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Biofeedback-based Motor Learning to Ameliorate Freezing of Gait

Our objective is to demonstrate that an intervention program based on motor learning principles can be applied to train subjects with Parkinson's disease (PD) who suffer from freezing to walk in a way that minimizes the occurrence of freezing.  Since sufficient motor learning capabilities are preserved in PD, we hypothesize that an intervention program that targets the time periods just prior to an approaching freezing episode can modify the walking strategies so that the episode will now be averted. 

Project Description
The freezing burden will be quantified in subjects with PD before and after 6 weeks of training.  Two types of interventions (20 subjects in each group) will be tested: 1) Open-loop group (OLG); 2) Closed-loop group (CLG).  Each session of the OLG training includes walking courses aimed at provoking freezing episodes. The experimenter will trigger an auditory rhythmic stimulation (RAS) in walking conditions likely to invoke freezing (e.g., turning) and the subject will learn to synchronize his/her gait with the auditory cues, i.e., to keep the walking pace and coordination and, as a result, to avoid freezing.  Similar principles will apply for the CLG training; however, the RAS will be elicited automatically by a device that recognizes an approaching freezing episode.

Relevance to Diagnosis/Treatment of Parkinson’s Disease:  
If even partially successful, we will show, for the first time that freezing of gait is amenable to motor learning and that appropriate training with external cueing can alleviate these motor blockades.  While future studies will be needed to further assess long-term efficacy and other important questions about clinical efficacy and the mechanisms involved, this study should go a long way towards improving our understanding of freezing of gait and its amenability to appropriate therapy.   

Anticipated Outcome
We anticipate that after intensive training, the central nervous system (CNS) of subjects with PD will be able to anticipate impending freezing episodes based on awareness of the environmental conditions (e.g., an approaching turn) and/or based on sub-conscious response to a deteriorating gait pattern. As a result, an automated motor response that paces and coordinates gait will be internally triggered by the CNS and the approaching freezing episode will be averted.  The overall freezing burden will therefore decrease in trained subjects. 

Final Outcome

With MJFF support, we were able to develop two novel, auditory bio-feedback-based interventions that are designed to ameliorate the freezing of gait symptom in Parkinson's disease. The results to date clearly support the feasibility of both interventions. Our findings also support the potential clinical efficacy of "intervention-1". Patients who suffer from the freezing symptom (n=15) were trained extensively (3 sessions per week for 6 weeks) in laboratory and hospital settings, in basic daily walking (e.g., turning, chair circumventing, wondering within a retailer store). Whenever the gait situation involved a high chance for freezing, a metronome was sounded and the patients were instructed to pace, coordination and scale their steps with the rhythmic sound. The intention was to 'teach' the motor system to react so in high risk freezing situation. Comparison between pre- and post-.intervention testing in laboratory settings points to significant improvements. For example, the freezing occurrence rate decreased by ~ 80%, and the duration of freezing by ~70%. Intervention in which feedback is given to subjects wearing a portable device prior to the initiation of a freezing event has also begun. Ongoing studies demonstrate the ability to conduct training with such device.

Presentations & Publications
This work were presented in the Tel Aviv Sourasky Medical Center Research and Development Seminar Series (November 2nd, 2011) and in the Israeli Physiotherapist Association's Workshop on Parkinson's Disease (November 10th, 2011). An abstract (see below) has been accepted for oral presentation in the upcoming 62nd annual meeting of the Israeli Rehabilitation Medicine Society, Tel Aviv Israel, December 13-14th.

Can freezing of gait in patients with Parkinson's disease be alleviated using a motor learning based physiotherapy intervention?

Moran Dorfman, Marina Brozgol, Alexey Nesterov, Tanya Gurevitch, Nir Giladi, Jeffrey M. Hausdorff, Meir Plotnik
Laboratory for Gait and Neurodynamics, Movement Disorders Unit, Department of Neurology.

