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Table of Contents
ORIGINAL ARTICLE
Year : 2019  |  Volume : 2  |  Issue : 1  |  Page : 15-20

Clinical outcomes of step-synchronized vibration training in patients of Parkinson’s disease with freezing of gait


1 Department of Neurology, All India Institute of Medical Sciences, New Delhi, India
2 Biomechanics and Movement Science Program, University of Delaware, Newark, Delaware, United States, Present addresses: School of Nursing, Virginia, Commonwealth University, Richmond, Virginia
3 Biomechanics and Movement Science Program, University of Delaware, Newark, Delaware, United States, School of Informatics, Computing, and Cyber Systems, Northern, Arizona University, Flagstaff, Arizona
4 Biomechanics and Movement Science Program, University of Delaware, Newark, Delaware, United States, Department of Mechanical Engineering and Rehabilitation/Regenerative Medicine, Columbia University, New York, United States
5 Department of Neurology, All India Institute of Medical Sciences, New Delhi, India, Department of Neurology, Fortis Flt. Lt. Rajan Dhall Hospital, New Delhi, India

Date of Web Publication17-Apr-2019

Correspondence Address:
Madhuri Behari
Department of Neurology, Fortis Flt. Lt. Rajan Dhall Hospital, Vasant Kunj, New Delhi, India.
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/AOMD.AOMD_18_18

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  Abstract 

OBJECTIVE: To elucidate the effect of step-synchronized vibration training using PDShoe on balance, gait, and quality of life in patients of Parkinson’s disease (PD) with freezing of gait (FOG).MATERIALS AND METHODS: In a pilot study, 17 patients of PD with FOG were recruited for step-synchronized vibration training. The training involved 10 sessions of gait training over 2 weeks. Each session included three 6-min bouts of walking with step-synchronized vibration applied to the second metatarsal head and medial surface of calcaneus. Participants were assessed with the Unified Parkinson’s Disease Rating Scale-III (UPDRS III), Timed Up and Go (TUG) test, Berg Balance Scale (BBS), Timed 10-Meter Walk Test, Freezing of Gait Questionnaire (FOG-Q), Falls Efficacy Scale-International (FES-I), and Parkinson’s Disease Questionnaire-39 (PDQ-39). Measurements were collected pre-intervention, post-intervention, and at a 2-week follow-up. Friedman test followed by Wilcoxon signed-rank test were used for statistical analysis.RESULTS: All participants completed the intervention without any adverse effects. Fifteen participants reported for a follow-up evaluation 2 weeks after intervention. There was statistically significant improvement in UPDRS III (P = 0.044) and significant improvement in TUG test (P = 0.005), BBS (P = 0.026), FES-I (P = 0.041), and PDQ-39 (P = 0.021) scores between pre and follow-up evaluations. No significant changes were seen in FOG-Q and Timed 10-Meter Walk Test.CONCLUSION: Step-synchronized vibration is a novel intervention to improve balance, gait, motor features, and quality of life in patients of PD with FOG. Further research is warranted to confirm the results found in this pilot study.

Keywords: Freezing of gait, gait training, Parkinson’s disease, vibration therapy


How to cite this article:
Aggarwal R, Pretzer-Aboff I, Winfree KN, Agrawal SK, Behari M. Clinical outcomes of step-synchronized vibration training in patients of Parkinson’s disease with freezing of gait. Ann Mov Disord 2019;2:15-20

How to cite this URL:
Aggarwal R, Pretzer-Aboff I, Winfree KN, Agrawal SK, Behari M. Clinical outcomes of step-synchronized vibration training in patients of Parkinson’s disease with freezing of gait. Ann Mov Disord [serial online] 2019 [cited 2019 Jul 22];2:15-20. Available from: http://www.aomd.in/text.asp?2019/2/1/15/256493




