related Content PubMed PubMed Citation Articles by Zampieri, C. Articles by Di Fabio, R. P Related Collections Balance Training Gait and Locomotion Training Balance Parkinson Disease and Parkinsonian Disorders Social Bookmarking                      What's this?

Balance and Eye Movement Training to Improve Gait in People With Progressive Supranuclear Palsy: Quasi-Randomized Clinical Trial

C Zampieri, PT, PhD, is Postdoctoral Fellow, Department of Neurology, University of Maryland School of Medicine, 22 S Greene St N4W46, Baltimore, MD 21201 (USA). She was a doctoral student in the Department of Physical Medicine and Rehabilitation, University of Minnesota, Minneapolis, Minnesota, when the study was conducted
RP Di Fabio, PT, PhD, is Professor, Department of Physical Medicine and Rehabilitation, and a senior faculty member of the Graduate Programs in Neuroscience, University of Minnesota

Address all correspondence to Dr Zampieri at: czampieri{at}som.umaryland.edu

Submitted October 5, 2007; Accepted August 4, 2008

	Abstract

 
Background and Purpose: Although vertical gaze palsy and gait instability are cardinal features of progressive supranuclear palsy (PSP), little research has been done to address oculomotor and gait rehabilitation for PSP. The purpose of this study was to compare the benefits of a program of balance training complemented with eye movement and visual awareness training versus balance training alone to rehabilitate gait in people with PSP.

Participants: Nineteen people moderately affected by the disease were assigned to either a treatment group (balance plus eye movement exercises, n=10) or a comparison group (balance exercises only, n=9) in a quasi-random fashion.

Methods: The baseline characteristics assessed were diagnosis (possible versus probable), sex, age, time of symptom onset, dementia, and severity of symptoms. Within-group, between-group, and effect size analyses were performed on kinematic gait parameters (stance time, swing time, and step length) and clinical tests (8-ft [2.4-m] walk test and Timed "Up & Go" Test).

Results: The within-group analysis revealed significant improvements in stance time and walking speed for the treatment group, whereas the comparison group showed improvements in step length only. Moderate to large effects of the intervention were observed for the treatment group, and small effects were observed for the comparison group. The between-group analysis did not reveal significant changes for either group.

Discussion and Conclusion: These preliminary findings support the use of eye movement exercises as a complementary therapy for balance training in the rehabilitation of gait in people with PSP and moderate impairments. Additional studies powered at a higher level are needed to confirm these results.

	Introduction

Top Abstract Introduction Method Results Discussion Conclusion Appendix 1. Appendix 2. Appendix 3. Appendix 4. References

 
Progressive supranuclear palsy (PSP) is the most frequently occurring form of atypical parkinsonism.¹ The average survival time is 7 years; however, there have been reports of neuropathologically confirmed cases of survival of up to 11 years² or 16 years.³ Gait and mobility problems are among the most common early features of this disease,¹ and gait deficits progress rapidly.⁴ Oculomotor problems, such as vertical gaze palsy, also known as "slowness of saccades,"^3,5,6 and deficits in vestibuloocular reflex suppression, are also symptoms of PSP.^7–9

Gait problems in PSP are different from those in Parkinson disease (PD). Although freezing and festination are very common in PD,¹⁰ these features are typically not observed in PSP, although there have been reports of freezing in a few cases in which the diagnosis was confirmed postmortem.¹¹ The typical gait in PSP is unstable, with frequent falls,¹ and is clinically described as clumsy, resembling the gait of a drunken sailor.¹¹

There are several approaches to gait rehabilitation in PSP. There have been reports of balance training with a tiltboard,¹² eye-head movement strategies to improve awareness and safety during ambulation,¹² strength (force-generating capacity) training with resistive and isokinetic exercises,¹³ coordination exercises,^12,13 gait training over ground,¹³ and body-weight–supported treadmill training.^14,15 However, the outcomes were primarily qualitative, reflecting the opinions of therapists and patients. Improvement in standing balance¹² and safer ambulation were the main observations.^12,13 Quantitative measures were reported in only one study and included increases in walking speed, cadence, and step length.¹⁵

Rehabilitation of gait in PSP should also include oculomotor training because the ability to control eye movements is directly related to the control of gait and safe ambulation. Vision plays a critical role in the control of locomotion because it provides input for anticipatory reactions of the body in response to constraints of the environment.¹⁶ Anticipatory saccades occur normally in situations that involve changing the direction of walking¹⁷ or avoiding obstacles.¹⁸ When downward saccades are not frequently generated during obstacle avoidance tasks, there is an increase in the risk for falling. Di Fabio et al¹⁹ reported that elderly people at a high risk for falling generated fewer saccades than their low-risk counterparts during activities involving stepping over obstacles. In addition, foot clearance trajectories were asymmetric in the high-risk group, with the lag foot trajectory being significantly lower than the lead foot trajectory. Similar behavior has been observed in patients with PSP during stair-climbing activities. Di Fabio et al²⁰ recently reported that patients with severe oculomotor limitations had a lower lag foot trajectory than those with mild oculomotor limitations.

