Accepted Manuscript Assisted movement with proprioceptive stimulation reduces impairment and restores function in incomplete spinal cord injury Deborah Backus, PT, PhD Paul Cordo, PhD Amanda Gillott, OT Casey Kandilakis, PT, DPT Motomi Mori, PhD Ahmed M. Raslan, MD PII:
S0003-9993(14)00218-4
DOI:
10.1016/j.apmr.2014.03.011
Reference:
YAPMR 55781
To appear in:
ARCHIVES OF PHYSICAL MEDICINE AND REHABILITATION
Received Date: 22 April 2013 Revised Date:
11 February 2014
Accepted Date: 8 March 2014
Please cite this article as: Backus D, Cordo P, Gillott A, Kandilakis C, Mori M, Raslan AM, Assisted movement with proprioceptive stimulation reduces impairment and restores function in incomplete spinal cord injury, ARCHIVES OF PHYSICAL MEDICINE AND REHABILITATION (2014), doi: 10.1016/ j.apmr.2014.03.011. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT MOVEMENT AND STIMULATION IMPROVE FUNCTION
Assisted movement with proprioceptive stimulation reduces impairment and restores function in incomplete spinal cord injury
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Deborah Backus, PT, PhD Director, MS Research Director, SCI Upper Limb Research and Translation Lab
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Shepherd Center, Atlanta, GA
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Paul Cordo, PhD Professor, Dept of Biomedical Engineering
Oregon Health & Science University, Portland, OR
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Chief Technology Officer AMES Technology, Inc., Portland, OR
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Amanda Gillott, OT
Occupational Therapist and Clinician Researcher Shepherd Center, Atlanta, GA
[email protected] 2
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Casey Kandilakis, PT, DPT
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Occupational Therapist and Clinician Researcher Shepherd Center, Atlanta, GA
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Motomi Mori, PhD
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Professor, Division of Biostatistics Department of Public Health & Preventive Medicine Oregon Health & Science University, Portland, OR
Ahmed M. Raslan, MD
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[email protected] EP
Assistant Professor of Neurological Surgery
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Oregon Health & Science University, Portland, OR
[email protected] Corresponding author: Deborah Backus Shepherd Center, Atlanta, GA 2020 Peachtree Road NW Atlanta, Georgia 30309 3
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[email protected] RI PT
(404) 350-7599 Fax: (404) 350-7596 Abstract word count: 250
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Text word count: 3533
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Some contents of this manuscript were modified and presented as a poster at the 2012 ACRM (American Congress of Rehabilitation Medicine) Annual Conference in Vancouver, and have been submitted as a case study to the Journal of Neurological
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Physical Therapy.
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Author Cordo and Oregon Health & Science University (OHSU) both have significant financial relationships with AMES Technology, Inc., a company that may benefit from
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the work presented in this manuscript; this potential conflict of interest is managed by the OHSU Research Integrity Office.
Acknowledgements: The authors wish to acknowledge the contributions to this study by
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Linda Cordo, study coordinator and monitor for this study, and Heather Guerrero,
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Shepherd Center study coordinator and trainer for this study.
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Assisted movement with proprioceptive stimulation reduces impairment and restores function in incomplete spinal cord injury ABSTRACT
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Objective: To test whether, in people with incomplete tetraplegia, treatment combining
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assisted movement with vibration to the antagonist muscle would reduce impairments
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and restore upper limb (UL) function.
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Design: Prospective, pre-post study.
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Setting: University lab and non-profit rehabilitation hospital.
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Participants: We recruited 15 arms from 10 individuals (8 males, mean age 40.5, mean
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years post-spinal cord injury (SCI) 3) with chronic, incomplete tetraplegia.
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Intervention: Two to three 20-minute sessions per week over 9 to 13 weeks (25 sessions
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total) on the AMES device, which combines repeated movement with targeted vibration
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to the antagonist muscle.