  Background Top


Patients with Parkinson’s disease (PD) often have gait and balance disorders. The most disabling gait disturbance is freezing of gait (FOG), which is described by patients with PD as the feeling of their feet being glued to the ground.[1] Over 50% of them experience FOG.[2]

FOG is more commonly seen in atypical  Parkinsonism More Details, usually nonresponsive to levodopa, and is often an early sign. It can manifest as hesitation on gait initiation, freezing while walking in an open space or through a narrow passage or during turning or while approaching destination.[2],[3] FOG negatively affects quality of life, balance, and is often a contributing factor leading to falls.[4] Mitigation of FOG is elusive. Medical treatment using levodopa has been shown to increase the stride length in patients with PD. However, it is less effective on the temporal parameters of gait, such as cadence, swing duration, and double support time, which is altered due to the FOG. Deep brain stimulation (DBS) targeting the subthalamic nuclei (STN) can improve levodopa-responsive symptoms although freezing is resistant.[5] Neither medical nor surgical modes of treatment have shown to be successful in alleviating the symptoms of FOG. Sensory cuing and attention-focusing interventions have been used with some success, but more work developing and testing such therapies is warranted.[6]

There is a growing interest in the effect of vibration on parkinsonian motor symptoms. Previously, researchers have studied the impact of whole body vibration in patients with PD and reported improvements in tremor, muscle rigidity, postural stability, and gait when assessed with the Unified Parkinson’s Disease Rating Scale-III (UPDRS III).[7],[8] Moreover, improvement in standing sway was reported by Han et al.[9] in which vibration stimuli were delivered to specific muscle groups in the lower extremities. De Nunzio et al.[10] showed improved stride length, cadence, and gait velocity with vibration delivered in an alternate and rhythmic manner to the trunk of patients with PD during walking. Novak’s team applied step-synchronized vibration to the soles of the patients with PD feet and showed improved stride duration, length, and cadence; however, they excluded patients with PD who experienced FOG.[11] Application of step-synchronized vibration to the medial malleolus and metatarsal bones by PDShoe has showed a decreased variability of gait and decreased stride duration in the participants who experienced FOG.[12] Overall, FOG is seen to be a major concern by the PD population, and therefore requires serious attention. This pilot study focused to evaluate the effect of a step-synchronized vibration training using the PDShoe on patients of PD with FOG.


  Materials and Methods Top


This study was carried out at a tertiary care teaching hospital after approval by the institutional ethics committee. Seventeen non-demented (Mini-Mental State Examination >24) ambulatory persons with idiopathic PD who experienced FOG episodes in the previous month were recruited from the movement disorder clinic of the hospital. All participants signed an informed consent before participation in the study. Diagnosis of PD was confirmed by a neurologist on the basis of the Queen’s Square Parkinson’s Disease Brain Bank Diagnostic Criteria.[13] Travel to the study site for all participants and lodging for out-of-town participants were provided to facilitate participants’ availability for the study.

Participants were assessed at baseline for disease severity using modified Hoehn and Yahr scale,[14] UDPRS III,[15] and Schwab and England Activities of Daily Living Scale.[16] Levodopa equivalent daily dosage was calculated using a standard formula,[17] and hemodynamic stability was determined by measuring blood pressure in sitting and standing positions. Balance and mobility were assessed using the Berg Balance Scale (BBS),[18] Timed Up and Go (TUG) test,[19] and Timed 10-Meter Walk Test (10MWT).[20] Self-reported measures included Freezing of Gait Questionnaire (FOG-Q),[21] Falls Efficacy Score-International (FES-I),[22] and quality of life using the 39-item Parkinson’s Disease Questionnaire (PDQ-39). Two Global Perceived Effect (GPE)[23] questions were used to determine participant’s perception of gait and balance directly after the intervention and at follow-up.