Aside from the influence of oculomotor control on stepping kinematics, deficits in cognition, especially attention and executive functions, also have been linked to an increased risk for falling in elderly people^19,21 and people with Alzheimer disease²² and PD.²³ In PSP, in particular, a strong correlation has been found between the ability to suppress the vertical vestibuloocular reflex and certain domains of cognition: attention and visual awareness.⁹

Even though evidence has shown that gaze limitations have a strong impact on locomotion, the effects of eye movement training have never been investigated in a group of subjects with PSP. The purpose of this study was to compare the benefits of a program of balance training supplemented with oculomotor and visual awareness training versus balance training alone for gait rehabilitation in PSP. We hypothesized that greater improvements in gait would be observed for subjects who received balance and eye movement exercises than for subjects who received balance training alone.

	Method

Top Abstract Introduction Method Results Discussion Conclusion Appendix 1. Appendix 2. Appendix 3. Appendix 4. References

 
Design Overview

A quasi-randomized 2-group pretest-posttest crossover design was used to study the effects of balance and eye movement (balance + eye) training and of balance training alone on gait. Twenty people were alternately assigned to either a treatment group (balance + eye training) or a comparison group (balance training only), except for allocation based on geographical distance from the testing center (several people who resided in distant locations and were unable to participate in the crossover component of the study were assigned to a treatment group that did not cross over). For validation of the allocation procedure, the equivalence of baseline characteristics in the comparison and treatment groups was evaluated (see discussion below). The crossover component of the larger study is not presented here. Only the pretest-posttest phase was analyzed for the present study. At the beginning of the study, there were 10 participants in each group; however, 1 individual dropped out because of a urinary tract infection, leaving the comparison group with 9 participants.

The baseline characteristics assessed were diagnosis (possible versus probable), sex (male versus female), age, time of symptom onset, dementia (with the Mini-Mental State Examination [MMSE] score),²⁴ severity of symptoms (with the Unified Parkinson's Disease Rating Scale motor component [UPDRSm] score),²⁵ and the PSP Rating Scale.²⁶ The UPDRSm, originally specific for PD, has been tested for PSP as well and has shown high internal consistency (Cronbach alpha=.90).²⁵ The PSP Rating Scale has good interrater reliability, with an intraclass correlation coefficient of .86.²⁶

Participants

Twenty people with PSP and living in the community were enrolled in this study. Participants were recruited through the University of Minnesota Movement Disorders Clinic, local PD clinics, and the PSP Society. Recruitment occurred over a period of 2 years. To be included, participants needed to have a possible or probable diagnosis of PSP according to the criteria established by the National Institute of Neurological Disorders and Stroke.²⁷ Other inclusion criteria were the ability to walk short distances independently (with an assistive device when necessary but no direct assistance from another person), an MMSE score of 23,²⁴ and a corrected far visual acuity of at least 20/80. No changes in medications were implemented for this investigation. All participants provided written informed consent prior to enrollment.

Intervention

The intervention was performed by a trained group of researchers supervised by the investigators of this study. Researchers administering the intervention were aware of group assignments. A different group of researchers involved with baseline and postintervention data collection and analysis were unaware of group assignments. The intervention sessions were delivered to each participant individually. All treatment sessions took place in the Motion Analysis Laboratory, Department of Physical Medicine and Rehabilitation, University of Minnesota. The location of the intervention sessions minimized sound and visual distractions. Participants in both groups received the intervention for 1 hour 3 times per week for 4 weeks. The duration of the intervention was chosen on the basis of literature reporting rehabilitation for PD^28,29 and on standard practice adopted by local rehabilitation clinics. Each group of participants received common and group-specific sets of exercises.

Common exercises.
Both groups practiced a tandem stance with eyes open and closed, turning 360 degrees while marching in place, moving from a sitting position on a chair to a standing position (sit-to-stand), and moving from a standing position to a sitting position on a chair (stand-to-sit). These exercises were based on a fall prevention program for older women.³⁰ In addition, participants practiced corrective postural reactions to gentle perturbations backward. Trainers pulled on the participants’ shoulders or hips with enough strength to evoke protective steps backward. A similar technique has been used to improve postural instability and gait in PD.^29,31 The common exercises were performed by both groups once per week for 1 hour each time. Appendix 1 describes the details of the common exercises. In addition, each group received a supplemental set of exercises 2 times per week for 1 hour each time. These activities are listed below.

Group-specific exercises.
Participants in the treatment group received eye movement and visual awareness training as a supplemental activity. To develop this protocol, we gathered parts of protocols from different studies on the rehabilitation of people with similar problems. To improve the visual awareness of our participants, we developed a scanning exercise based on techniques used for visual neglect attributable to stroke.^32,33 The practice consisted of scanning the environment to identify hidden objects. To improve saccadic eye movements, we used computer-assisted saccade exercises, in which participants had to respond with a key press to visual stimuli presented in random locations on the computer screen. For this practice, we used software developed by the Optometric Extension Program Foundation,^* which has been used mainly to improve reading skills in the general population. Another technique that we adopted to improve saccades was auditory feedback, in which participants practiced changing the direction of eye movements to produce different sounds.³⁴ This technique has been proven successful in the rehabilitation of congenital nystagmus.³⁵ Finally, our protocol also involved a stimulus-response compatibility paradigm with the objective of improving attention and enhancing eye-foot coordination. This paradigm was developed and tested in our laboratory¹⁸ with elderly individuals. The supplemental exercises were performed 2 times per week for 1 hour each time. Appendix 2 describes the details of these exercises.