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Main Outcome Measure(s): Strength and Active Motion Tests on the AMES device;
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International Standards for the Neurological Classification of SCI (ISNCSCI) motor and
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sensory exams; Modified Ashworth Scale (MAS); Grasp and Release Test (GRT); Van
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Lieshout Test (VLT); Capabilities of Upper Extremity questionnaire (CUE).
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Results: AMES Strength Test scores improved significantly in MCP flexion (p=0.024)
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and extension (p=0.0067), and wrist flexion (p=0.001) and extension (p1 yr) incomplete tetraplegia due to traumatic SCI, after 25
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sessions of AMES treatment, and again 3 months after treatment ended, to test the
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hypothesis that AMES treatment would reduce impairments and restore UL function in
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these people.
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METHODS
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Participants
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Prospective participants were identified from a database of people indicating
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interest in research opportunities, or who contacted an investigator in response to an
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advertisement. Candidates were screened to determine general eligibility. Medical
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approval for participation was required prior to initiating study procedures. Criteria for participation in the study included: 1) traumatic cervical, motor
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incomplete SCI (cervical 2 through cervical 7); 2) age 18-65 years; 3) at least 1 yr post
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SCI; 4) able to tolerate sitting upright for at least 1 hr; 5) able to identify >70% of the
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time the correct direction of passive finger/wrist motion in the UL being treated; 6) motor
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grade >1 in the wrist extensors, finger flexors, and finger abductors of the UL being
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treated; and 7) cognitively and behaviorally capable of complying with study procedures.
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Exclusion criteria included: 1) greater than 50% loss of range of motion (ROM)
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due to fracture, osteo-or rheumatoid-arthritis, or contractures; 2) concomitant traumatic
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brain injury (TBI) or CVA (participants who sustained mild TBI with no evidence of
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structural abnormalities as obtained from medical record, physician clearance letter, or
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participant/caregiver report qualified for the study); 3) chronic intrathecal baclofen
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therapy; 4) uncontrolled seizure disorder; 5) uncontrolled high blood pressure/angina; 6)
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participation in an activity-based or other therapy program; 7) progressive
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neurodegenerative disorder; or 8) any of the following in the treated UL: pain or exercise
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intolerance, deep vein thrombosis, peripheral nerve injury, skin condition not tolerant of
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the device, or Botox treatment in the previous 5 months. Whether the candidate met the
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criteria was determined via responses on a participant questionnaire, their medical record,
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when available, or through the medical release form signed by the candidate’s physician.
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Eighteen candidates were screened for inclusion of either of their ULs. If both ULs met
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the inclusion criteria, then both were enrolled in the study. There were 5 screen failures.
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Three candidates were excluded due to being too strong, one due to chronic degeneration
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of the spine, and one for no active abduction in the little finger. Five participants were
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enrolled for both ULs. In total, 18 ULs from 13 participants with traumatic SCI were
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enrolled in the study. Three enrolled participants withdrew from the study before
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completing all treatments and the post-treatment evaluation, leaving for analysis a total
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15 limbs in 10 people, all of which received both pre- and post-treatment evaluations.
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One drop-out stopped attending sessions, and could not be reached; one became ill,
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requiring hospitalization; and a third injured his hand and was unable to continue the
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study. These latter two adverse events were reported to the institutional research review
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board (IRB). Informed consent was obtained from all participants using a form approved
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by the IRB.
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When both ULs qualified for the study, treatment of both limbs was done consecutively, with the dominant UL being treated first, and the non-dominant being
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treated after the dominant UL had completed all treatment sessions and performed the
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follow-up evaluation.
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Therapy Device and Procedure
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Identical study activities were carried out at 2 sites (Site 1 and Site 2), with Site 1 serving as the Coordinating Center. At each site, a physical or occupational therapist
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performed the outcome measures, and a trained treatment specialist performed the
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treatment with the AMES device (AMES Technology, Inc., Portland, OR) (Figure 1) in a
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therapy gym.
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At the beginning of each treatment session, two tests were performed using the
AMES device. In the Strength Test, performed first for the metacarpophalangeal (MCP)
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joints (all 4 combined), and then for the wrist, the participant made 6 maximal-effort
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contractions, 3 in extension and 3 in flexion, while the AMES device held the hand static.
