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Effects of Overground Locomotor Training on Walking Performance in Chronic Cervical Motor Incomplete Spinal Cord Injury: A Pilot Study
Accepted Manuscript Effects of Overground Locomotor Training on Walking Performance in Chronic Cervical Motor-Incomplete Spinal Cord Injury: A Pilot Study Jared M. Gollie, PhD, Andrew A. Guccione, PT, PhD, DPT, FAPTA, Gino S. Panza, MS, Peter Y. Jo, MS, DC, Jeffrey E. Herrick, PhD PII:
S0003-9993(16)31292-8
DOI:
10.1016/j.apmr.2016.10.022
Reference:
YAPMR 56733
To appear in:
ARCHIVES OF PHYSICAL MEDICINE AND REHABILITATION
Received Date: 19 May 2016 Revised Date:
21 October 2016
Accepted Date: 29 October 2016
Please cite this article as: Gollie JM, Guccione AA, Panza GS, Jo PY, Herrick JE, Effects of Overground Locomotor Training on Walking Performance in Chronic Cervical Motor-Incomplete Spinal Cord Injury: A Pilot Study, ARCHIVES OF PHYSICAL MEDICINE AND REHABILITATION (2017), doi: 10.1016/ j.apmr.2016.10.022. 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.
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Running Head
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Effects of Overground Locomotor Training
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Effects of Overground Locomotor Training on Walking Performance in Chronic Cervical
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Motor-Incomplete Spinal Cord Injury: A Pilot Study
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Authors
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Jared M. Gollie, PhD, Andrew A. Guccione, PT, PhD, DPT, FAPTA, Gino S. Panza, MS,
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Peter Y. Jo, MS, DC, Jeffrey E. Herrick, PhD
Institution where study was performed and author affiliation
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Department of Rehabilitation Science, George Mason University, Fairfax VA. All
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authors are affiliated with the Department of Rehabilitation Science.
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Acknowledgments
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The authors thank Randall E. Keyser, PhD, Lisa M.K. Chin, PhD, and John P. Collins,
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PhD, for their review and feedback of the manuscript. The authors would also like to
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express their appreciation to all those who assisted in the development and
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implementation of the training protocol.
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Andrew A. Guccione, PT, PhD, DPT, FAPTA Department of Rehabilitation Science George Mason University 4400 University Drive MS2G7 Fairfax, VA 22030 [email protected]
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Reprints: Not available.
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Corresponding Author:
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Conflicts of interest: None.
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Abstract
2 Objective: To determine the effects of a novel overground locomotor training (OLT)
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program on walking performance in people with chronic cervical motor-incomplete
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spinal cord injury (iSCI).
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Design: Before-After Pilot Study.
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Setting: Human performance research laboratory.
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Participants: Adults (n=6; age>18 years) with chronic cervical iSCI C & D according to
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the American Spinal Injury Association Impairment Scale (AIS).
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Intervention: OLT included two 90-minute sessions per week for 12-15 weeks.
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Training sessions alternated between uniplanar and multiplanar stepping patterns.
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Each session was comprised of five segments: joint mobility; volitional muscle
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activation; task-isolation; task-integration; activity rehearsal.
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Main Outcome Measures: Overground walking speed, oxygen consumption (VO2),
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carbon dioxide production (VCO2).
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Results: OLT increased overground walking speed (0.36±0.20 vs 0.51±0.24 m·s;
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P<0.001, d=0.68). Significant decreases in VO2 (6.6±1.3 vs 5.7±1.4 ml·kg·min;
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P=0.038, d=0.67) and VCO2 (753.1±125.5 vs 670.7±120.3 ml·min; P=0.036, d=0.67)
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during self-selected constant work-rate treadmill walking was also noted after training.
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Conclusions: OLT program used in this pilot study is feasible and improved both
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overground walking speed and walking economy in a small sample of people with
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chronic cervical iSCI. Future studies are necessary to establish the efficacy of this OLT
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program as well as to differentiate among potential mechanisms contributing to
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enhanced walking performance in people with iSCI following OLT.