Supplemental activity for the comparison group consisted of additional supervised balance exercises that were also part of a fall prevention program.³⁰ These exercises were performed 2 times per week for 1 hour each time. Appendix 3 describes the details of these exercises. Appendix 4 shows an outline of the protocol.

Outcome Measures

Outcome measures consisted of kinematic gait assessments and clinical tests. The kinematic gait measures were stance time (amount of time that the foot was in contact with the ground, in seconds), swing time (amount of time that the foot was not in contact with the ground, in seconds), and step length (distance from the heel strike of one foot to the heel strike of the opposite foot in the forward direction, in centimeters). The clinical assessments included the 8-ft (2.4-m) walk test,³⁶ a measurement of gait speed, and the Timed "Up & Go" Test (TUG),³⁷ a measurement of general mobility and risk for falling. Excellent reliability has been reported for the 8-ft walk test (intraclass correlation coefficient=.79) in frail elderly people³⁸ and for the TUG in people with PD,³⁷ with Pearson correlations of .79 and .99 in people on and off medications, respectively, and an intraclass correlation coefficient of .99.³⁷ The reported minimal clinically important difference (MCID) for comfortable gait speed in people with PD is about 0.18 m/s.^39,40 The MCID for the TUG in people with PD varies; there have been reports of 2 seconds,³⁹ 5 seconds,⁴¹ and 11 seconds.⁴⁰

Gait analysis.
Tracking of foot motion was done with electromagnetic sensors with 6 degrees of freedom. The sensors were fixed with electrode tape to the dorsum of each foot. Participants wore a headband apparatus that held an infrared oculography system (Series 1000 Binocular Infrared Recording System)^{, 42} and an eye-tracking camera positioned laterally to avoid obstruction of vision. Analysis of eye movements was part of a larger study and is described elsewhere.⁴³ Kinematic data were collected at 100 Hz and exported to Matlab^|| for offline processing. Custom-designed software in the form of Matlab m-files was developed to allow the researchers to view each trial and select relevant parts of the traces corresponding to the kinematic gait measures defined above. Participants were asked to walk at a comfortable speed on a 3-m walkway while guarded by a laboratory assistant to prevent falls. For each participant, 2 trials were analyzed and then averaged for data analysis.

Clinical measures.
During the 8-ft walk test and the TUG, participants were asked to walk at a comfortable speed. Data were averaged from 2 trials.

Data Analysis

Skewness, kurtosis, and omnibus normality were tested with NCSS statistical software.^# All hypotheses were nondirectional (no difference between means), and the critical alpha level was established at .05.

Baseline comparisons.
To examine baseline differences between the treatment and the comparison groups, we used a chi-square test to compare categorical baseline measurements: diagnosis (possible versus probable) and sex (male versus female). A 2-sample t test was used to compare continuous baseline measurements: disease duration, UPDRSm,²⁵ PSP Rating Scale,²⁶ the gait section of the PSP Rating Scale, and MMSE baseline values.²⁴

Between-group comparisons.
Differences between groups were analyzed with a 2-sample t test, in which change scores for each group were compared for each variable (change score = posttest value – pretest value). When data did not conform to a normal distribution, a Mann-Whitney U test for the difference in means was used, and a z score was approximated with correction for continuity.

Within-group comparisons.
To further explore improvements within groups separately, we used a matched-pairs t test to compare pretest and posttest scores within each group. When data did not conform to a normal distribution, a Wilcoxon signed rank test for the difference in medians was used, and a z score was approximated with correction for continuity.

Effect sizes (ES).
To express the clinical meaningfulness of the data, we also calculated ES across groups by using change scores as the unit of measure. The formula used to calculate ES was as follows: (change score for treatment group – change score for comparison group)/SD of change score for comparison group. To interpret ES, we followed the criteria established by Cohen, in which an ES of .2 is considered small, an ES of .5 is considered moderate, and an ES of .8 is considered large.⁴⁴

Role of the Funding Source

This study was funded by grant H133G030159 from the National Institute of Disability and Rehabilitation Research to Dr Di Fabio. The views contained in this publication are those of the grantee and do not necessarily reflect those of the US Department of Education.

	Results

Top Abstract Introduction Method Results Discussion Conclusion Appendix 1. Appendix 2. Appendix 3. Appendix 4. References

 
Baseline Measurements

The baseline characteristics of each group are shown in Table 1. Measurements obtained for disease severity with the UPDRSm²⁵ and the PSP Rating Scale²⁶ indicated moderate stages of the disease. There were no significant differences between the groups for diagnosis (possible versus probable), sex, age, time of symptom onset, disease severity, or PSP Rating Scale scores. A significantly lower MMSE score was observed for the treatment group.

View larger version (24K): [in this window] [in a new window]   Figure. Pretest and posttest values for the treatment and comparison groups for the following variables: stance time (A), swing time (B), step length (C), gait speed measured with the 8-ft (2.4-m) walk test (D), and time to complete the Timed "Up & Go" Test (E). Values are reported as means (SEs). Asterisk indicates significant difference.