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The peak volitional torque produced during each of the 3 maximal efforts by the MCP
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joints and the wrist in each direction was averaged to provide an estimate of strength for
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that joint in that direction for that day. The treatment specialist also used the Strength
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Test results to adjust the participant’s target levels of assistance for the treatment session.
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In the Active Motion Test, which measured joint coordination and active ROM, the participant was instructed to follow a graphically presented target on the video screen
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by rotating the MCP joints or wrist in the AMES device through a 30° arc. The target
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moved at 2 deg/through the equivalent of ±15 deg extension and then ±15 deg flexion of
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all MCP finger joints or of the wrist, with intermittent 2-3 second pauses at 6 stop-points.
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For this test, the AMES device was set for minimal resistance to the applied movement .
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Scoring was based on the total time spent with the cursor in line with the target.
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After the completion of testing each session, the participant received treatment on
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the AMES device. During the AMES treatment of the MCP joints (20 min), the AMES
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device flexed and extended all of the MCPs of the thumb and fingers simultaneously and
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cyclically , with the participant assisting this motion. Each complete cycle of movement
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included 30-deg MCP extension (hand-opening) and 30-deg MCP flexion (hand-closing).
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Vibration (60 pps, 2 mm displacement) was applied to the MCP flexor tendons during
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hand-opening and to the extensor tendons during hand-closing in order to exaggerate the
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proprioceptive input that would naturally occur during the movement. Treatment of the
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wrist was carried out similarly (10 min), with cyclical wrist extension and flexion
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movements (30 deg at 5 deg/s), and vibration applied to the wrist flexors and extensors,
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respectively. In all cases the effort during movement was shown as visual biofeedback
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on the computer screen in front of the participant.
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Each participant trained 2-3 times a week, for a total of 25 therapy sessions over a period of 9-13 weeks. The AMES device logged the duration of each treatment session
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and the results of the Strength and Active Motion Tests. The AMES Strength and Active
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Motion Tests were not performed at the three-month follow-up evaluation.
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Outcome Measures
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Evaluation of impairment and function
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In addition to the AMES Strength and Active Motion Tests during each treatment
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session, a qualified PT or OT evaluated each participant before the study, after the last
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treatment, and 3 months after treatment ended. The clinician first determined the
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participant’s motor and sensory scores of the treated UL, according to the International
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Standards for Neurological Classification of SCI (ISNCSC).13 The Modified Ashworth
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Scale (MAS)14 was used to evaluate spasticity in the wrist-and-finger flexors and
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extensors, and in the elbow flexors and extensors; the 4 scores were summed for analysis.
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Function was evaluated with the Grasp and Release Test (GRT)15 and the Van Lieshout
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Test-Short Version (VLT).16 The participant’s perception of function was assessed using
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the self-evaluation Capabilities of Upper Extremity (CUE) instrument.17
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Data Acquisition and Analysis
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Upon enrollment, each participant was assigned a numerical code that was used to identify data collected in the course of the study. All data were stored either on a
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computer using the participant-code as an identifier, or in a locked file cabinet in the
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Study Coordinator’s office. The data were accessible to the PI, the Co-investigators, and
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the Study Coordinator.
The unit of analysis was one UL, and each UL is considered independent even
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when both ULs from the same participant were treated. The analysis set of this single-
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arm, proof-of-concept study included 15 ULs from 10 participants, all of whom
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minimally completed both pre- and post-treatment evaluations. Two ULs from one
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participant, who fell outside the allowable age range (71.5 years), are included in the
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analysis set. This protocol deviation was reported to the IRB. Prior to enrolling the first
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participant, the GRT was designated as the primary outcome variable. As the AMES
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Strength and Active Motion Tests were performed 25 times, the average scores for
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sessions #1-3 were designated as the “pre-treatment” score and for sessions #23-25 as the
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“post-treatment” score.. Averages were used for these initial and final test scores to
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minimize the effects of day-to-day variability and motor learning.