The TUG and 10MWT were each performed three times and the average of these scores was recorded. All tests were performed in the “ON” state determined by subject’s confirmation that their medications were working before each test. The order of assessments was in random manner to avoid fatigue or habituation effects. Subjects selected the size of PDShoe that fit them most comfortably. Sizes were available in American whole size increments from men’s 6 to 13. After the comfortable fitting of the PDShoe, each insole was tested for transmission of pressure signals to the computer and actuation of each vibrator. The participant verified sensation of vibration before starting each session.

The PDShoe is an untethered vibratory system with pressure sensors embedded in the insole (heel, balls of metatarsals, and toes) to sense real-time pressure changes during standing and walking. It has two vibrators, one placed on the dorsum of the foot and the other on the medial aspect of the heel. The shoe delivered vibrations in a step-synchronized manner. The vibrator on the dorsum of the foot was activated when the toes were in contact with the ground and stopped vibrating once the toes were off the ground. Similarly, the heel vibrator activated once the heel was in contact with the ground and stopped when the pressure sensor sensed it was off the ground.

All participants underwent a training program of 10 sessions in 2 weeks (5 days per week). During the training session, the participants were asked to walk back and forth on a 25-m straight path while wearing the PDShoes. Each session included a 2-min walking bout (vibration off) followed by three 6-min walking bouts (vibration on) and ending with a 2-min walking bout (vibration off). The first and second walking bouts without vibration were used to collect data. Participants rested for at least 2min between each bout. After completing 10 training sessions, participants were reassessed using the same test battery as used at the baseline with the addition of the GPE questions. Participants returned after 2 weeks for a follow-up assessment to evaluate any carryover effect. Medication regime was kept constant for all participants throughout the study period.

The Freidman’s test was used to identify the changes in repeated measurements of clinical outcome measures. Significance level was set at α <0.05. A post hoc analysis with Wilcoxon signed-rank tests was conducted. The Statistical Package for the Social Sciences (SPSS) software, version 16.0 (SPSS Inc. 233 South Wacker Drive, 11th Floor Chicago, IL 60606-6412 USA) was used for all statistical analyses.


  Results Top


Seventeen patients with idiopathic PD with mean age of 55 years (standard deviation [SD] = 10.1 years), male/female ratio = 13:4, and mean onset of symptoms at age 46 years (SD = 9.8 years) participated in the study. Demographic summary of the participants is shown in [Table 1]. Median score for Schwab and England Activities of Daily Living Scale was 70 (range, 40–90). None of the participants had orthostatic hypotension. Of the 17 patients with PD, two had undergone subthalamic nucleus DBS surgery (mean duration, 7 years), five had at least one fall in the last 6 months, and all experienced FOG. All participants completed the study with 10 training sessions. Shoes were reported to be comfortable, and no complications wearing the PDShoes were identified. Twice the battery dislodged from the PDShoe during a training session but was immediately fixed and did not disturb the working of the PDShoe. Fifteen participants (88.2%) reported for the 2-week follow-up data collection. Of the two unavailable for follow-up, one with STN DBS was out for vacations, whereas the other could not come due to work schedules.
Table 1: Participants characteristics (n = 17)

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[Table 2] shows the clinical outcome measurements of participants at three points of times (baseline, after training, and follow-up of 2 weeks). An overall statistically significant improvement was observed in the UPDRS III score (χ2 (2) = 6.13, P = 0.047), TUG (χ2 (2) = 14.5, P = 0.001), BBS (χ2 (2) = 8.48, P = 0.014), PDQ-39 (χ2 (2) = 11.22, P = 0.004), and FES-I (χ2 (2) = 6.96, P = 0.03). No statistically significant difference was observed in the number of steps (χ2 (2) = 1.00, P = 0.61) and time (χ2 (2) = 4.13, P = 0.13) taken to complete 10MWT and FOG-Q (χ2 (2) = 3.43, P = 0.18). None of the participants including two participants with STN DBS reported any adverse effects after 2 weeks of training.
Table 2: Clinical outcome measurements of participants