	Discussion

Top Abstract Introduction Method Results Discussion Conclusion Appendix 1. Appendix 2. Appendix 3. Appendix 4. References

 
In the present study, we investigated the benefits of balance training complemented with eye movement exercises versus balance training alone for improving gait in participants with PSP. Our within-group comparisons and ES analysis indicated that the subjects receiving balance + eye training showed more improvements than those receiving balance training only. We believe that these preliminary results support the use of balance + eye exercises to improve gait in people who have PSP and are still ambulatory.

Mechanisms Underlying Improvement

At baseline, the MMSE score was lower in the treatment group than in the comparison group (Tab. 1). This difference was not considered important because the score was used as a screening tool to ensure that participants were able to follow instructions, and participants in both groups reached the cutoff score of 23. In addition, because participants in the group with the lower MMSE score showed greater improvements, we do not believe that the MMSE score considerably affected our results.

In previous work, eye movement training was used to improve gait in people with cerebellar ataxia.⁴⁵ The exercises consisted of eye movement rehearsal to fixate objects on the floor (displayed in a random stepping pattern). After eye movement rehearsal, the participants showed improved temporal aspects of gait, such as stance time, double-support time, and swing time variability (reduced). When participants attempted repetitive walking without eye movement training, they did not show any improvement. Our findings agree with those of Crowdy et al⁴⁵ in that visual awareness can help improve temporal aspects of gait. Like cerebellar ataxia, PSP also affects areas of the brain related to the cerebellum, such as the dentate nucleus, cerebellar peduncle, and midbrain tectum.⁴⁶ Both diseases also have common deficits in balance, gait, and ocular movements. Both our findings and those of Crowdy et al show that oculomotor and gait control systems have the potential for rehabilitation even in progressive neurodegenerative disorders.

Although studies on gait in PSP are lacking, the literature supports the rehabilitation of gait in PD.^47,48 It is possible to improve gait cadence and speed with the use of external cues, such as visual stimuli, in PD.⁴⁷ The focus of interventions for PD, however, differs from that for PSP because freezing of gait is not the main problem in PSP. In our group of participants, only 2 of 20 reported freezing episodes. The main gait problem in PSP is instability, with frequent falls. Nevertheless, the concepts behind the effectiveness of eye movement training for PSP and visual cues for PD might be the same: Enhancing a person's attention and visual awareness, thereby enhancing cortical activity, could compensate for defective basal ganglion circuitry.

Blin et al⁴⁹ showed that some aspects of gait, primarily temporal parameters, such as stance time and swing time, are controlled by areas of the brain outside the basal ganglia (BG). In contrast, spatial parameters, such as step length, are probably controlled by dopa-sensitive areas of the brain.⁴⁹ Our results show that balance + eye training had a positive effect on the temporal aspects of gait (Tab. 3 and graphs A and D of the Figure). On the other hand, balance training alone had a positive effect on step length, which is a spatial parameter (Tab. 3 and graph C of the Figure). These findings support the idea that the "eye" exercise portion of the intervention might have had a specific effect on areas of the brain outside the BG, whereas the "balance" portion of the intervention might have elicited activity in the BG. Although there is a generalized neuronal loss in the BG⁴⁹ of people with PSP, in the substantia nigra (pars reticulata and pars compacta), striatum, globus pallidus, and subthalamic nucleus^50–52 there seems to be some potential for rehabilitation.

We speculate that, outside the BG, the brain stem and frontal cortex might be recruited by balance + eye training. Many areas of the brain stem responsible for the control of eye movements are affected in PSP: the rostral interstitial nucleus of the medial longitudinal fasciculus, pontomesencephalic tegmentum, pontomedullary reticular formation, superior colliculus,^50,53 and pedunculopontine nucleus (PPN).⁵⁴ Most of these structures are restricted to the control of eye movements, but the PPN is known to integrate the systems controlling eye movements and locomotion⁵⁵; therefore, it is the key target of balance + eye training. The PPN, located in the rostral portion of the midbrain, projects to the frontal eye field,⁵⁶ which is known to be an area of overlap for the control of eye movements and attention.⁵⁷ It also projects to the spinal cord through BG⁵⁸ and plays a role in the control of posture and gait.⁵⁸ The problems with postural instability and cognitive impairment in PSP have been attributed to neuronal loss involving cholinergic pathways,⁵⁶ including the PPN, which exhibits 60% neuronal loss in the presence of the disease.⁵⁴ Because the PPN has an integrative role and is not completely degenerated in PSP, we speculate that this structure and its neural circuitry remain responsive to balance + eye training.

General Mobility, Gait Speed, Step Length, and Risk for Falling

Our results based on ES analysis showed that the balance + eye intervention had a moderate effect on general mobility, as measured with the TUG (Tab. 3). These results suggest that the eye exercise component of the therapy is the main factor causing the improvement in general mobility. The TUG involves a combination of tasks besides walking (turning, sit-to-stand, and stand-to-sit). It would be interesting to find the specific component of the test that improved with the exercises. It is possible that only the gait component improved and that this improvement alone accounted for the decrease in time. In contrast, it is possible that visual awareness helped improve the other components of the test. We were unable to access that information because no motion analysis was done during the TUG.