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The Shapiro-Wilk test was used to assess the normality of the distribution for each outcome variable. Since there was no strong indication of non-normality, the mixed
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effects model (with a random subject effect) was used to analyze the MAS, ISNCSCI
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(motor – C5-T1; sensory – C2-T2), GRT, VLT and CUE outcome variables. Specifically,
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we evaluated whether there was a significant change over time in these scores (pre, post
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and follow-up). Bonferroni multiple comparison was used for pairwise time comparisons
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(pre vs. post, pre vs. follow-up, post vs. follow-up). Because the data from the AMES
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Strength and Active Motion Tests were not normally distributed, the Wilcoxon signed
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rank test was used to evaluate pre- versus post- changes. No multiple comparison
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procedure was performed to control the overall type I error of multiple outcome
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variables, as this was a small proof of concept study to investigate safety and to provide
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preliminary evidence of clinical efficacy. All statistical analyses were performed using
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Statistical Analysis System (SAS version 9.3).
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RESULTS
Participant demographics are presented in Table 1.
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Treatment effect on impairment level
Table 2 provides the means and standard deviations of clinical impairment
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assessments. There was no change in the MAS or ISNCSCI scores. . In contrast, Figure
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2 presents significant improvements in MCP and wrist strength and joint control , as
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measured by the AMES Strength and Active Motion Tests, respectively. 10
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Treatment effect on function
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Table 2 presents the scores for the GRT, VLT, CUE. Only GRT scores were
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significantly improved after training. The GRT scores also increased slightly between
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post-treatment and 3 months after the treatment ceased.
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Changes in somatosensation
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While we did not systematically test for changes in somatosensation, 5 of the 10 participants spontaneously reported a return of sensation to the digits after the first,
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second or third treatment session. Their comments, which were transcribed by the
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treatment specialist, included “I can feel my fingers for the first time since my injury”; “I
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can feel the bed sheets now”; and “I could feel enough to unlock the brake on my
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walker”.
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DISCUSSION
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Overall, treatment with a device that combines repeated movements with targeted
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vibration to the antagonist muscle led to some improvements in impairments and UL
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function in this population of people with chronic, incomplete tetraplegia due to
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traumatic SCI.
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AMES Strength and Active Motion Test scores improved in both MCP and wrist flexion and extension. Interestingly, we did not find significant changes in either the
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ISNCSCI or MAS outcome measures. The American Spinal Injury Association
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developed the ISNCSCI as the recommended practice guideline for evaluating and
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classifying the neurological impairment of SCI.13 The ISNCSCI only assesses five
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muscles of the UL (and five in the lower limb). Changes observed in UL function may
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be due to changes muscles not tested with the ISNCSCI. The MAS has been criticized as
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not being sensitive to the alterations in muscle tone and spasticity seen in SCI,18-20 and
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may not have been useful in determining changes in tone and spasticity in this study. The
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potential also exists that changes in tone and spasticity were not necessary for the
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changes observed in AMES Strength and Motion Test scores, and function.
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There was a 23% increase in GRT scores between pre- and post-treatment. Further, we recorded an additional 7.6% increase in scores between post-treatment and
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follow-up. While not significant, this increase nominally demonstrates that UL function
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restored during the course of treatment was retained, at least for the first 3 months post-
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treatment.
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However, there was no change on the VLT. There were two patterns of scores observed. In some cases, the participants were too strong for the VLT, such that .if they
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were able to do the VLT tasks before, they could also do them after. In other cases, if
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the participant had a low score at baseline, he/she also had a low score after completing
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25 treatments. Change was difficult to see, suggesting that for this population of
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participants with incomplete tetraplegia, the VLT may not be an appropriate measure.
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That there was a change in the GRT scores, but not in the VLT, may be due to the
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complexity of the tasks in the VLT. Specifically, the VLT tasks often require transport of
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the UL, not just function of the distal UL, whereas the tasks for the GRT are performed in
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a much smaller space, requiring less transport of the entire UL. The CUE also consists of
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complex tasks, which may also explain the lack of significant improvement in those
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scores as well. Participants may have improved in distal function and not proximal, and
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therefore there would be a discrepancy in these scores. This requires further
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investigation.