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On post hoc analysis using the Wilcoxon signed-rank tests, a statistically significant improvement was observed between baseline and post-training measurements of TUG test (median difference = –2.5s, P = 0.006), BBS (median difference = 3, P = 0.009), PDQ-39 (median difference = –16, P = 0.001), UPDRS III (median difference = 0, P = 0.048), and FES-I (median difference = –2, P = 0.04). This improvement was sustained at the 2-week follow-up assessment. No statistically significant change was observed between post-intervention and 2-week follow-up measurements in any scale except UPDRS III (P = 0.016). After training, the subjective evaluation by participants on GPE for gait improvement was reported as much improvement (n = 3), slight improvement (n = 9), and no improvement (n = 5). On GPE, for the question about if the participants noted any improvement in their balance, the answers were much improvement (n = 1), slight improvement (n = 6), and no improvement (n = 10). No participant reported any worsening in gait or balance after training. At 2-week follow-up after training, GPE for gait was reported as much improvement (n = 1), slight improvement (n = 5), no improvement (n = 8), and slight worse (n = 1), whereas GPE for balance was reported as slight improvement (n = 5), no improvement (n = 8), and slight worse (n = 2).


  Discussion Top


We examined the effect of gait training using PDShoe in patients with idiopathic PD. Patients with atypical parkinsonian with FOG were not included in the study because of wide spectrum of their pathophysiology and multiple systemic involvements making it a heterogeneous group of patients. At our center, we usually call patients with PD at 3-month interval for follow-up. Our study required their participation on daily basis for 2 weeks, so we provided travel to the study site for all participants and lodging for out-of-town participants. Recruitment of participants in the study was based on willingness and informed consent. There was no monetary incentive for their participation.

The results of this study revealed four main findings: (1) the vibration intervention improved functional mobility on TUG test that was sustained for 2 weeks after the intervention at follow-up data collection, (2) the intervention improved balance based on the BBS and the effect persisted for at least 2 weeks, (3) the intervention reduced fear of falling as tested by FES-I with the effect persisting for 2 weeks after training, and (4) the intervention improved health-related quality of life as reported on the PDQ-39.

The PDShoe is a novel system that has the ability to provide vibratory stimuli synchronized with gait activity.[12] Gait is controlled by a constant feedback between proprioceptive inputs and central pattern generator. The defective automatic control of gait pattern in PD can be supplemented by proprioceptive stimuli to stimulate supraspinal areas to regulate the central pattern generator.[24] It is possible that synchronized vibrations with steps provide an augmented sensory feedback to regulate the gait pattern. However, it is not clear how these cues improve movement. Perhaps, they provide an external rhythm that compensates for the improperly supplied internal rhythm of the basal ganglia, which corrects for the motor set deficiency. The scientific explanation of these outcomes is ingrained within the phenomenon of kinesthetic illusion.[25] The PDShoe was developed to reduce FOG episodes and thereby improve walking and balance. Freezing is a manifestation of proprioceptive and central gait pattern originator dysfunction.[24] Vibrations act as proprioceptive cues and stimulate dorsolateral premotor control system and bypass supplementary motor area, thereby helping in maintaining continuity of gait. In literature, we found only a single study by Novak and Novak[11] who used step-synchronized vibration stimulation to plantar surface of foot for gait training in patients with PD. Studies on vibration therapy are mainly focused on whole body vibration and few on segmental vibration stimulating trunk or leg muscles.[8],[9],[10],[11] We compared our results with available studies using vibration therapy as an intervention.