The TUG not only is a measure of mobility but also helps evaluate the risk for falling. Scores of higher than 13.5 seconds indicate a higher risk in elderly people.⁵⁹ Participants who received the balance + eye intervention decreased their time by 3.90 seconds (Tab. 2). This change was not statistically significant, nor did it fall below the cutoff point of 13.5 seconds; these results indicate that, despite being faster after intervention, our participants were still at risk for falling. Still, an improvement of 3.90 seconds may have clinical relevance because it is greater than the MCID of 2 seconds reported in the literature.³⁹ Even though other authors have reported higher TUG MCID scores,^40,41 our participants likely were more functionally involved than the individuals with PD and, therefore, lower MCID scores were expected.

Gait speed values increased by 10.85 cm/s in participants receiving balance + eye training (Tab. 2). This improvement reflected a large effect of the intervention (Tab. 3). In addition, the change of 0.10 m/s was very close to the MCID of 0.18 m/s reported in the literature for PD.³⁹ We still consider these results to be clinically relevant given the severity of disease in our participants compared with that in the literature.

Regarding step length, the comparison group showed statistically significant improvements, as indicated by the within-group analysis and a small effect of the intervention (Tab. 3 and graph C of the Figure). The reason why the comparison group showed improved step length whereas the treatment group did not may be a difference in the intervention protocols. Participants receiving balance training alone practiced more standing and stepping activities and, therefore, had more chances to improve stepping than participants receiving balance + eye training, who were seated for most of the "eye training" part of the intervention.

Changes in step length can also be related to a risk for falling. Kerrigan et al⁶⁰ showed that elderly people at a higher risk for falling have reduced hip extension, which is reflected by reduced step length. The authors suggested that falls are likely to occur in situations requiring a larger step to quickly adjust the base of support to maintain balance, such as a change in ground surfaces or obstacle avoidance. Therefore, an increase in step length can be viewed as a positive effect. However, the extent to which it translates into practical situations in which people are required to take larger steps quickly is not known, because we were unable to track episodes of falling in our participants. Participants were constantly monitored by their caretakers, making tracking of falling episodes an unreliable and biased measure.

Limitations

One limitation of the present study was the fact that each group contained a small number of participants, limiting the statistical power to detect changes. However, given that PSP is a rare disease^6,61 and is often misdiagnosed as PD, it is very difficult to recruit large numbers of participants. We consider the number of participants recruited for the present study to be adequate for a preliminary investigation. In addition, given the lack of published rehabilitation studies for PSP, we believe that the present investigation makes an important contribution to the literature in this area.

Statistically, the most appropriate analysis for this kind of study is between-group analysis rather than within-group analysis. Our between-group analysis, however, lacked power to detect the effects of the intervention because of the low prevalence of PSP in the population^6,61 and, hence, a small number of participants in each group. In contrast, ES are not affected by the number of participants. Our descriptive analysis of between-group ES extended the findings of the other tests by illustrating the direction and magnitude of changes among the groups (Tab. 3). Our ES were normalized to the control group standard deviation rather than a polled standard deviation (see Glass et al⁶² for a discussion justifying this technique). Effect sizes calculated in this way highlighted some effects not found with the 2-sample t tests.

Other limitations included the lack of full research masking and the use of a short walkway (3 m) to collect kinematic gait data (usually, gait parameters are measured on longer walkways, but we were limited by physical space in the laboratory).

Future Studies

The present study was a preliminary investigation with a limited number of participants. Additional studies powered at a higher level are needed to confirm these results. Furthermore, the treatment duration of 4 weeks might have been insufficient to promote an optimal response to the intervention in our participants. It remains unknown whether additional benefits can be obtained with a longer treatment period. In addition, we investigated the immediate effects of rehabilitation in PSP. Future studies should be done to investigate possible carryover effects of the therapy. It also would be interesting to learn how therapy involving balance + eye training can help people with other daily activities, such as negotiating obstacles or steps in the walking path. In addition, more research is needed to investigate the effects of balance + eye training on populations with similar problems, such as cerebellar ataxia and corticobasal degeneration.

	Conclusion

Top Abstract Introduction Method Results Discussion Conclusion Appendix 1. Appendix 2. Appendix 3. Appendix 4. References

 
The present study has provided preliminary evidence that balance exercises coupled with eye movement exercises may improve gait in people with PSP. Improvements in spatial gait parameters, gait speed, and TUG scores were observed for participants who received balance + eye training. Future research is needed to confirm these results on a larger scale, to explore the possible retention of improvements, to determine how balance + eye exercises may influence the ability to negotiate obstacles in the walking path, and to test the benefits of this intervention in other populations.

	Appendix 1.

Top Abstract Introduction Method Results Discussion Conclusion Appendix 1. Appendix 2. Appendix 3. Appendix 4. References

 

View larger version (30K): [in this window] [in a new window]   Appendix 1. Common Exercises for Balance Training

	Appendix 2.

Top Abstract Introduction Method Results Discussion Conclusion Appendix 1. Appendix 2. Appendix 3. Appendix 4. References

View larger version (76K): [in this window] [in a new window]   Appendix 2. Specific Exercises for the Treatment Group

	Appendix 3.

Top Abstract Introduction Method Results Discussion Conclusion Appendix 1. Appendix 2. Appendix 3. Appendix 4. References

View larger version (43K): [in this window] [in a new window]   Appendix 3. Specific Exercises for the Comparison Group

	Appendix 4.