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The data from this study suggest that people with incomplete tetraplegia, even several years post-SCI, can achieve improvements in impairments and function with
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repetitive, impairment-oriented therapy that combines assisted movement with muscle
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vibration.. By reducing the extent of impairment in people with dysfunctional ULs, latent
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capacity for both sensory and motor function can emerge, even in the severely impaired.
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This is an important area requiring further study. Unfortunately, people with incomplete
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tetraplegia often have difficulty obtaining treatment to address their unique sensorimotor
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impairments. They are often treated in similar fashion to those with complete tetraplegia,
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using bracing and substitution for their dysfunction, when in fact they have the potential
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for greater independent function, if given the opportunity, such as with impairment-
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oriented interventions like AMES.
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The mechanisms underlying the changes observed in this study remain to be
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elucidated. The goal of this pilot study was to first explore the potential for people with
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chronic incomplete tetraplegia to demonstrate changes in impairments and function after
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treatment with repeated movement and enhanced sensation. Therefore, a comparison has
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not yet been made between the outcomes after repeated treatment alone, vibration alone
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and the combination of the two, as used in this study.
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Insights into potential mechanisms can be gained, however, from other studies in people with incomplete tetraplegia. Our findings are in line with previous studies which
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showed that repetitive physical training with submotor threshold electrical stimulation to
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the median nerve improved somatosensation and strength in people with chronic
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tetraplegia >1 yr post-SCI.21-23 Given that the median nerve supplies the skin and other
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tissues of the thumb, index and middle fingers, electrical stimulation provided in this
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fashion likely activated somatosensory input from a wide variety of mechanoreceptors
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throughout the nerve’s sensory field(s). Muscle vibration as applied in our study provided
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a different type of stimulation. Vibration via one or more tendons activates principally
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muscle spindle Ia afferents, although a small number of cutaneous afferents located
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directly under the probe will also be activated. Furthermore, the AMES vibrators can
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specifically alternate the activation of muscle spindles from one side of the joint to the
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other during treatment, just as occurs during natural movement. Thus, the AMES
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approach to augmenting proprioceptive input may be perceived by the CNS as more
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natural than electrical nerve stimulation, which could then produce a more pragmatic
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form of CNS plasticity, and lead to greater functional improvements. Further study is
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warranted to test this hypothesis.
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Study Limitations
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This was a single-arm trial without a placebo group, and thus we did not control
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for expectancy effect or natural recovery processes. Furthermore, the SCI was not fully
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characterized in the participants of this study. Specifically, the zone of partial
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preservation and extent of remaining function were not defined. If a participant had a
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motor exam within a year, another one was not performed, except for the five key
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muscles of the ISNCSCI13 at the time of pre- and post- assessments. The inclusion
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criteria were chosen, however, to allow more homogeneity in the sample, by having all
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participants have similar functional abilities. Future studies should employ methods to
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characterize the SCI more clearly to allow better interpretation of the findings.
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Another limitation is that changes in somatosensation described verbally by the participants, were not quantified. Given the role somatosensation may play in the normal
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control of UL movement,24-29 as well as the aforementioned anecdotal evidence for
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changes in somatosensory perception, further research is warranted in which
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somatosensation is accurately and comprehensively tracked throughout the study.
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Finally, in this study 5 participants trained on the AMES device with both
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qualified ULs, one after the other. Treating the first UL could have affected subsequent
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outcomes in the second UL due to bilateral effects. This requires further investigation.
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CONCLUSIONS
Some people with chronic incomplete tetraplegia may experience improvements
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in impairments and function after impairment-oriented treatment on a novel device
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combining repeated movements with targeted vibration. These findings suggest that
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further investigation is warranted.
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25. Johansson RS, Häger C, Riso R. Somatosensory control of precision grip during unpredictable pulling loads. Experimental Brain Research 1992;89:192-203.