During training, the participants described FOG episodes to be reduced noticeably while wearing the PDShoes at the study site. However, the participants did not report any change in FOG characteristics as measured by FOG-Q when they were not wearing the PDShoes. There are four items on severity of freezing, whereas only one item on frequency of freezing in the FOG-Q; as such, it has poor sensitivity for detecting improvement in frequency of freezing episodes. Training with PDShoes improved the fear of falling in day-to-day activities. A statistically significant improvement was observed in FES-I that sustained even at 2 weeks although fear of falling was independently associated with frequency of falls.[26] Thomas et al.[26] reported patients with PD who were most frequent fallers did not have the higher fear of fall and there were many more reasons such as disease severity, mental function, and previous experiences with falls that contribute to fear of fall. In a comparative study of whole body vibration with conventional physiotherapeutic exercises, superiority of either program was not shown[27] but vibration training may be attractive for those who were unwilling or unable to exercise regularly.[28]

Effect of vibration training on motor symptoms

Vibration therapy has shown potential to improve motor functions. In a study on rats, Nakamura et al.[29] showed activation of dopaminergic pathways by vibratory stimulations that are associated with improvement in motor activities. In another study, Cardinale et al.[30] showed that a single session of whole body vibration therapy produces a rapid and sustained increase in insulin-like growth factor-1 and cortisol levels in elderly population, which simulates strength training-like effects to improve motor functions. We did not observe a clinically important difference in the motor scores measured by UPDRS III as the median score of the UPDRS III remained constant across measurements at baseline, after intervention, and follow-up. Our findings were in contrast to those of Haas et al.[8] who reported an improvement of 25% and 24% in tremor and rigidity score, respectively, after administering random whole body vibration.

Effect of training on balance and functional mobility

Training with the PDShoe improved functional mobility as there was 21% reduction in time to complete the TUG test. Training also improved balance (postural stability) as there was improvement by three points in BBS. Vibration training provides proprioceptive and tactile stimuli to the body. These stimuli reach sensory cortex and may improve strength and endurance, which is a prerequisite for postural stability and gait.[31] Our results are in concordance with a similar study by Novak and Novak,[11] where they used step-synchronized vibration training in patients with PD and reported improvements in gait speed and steadiness.

Effect of training on health-related quality of life

Health-related quality of life was measured by PDQ-39 scale. There was 25% improvement in total score of PDQ-39 after training. Quality of life in chronic conditions such as PD reflects the patients’ overall perception of effect of intervention on physical, social, and emotional domains of their lives. We found improvement in all eight domains of PDQ-39 after training but this effect was more prominent in mobility and activities of daily living. Our results are in agreement with a study by Soares et al.,[32] which showed beneficial effect of vibration therapy on quality of life.

The major limitation of this study was lack of a control group, thus limiting our ability to rule out a placebo effect, as was the case in a previous study, which showed a placebo effect of whole body vibration compared to that of control group.[33] However, to overcome this flaw, we used each patient as his/her own control and compared the results pre- and post-intervention and at 2-week follow-up. In the statistical analysis, Bonferroni correction was not used after post hoc analysis as Perneger[34] cautioned against its use as it may increase probability of type II error in a pursuit to decrease type I error. This was a single-center study with a small sample size, thereby limiting its results for generalization to whole community of patients with PD. This study may serve as a pilot study for future researches with a more rigorous research methodology.


  Conclusion Top


Step-synchronized vibration is a novel intervention for people with PD who experience FOG. The findings from this study showed an improvement in FOG as reflected in improved TUG and FES-I scores, balance as shown by the change in BBS, and quality of life as shown in PDQ-39 self-report. The application of step-synchronized vibration is also safe in patients with PD who have undergone STN DBS and experienced FOG. Further research is warranted in larger number of participants with longer period of follow-up before it can be used in clinical practice.

Acknowledgement

We would like to thank Tania Shiva, Garima Dhankar, and Dr. Vineet Vashisht for helping in data collection.

Financial support and sponsorship

This work was supported by a grant from Indo-US Science and Technology Forum. The study sponsors had no involvement in the study design, collection, analysis, or interpretation of the data; in the writing of the manuscript; or in the decision to submit the manuscript for publication.

Conflicts of interest

There are no conflicts of interest.



 
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