Top Abstract Introduction Method Results Discussion Conclusion Appendix 1. Appendix 2. Appendix 3. Appendix 4. References

View larger version (36K): [in this window] [in a new window]   Appendix 4. Protocols for the Treatment and Comparison Groups

	Footnotes

 
Both authors provided concept/idea/research design, writing, data collection and analysis, project management, and consultation (including review of manuscript before submission). Dr Di Fabio provided fund procurement, facilities/equipment, and institutional liaisons.

The protocol used in this study was approved by the University of Minnesota Human Subjects Research Committee.

This study was supported by grant H133G030159 from the National Institute of Disability and Rehabilitation Research to Dr Di Fabio. The opinions contained in this publication are those of the grantee and do not necessarily reflect those of the US Department of Education.

^* Vision Builder Software, Helga Blystadsvei 8, 2316 Hamar, Norway.

Innovative Sports Training Inc, 3711 N Ravenswood, Suite 150, Chicago, IL 60613.

MicroGuide Inc, 1635 Plum Ct, Downers Grove, IL 60515.

Arrington Research Inc, 27237 N 71st Pl, Scottsdale, AZ 85266.

^|| The Mathworks Inc, 3 Apple Hill Dr, Natick, MA 01760-2098.

^# NCSS Software, 329 North 1000 East, Kaysville, UT 84037.

	References

Top Abstract Introduction Method Results Discussion Conclusion Appendix 1. Appendix 2. Appendix 3. Appendix 4. References

 