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26. Nowak DA, Hermsdörfer J. Selective deficits of grip force control during object manipulation in patients with reduced sensibility of the grasping digits. Neuroscience Research 2003;47:65-72.
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27. Jenmalm P, Dahlstedt S, Johansson RS. Visual and tactile information about objectcurvature control fingertip forces and grasp kinematics in human dexterous manipulation. Journal of Neurophysiology 2000;84:2984-97.
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28. Nowak DA, Glasauer S, Hermsdörfer J. How predictive is grip force control in the complete absence of somatosensory feedback?. Brain 2004;127:182-92.
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29. Augurelle AS, Smith AM, Lejeune T, Thonnard JL. Importance of cutaneous feedback in maintaining a secure grip during manipulation of hand-held objects. Journal of Neurophysiology 2003;89:665-71.
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Supplier List
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AMES Device
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AMES Technology, Inc.
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Portland, Oregon
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Figure Legends
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Figure 1: AMES treatment device.
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Figure 2. Reduction of UL impairment. Each bar graph includes test scores obtained
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before receiving and treatment (open bars) and after completing all treatments (filled
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bars). Strength Test scores increased significantly for MCP extension and flexion (A)
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and for wrist extension and flexion (B). Active Motion Test scores also increased
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significantly for the MCP joints (C) and the wrist (D). Strength units are Nm and Active
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Motion units are 0.1 s.
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Table 1—Participant Demographics Variable Level Participant Upper Limbs Number (%) Gender Female 2 (20%) Male 8 (80%) Enrollment per site Site 1 7 (70%) 12 (80%) Site 2 3 (30%) 3 (20%) Level of injury C2-C3 3 (30%) C4-C7 7 (70%) Number of 24 1 (7%) sessions 25 13 (87%) 26 1 (7%) Mean (SD) and Minimum-Maximum Range Age at SCI (years) 40.5 (13.0) 24.3 -71.5 ASIA Motor Score 15.8 (3.9) 9-21 Time since injury 3.0 (1.1) (years) 1.0-4.9
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C=cervical
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Clinical Assessment of Impairment 15, 14, 13 5.3 (3.4) 4.4 (3.2) 15, 13, 11 15.3 (3.9) 14.6 (4.4)
4.2 (3.3) 16.1 (4.7)
0.371 0.299
15, 14, 12
14.1(3.3)
13.8 (3.3)
14.5 (3.1)
0.459
15, 14, 12
10.5 (5.4)
11.3 (5.3)
11.1 (4.6)
0.343
Assessment of Function 15, 15, 13 58.5 (37.9) 72.0 (40.0) 15, 15, 13 27.2 (11.8) 27.3 (11.1) 12, 14, 13 58.2 (23.0) 64.1 (24.6)
77.5 (44.9) 27.4 (12.6) 63.8 (25.8)
0.025 0.951 0.164
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GRT (no max) VLT (0 - 50) CUE (32-224)
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N = # of limbs tx = treatment ISNCSCI=International Standards for the Neurological Classification of SCI
AC C
P-value (pre-tx to followup)
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MAS (0 - 20) ISNCSCI Motor (0 - 25) ISNCSCI Sensory – Light touch (0 - 18) ISNCSCI Sensory – Pin Prick (0 - 18)
3-month follow-up Mean (SD)
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Outcome (units; range of scores)
Table 2—Descriptive Statistics N Pre-tx Post-tx (pre-tx, post- Mean (SD) Mean (SD) tx, follow-up)
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**
***
4.0 2.0
1.0
Extension
Flexion
0
THUMB-FINGERS
15
10
5
0
Flexion
Extension
THUMB-FINGERS
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WRIST
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35 Active Motion Test Score (s)
6.0
***
D
***
30 25
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**
8.0
C
SC
Strength (Nm)
* p≤0.05 ** p≤0.01 p≤0.001 *** 3.0
0
20
10.0
– Pre-treatment – Post-treatment
4.0
2.0
B
AC C
Strength (Nm)
5.0
12.0
Active Motion Test Score (s)
A
*
20
15
10 5 0
WRIST
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