Key words: Parkinson's disease, Freezing of gait, Motor learning, Rhythmic auditory stimulation.
Background: Freezing of gait (FOG) is a paroxysmal gait disturbance commonly seen among patients with advanced Parkinson's disease (PD). FOG episodically disables the subjects from producing effective gait. To date, treatment efficacy, e.g., dopaminergic facilitation, exercise and external cueing, is limited. Aim: To test the hypothesis that an intervention that utilizes motor learning provided through intensive exercise can alleviate the symptom. Methods: 9 subjects with PD suffering from FOG (age: 70±2.3 [SE]; Hoehn&Yahr scale: 3.2±0.3); participated in a 6 weeks progressive gait exercise program (3 training sessions per week – open trial). A training session included FOG provoking situations (e.g., tight turns). Prior to each presumed FOG provocation (e.g., just before a turn), rhythmic auditory stimulation (RAS) was elicited by the experimenter (or in the case a FOG episode). The subject was trained to pace and coordinate left-right stepping and to scale up step size, utilizing the RAS cueing. In each time, the RAS lasted for 5 s or after the FOG or FOG provocation ended, whichever came later. To achieve progressiveness, net training duration increased from week to week and secondary cognitive tasks while walking were added (to increase FOG propensity). Pre- and post- intervention a battery of evaluations was used to assess changes in the FOG symptom burden. Testing included the number and duration of FOG episodes in a given trajectory (corridor walking and curved trajectories) and the scores on subjective questionnaires (e.g., FOG- questionnaire) and the motor part of the unified Parkinson's disease rating scale (UPDRS). Results: Table 1 summarizes the effects of the intervention on FOG symptoms as measured 3 days before ('pre') and 3 days after ('post') the completion of the training program. Number of FOG episodes in corridor walking decreased from 5.6 ± 1.9 to 1.8 ± 1.3 per trial (p=0.018) when comparing pre and post testing, respectively, and the mean duration of the episodes decreased from 4.8 ± 1.8 s to 1.4 ± 0.7 s, correspondently. The corresponding reductions in curved trajectories when comparing pre to post testing were from 4.5 ± 1.9 to 2.8 ± 2.1 episodes per lap (p=0.168) and from to 4.5± 3.6 s to 1.8 ± 1.2 s (p=0.051). FOG-Q and PDQ scores did not change significantly, and marginally significantly change was seen in the UPDRS motor score (from 42.0 ± 3.5 to 34.8 ± 4.5, p=0.08). Conclusion: These preliminary results suggest that the physiotherapy based on conditional motor learning principals effectively reduces the freezing burden during typical walking conditions (corridor and curved trajectories). While subjective improvement was not reported by the subjects, objective clinical evaluation points to significant improvements.

Parameter Pre- intervention Post- intervention P value*
Number of FOG episodes - corridor† 5.6 ± 1.9 1.8 ± 1.3 0.018
Duration of FOG episodes- corridor (s) 4.8 ± 1.8 1.4 ± 0.7 0.028
Number of FOG episodes - curves 4.5 ± 1.9 2.8 ± 2.1 0.168
Duration of FOG episodes- curves (s) 4.5± 3.6 1.8 ± 1.2 0.051
FOG-Q score 25.1 ± 1.8 21.8 ± 3.2 0.270
PDQ-score 49.1 ± 8.9 48.9 ± 7.10 0.766
UPDRS motor 42.0 ± 3.5 34.8 ± 4.5 0.08
Entries are means ± SE calculated across all subjects. FOG-Q- Fog questionnaire; PDQ- Parkinson's disease quality of life questionnaire; *Non-parametric statistics. † Gait data from one subject who used a different walking aid in the pre and post- evaluations was excluded.

Acknowledgement: This project is funded in part by The Michael J Fox Foundation for Parkinson's research RRIA 2010, and by funds from the Tel Aviv Sourasky Medical Center Grant of Excellence.



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