1. Nath U, Ben-Shlomo Y, Tomson RG, et al. Clinical features and natural history of progressive supranuclear palsy: a clinical cohort study. Neurology. 2003;60:910–916.[Abstract/Free Full Text]
2. Birdi S, Rajput AH, Fenton M, et al. Progressive supranuclear palsy diagnosis and confounding features: report on 16 autopsied cases. Mov Disord. 2002;17:1255–1264.[CrossRef][Web of Science][Medline]
3. Litvan I. Diagnosis and management of progressive supranuclear palsy. Semin Neurol. 2001;21:41–48.[CrossRef][Web of Science][Medline]
4. Goetz CG, Leurgans S, Lang AE, Litvan I. Progression of gait, speech and swallowing deficits in progressive supranuclear palsy. Neurology. 2003;60:917–922.[Abstract/Free Full Text]
5. Duvoisin RC, Golbe LI, Lepore FE. Progressive supranuclear palsy. Can J Neurol Sci. 1987;14:547–554.[Medline]
6. Golbe GI, Davis PH, Shoenberg BS, Duvoisin RC. Prevalence and natural history of progressive supranuclear palsy. Neurology. 1988;38:1031–1034.[Abstract/Free Full Text]
7. Di Fabio RP, Zampieri C, Tuite P. Gaze-shift strategies during functional activity in progressive supranuclear palsy. Exp Brain Res. 2006;178:351–362.
8. Di Fabio RP, Zampieri C, Tuite P, Konczak J. Independent gaze theory supported by progressive supranuclear palsy. In: 34th Annual Meeting of the Society for Neuroscience. San Diego, CA: Society for Neuroscience; 2004.
9. Di Fabio RP, Zampieri C, Tuite P, Konczak J. Association between vestibuloocular reflex suppression during smooth movements of the head and attention deficit in progressive supranuclear palsy. Mov Disord. 2006;21:910–915.[CrossRef][Web of Science][Medline]
10. Muller J, Seppi K, Stefanova N, et al. Freezing of gait in postmortem-confirmed atypical parkinsonism. Mov Disord. 2002;17:1041–1045.[CrossRef][Web of Science][Medline]
11. Burn DJ, Lees AJ. Progressive supranuclear palsy: where are we now? Lancet. 2002;1:359–369.
12. Izzo KL, DiLorenzo P, Roth A. Rehabilitation in progressive supranuclear palsy: case report. Arch Phys Med Rehabil. 1996;67:473–476.
13. Sosner J, Wall GC, Sznajder J. Progressive supranuclear palsy: clinical presentation and rehabilitation of two patients. Arch Phys Med Rehabil. 1993;74:537–539.[CrossRef][Web of Science][Medline]
14. Steffen TM, Bradley FB, Mollinger-Riemann LA, Petersen CM. Long-term locomotor training for gait and balance in a patient with mixed progressive supranuclear palsy and corticobasal degeneration. J Neurol Phys Ther. 2007;31:1078–1087.
15. Suteerawattananon MB, Neil BM, Elizabeth P. Supported treadmill training for gait balance in a patient with progressive supranuclear palsy. Phys Ther. 2002;82:485–495.[Abstract/Free Full Text]
16. Patla AE, Vickers JN. Where and when do we look as we approach and step over an obstacle in the travel path? Neuroreport. 1997;8:3661–3665.[Web of Science][Medline]
17. Hollands MA, Patla AE, Vickers JN. "Look where you’re going!" Gaze behaviour associated with maintaining and changing the direction of locomotion. Exp Brain Res. 2002;143:221–230.[CrossRef][Web of Science][Medline]
18. Di Fabio RP, Greany J, Zampieri C. Saccade-stepping interactions revise the motor plan for obstacle avoidance. J Mot Behav. 2003;35:383–397.[Web of Science][Medline]
19. Di Fabio R, Zampieri C, Henke J, et al. Influence of elderly executive cognitive function on visual attention in the lower visual field. Gerontology. 2005;51:94–107.[CrossRef][Web of Science][Medline]
20. Di Fabio R, Zampieri C, Tuite P. Gaze control and foot kinematics during stair climbing: characteristics leading to fall risk in progressive supranuclear palsy. Phys Ther. 2008;88:240–250.[Abstract/Free Full Text]
21. Rubenstein LZ. Falls in older people: epidemiology, risk factors, and strategies for prevention. Age Ageing. 2006;35(suppl 2):ii37–ii41.
22. Sheridan P, Hausdorff J. The role of higher-level cognitive function in gait: executive dysfunction contributes to fall risk in Alzheimer's disease. Dement Geriatr Cogn Disord. 2007;24:125–137.[CrossRef][Web of Science][Medline]
23. Hausdorff J, Doniger G, Springer S, et al. A common cognitive profile in elderly fallers and in patients with Parkinson's disease: the prominence of impaired executive function and attention. Exp Aging Res. 2006;32:411–429.[CrossRef][Web of Science][Medline]
24. Folstein MF, Folstein SE, McHugh PR. "Mini-mental state": a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12:189–198.[CrossRef][Web of Science][Medline]
25. Cubo E, Stebbins GT, Golbe LI, et al. Application of the Unified Parkinson's Disease Rating Scale in progressive supranuclear palsy: factor analysis of the motor scale. Mov Disord. 2000;15:276–279.[CrossRef][Web of Science][Medline]
26. Golbe LI. A clinical rating scale for progressive supranuclear palsy. Brain. 2007;130:1552–1565.[Abstract/Free Full Text]
27. Litvan I, Bhatia KP, Burn DJ, et al. SIC task force appraisal of clinical diagnostic criteria for parkinsonian disorders. Mov Disord. 2003;18:467–486.[CrossRef][Web of Science][Medline]
28. Comella C, Stebbins G, Brown-Toms N, Goetz C. Physical therapy and Parkinson's disease: a controlled clinical trial. Neurology. 1994;44:376–378.[Abstract/Free Full Text]
29. Protas EJ, Mitchell K, Williams A, et al. Gait and step training to reduce falls in Parkinson's disease. NeuroRehabilitation. 2005;3:183–190.
30. Findorff M, Stock HH, Gross C, Wyman J. Does the transtheoretical model (TTM) explain exercise behavior in a community-based sample of older women? J Aging Health. 2007;19:985–1003.[Abstract/Free Full Text]
31. Jöbges M, Heuschkel G, Pretzel C, et al. Repetitive training of compensatory steps: a therapeutic approach for postural instability in Parkinson's disease. J Neurol Neurosurg Psychiatry. 2004;75:1682–1687.[Abstract/Free Full Text]
32. Bailey M, Riddoch M, Crome P. Treatment of visual neglect in elderly patients with stroke: a single-subject series using either a scanning and cueing strategy or a left-limb activation strategy. Phys Ther. 2002;82:782–797.[Abstract/Free Full Text]
33. Luauté J, Halligane P, Rodea G, et al. Visuo-spatial neglect: a systematic review of current interventions and their effectiveness. Neurosci Biobehav Rev. 2006;30:961–982.[CrossRef][Web of Science][Medline]
34. Di Fabio RP, Zampieri C, Tuite P, Konczak J. Vertical gaze enhanced with biofeedback for patients with progressive supranuclear palsy: evidence for movement related plasticity in a chronic progressive neurological disorder [abstract]. Mov Disord. 2004;19:1124.
35. Sharma P, Tandon R, Kumar S, Anand S. Reduction of congenital nystagmus amplitude with auditory biofeedback. J AAPOS. 2000;4:287–290.[Medline]
36. Guralnik JM, Simonsick EM, Ferrucci L, et al. A short physical performance battery assessing lower extremity function: association with self-reported disability and prediction of mortality and nursing home admission.J Gerontol. 1994;49:M85–M94.[Abstract]
37. Morris S, Morris ME, Iansek R. Reliability of measurements obtained with the Timed "Up & Go" Test in people with Parkinson disease. Phys Ther. 2001;81:810–818.[Abstract/Free Full Text]
38. Jette AM, Jette DU, Ng J, et al. Are performance-based measures sufficiently reliable for use in multicenter trials? Musculoskeletal Impairment (MSI) Study Group. J Gerontol A Biol Sci Med Sci. 1999;54:M3–M6.[Abstract]
39. Lim LI, van Wegen EE, de Goede CJ, et al. Measuring gait and gait-related activities in Parkinson's patients own home environment: a reliability, responsiveness and feasibility study. Parkinsonism Relat Disord. 2005;11:19–24.[CrossRef][Web of Science][Medline]
40. Steffen TM, Seney M. Test-retest reliability and minimal detectable change on balance and ambulation tests, the 36-Item Short-Form Health Survey, and the Unified Parkinson Disease Rating Scale in people with parkinsonism. Phys Ther. 2008;88:733–746.[Abstract/Free Full Text]
41. Campbell CM, Rowse JL, Ciol MA, Shumway-Cook A. The effect of cognitive demand on Timed Up and Go performance in older adults with and without Parkinson disease. Neurol Rep. 2003;27:2–7.
42. Kumar A, Krol G. Binocular infrared oculography. Laryngoscope. 1992;102:367–378.[CrossRef][Web of Science][Medline]
43. Zampieri C, Di Fabio RP. Improvement of gaze control following balance and eye movement training in patients with progressive supranuclear palsy: a quasi-randomized controlled trial. Arch Phys Med Rehabil. In press.
44. Cohen J. Statistical Power Analysis for the Behavioral Sciences. New York, NY: Academic Press; 1969.
45. Crowdy KA, Kaur-Mann D, Cooper HL, et al. Rehearsal by eye movement improves visuomotor performance in cerebellar patients. Exp Brain Res. 2002;146:244–247.[CrossRef][Web of Science][Medline]
46. Dickson D, Rademakers R, Hutton M. Progressive supranuclear palsy: pathology and genetics. Brain Pathol. 2007;17:74–82.[CrossRef][Web of Science][Medline]
47. Rubinstein TC, Giladi N, Hausdorff JM. The power of cueing to circumvent dopamine deficits: a review of physical therapy treatment of gait disturbances in Parkinson's disease. Mov Disord. 2003;17:1148–1160.
48. Trend P, Kaye J, Gage H, et al. Short-term effectiveness of intensive multidisciplinary rehabilitation for people with Parkinson's disease and their carers. Clin Rehabil. 2002;16:717–725.[Abstract/Free Full Text]
49. Blin O, Ferrandes A, Pailhous J, Serratrice G. Dopa-sensitive and dopa-resistant gait parameters in Parkinson's disease. J Neurol Sci. 1991;103:51–54.[CrossRef][Web of Science][Medline]
50. Collins S, Ahlskog J, Parisi J, Maraganore D. Progressive supranuclear palsy: neuropathologically based diagnostic clinical criteria. J Neurol Neurosurg Psychiatry. 1995;58:167–173.[Abstract/Free Full Text]
51. Hauw J, Daniel S, Dickson D. Preliminary NINDS neuropathologic criteria for Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy). Neurology. 1994;44:2015–2019.[Abstract/Free Full Text]
52. Yamada T, Calne DB, Akiyama H, et al. Further observations on Tau-positive glia in the brains with progressive supranuclear palsy. Acta Neuropathol. 1993;85:308–315.[Medline]
53. Juncos J, Hirsch E, Malessa S, et al. Mesencephalic cholinergic nuclei in progressive supranuclear palsy. Neurology. 1991;41:25–30.[Abstract/Free Full Text]
54. Jellinger K. The pedunculopontine nucleus in Parkinson's disease, progressive supranuclear palsy and Alzheimer's disease. J Neurol Neurosurg Psychiatry. 1988;51:540–543.[Abstract/Free Full Text]
55. Mena-Segovia J, Bolam JP, Magill PJ. Pedunculopontine nucleus and basal ganglia: distant relatives of part of the same family? Trends Neurosci. 2004;27:585–588.[CrossRef][Web of Science][Medline]
56. Warren NM, Piggott MA, Perry EK, Burn DJ.Cholinergic systems in progressive supranuclear palsy. Brain. 2005;128:239–249.[Abstract/Free Full Text]
57. Miler NR, Newman NJ. The ocular motor system. In: Miller NR, Newman NJ, eds. Walsh and Hoyt's Clinical Neuro-Ophthalmology. Vol 1. Baltimore, MD: Williams & Wilkins; 1998:1043–1505.
58. Pahaphill PA, Lozano AM. The pedunculopontine nucleus and Parkinson's disease. Brain. 2000;123:1767–1783.[Abstract/Free Full Text]
59. Shumway-Cook A, Brauer S, Woollacott M. Predicting the probability for falls in community-dwelling older adults using the Timed Up & Go Test. Phys Ther. 2000;80:896–903.[Abstract/Free Full Text]
60. Kerrigan DC, Lee LW, Collins JJ, et al. Reduced hip extension during walking: healthy elderly and fallers versus young adults. Arch Phys Med Rehabil. 2001;82:26–30.[CrossRef][Web of Science][Medline]
61. Bower JH, Marangone DM, McDonnell SK, Rocca WA. Incidence of progressive supranuclear palsy and multiple system atrophy in Olmsted County, Minnesota, 1976 to 1990. Neurology. 1997;49:1284–1288.[Abstract/Free Full Text]
62. Glass G, McGaw B, Smith M. Meta-Analysis in Social Research. London, United Kingdom: Sage Publications; 1981.

CiteULike

Complore

Connotea

Del.icio.us

Digg

Reddit

Technorati

This Article Abstract Full Text (PDF) All Versions of this Article: ptj.20070302v1 88/12/1460    most recent Submit a response Alert me when this article is cited Alert me when Rapid Responses are posted Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Zampieri, C. Articles by Di Fabio, R. P Search for Related Content PubMed PubMed Citation Articles by Zampieri, C. Articles by Di Fabio, R. P Related Collections Balance Training Gait and Locomotion Training Balance Parkinson Disease and Parkinsonian Disorders Social Bookmarking                      What's this?