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Exercise; Oxygen Consumption; Spinal Cord Injuries; Rehabilitation
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31 iSCI – motor-incomplete spinal cord injury
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OLT – overground locomotor training
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BWS – body-weight support
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FES – functional electrical stimulation
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AIS - American Spinal Injury Association Impairment Scale
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10MWT - 10-meter walk test
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CWR - constant work-rate
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MID - minimally important difference
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VO2 – oxygen consumption
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VCO2 – carbon dioxide production
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HR – heart rate
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RER – respiratory exchange ratio
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Decrements in gait velocity and walking performance are associated with increased
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energetic costs of walking in people who have motor-incomplete spinal cord injury
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(iSCI).1 This combination of less economical motor patterns and loss of
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cardiorespiratory fitness has a direct influence on endurance performance.2 Specific to
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walking economy, practice has been shown to reduce the energetic cost of task
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performance independent of changes in cardiorespiratory fitness.3,4 These changes in
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the metabolic cost of locomotion may be the result of improvements in mechanical
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efficiency, or conversely, improved gait mechanics may lower metabolic demands. The
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relationship between the amount of work done to move and the energy cost to perform
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it is dynamic in nature.5 Although improvements in walking speed have been reported
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following overground locomotor training (OLT), the effects of OLT on walking economy
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and metabolic adaptations in individuals with chronic iSCI are not entirely clear.6,7,8,9,10
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OLT is defined as any therapeutic exercise program aimed at promoting walking
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improvements through intense practice of walking performed overground.11 Approaches
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to OLT are diverse and have included body-weight supported (BWS) exercise,
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functional electrical stimulation (FES), and manual assistance, in addition to
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conventional gait training.12 Training methods using such approaches most often
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emphasize training volume and movement specificity in an attempt to promote
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neuroplasticity and motor learning.13 Movement variability has also been identified as
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an essential element influencing the motor learning process. However, the inclusion of
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additional treatment modalities in the training program has made it difficult to
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identification of the singular impact of locomotor training on walking difficult.
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In the present study an OLT program consisting solely of patterned movement routines
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based on phases of the gait cycle was developed and performed exclusively in the
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environmental context of overground walking. OLT was based on motor learning theory
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using three fundamental principles of adaptation (i.e. task-specificity, progressive
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overload, task-variation) and structured within a part-to-whole practice
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paradigm.14,15,3,16 It was hypothesized that OLT would improve walking performance as
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determined by increased walking speed and enhanced walking economy in this
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particular sub-group of the iSCI population.
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Ethical Approval
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The protocol and procedures were approved by George Mason University Institutional
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Review Board. Informed consent was obtained from all participants prior to voluntary
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participation in this study. The consent process included verbal and written explanations
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of the experimental protocol, human subjects’ rights, and risks related to testing
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procedures and were given to each participant prior to their enrollment.
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Study Design
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The study used a single arm pre-experimental group with two testing time points; at
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baseline (pretest) and immediately following the OLT regimen (posttest). Participants
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were recruited from the greater Washington D.C. metropolitan area. Each participant
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completed 12-15 weeks of OLT two times per week for 90-minutes each session.
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Testing was performed at the same time of day for pre- and post-testing and
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participants were asked to refrain from eating at least 2 hours prior to testing.
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Participants included a convenient sample of individuals with chronic cervical motor-
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incomplete SCI C & D according to the American Spinal Injury Association Impairment
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Scale (AIS) (Table 1). Participants were considered for study inclusion if they were 18
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years of age or older, at least 12-months post-injury, able to stand with minimal
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assistance from one other person and initiate and complete at least one step
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independently with or without assistive walking aids, and demonstrate the ability to walk
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safely on a treadmill. Exclusion criteria included individuals with complete spinal cord
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injury (AIS A) and incomplete spinal cord injury AIS B, any significant orthopedic
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complications, spasms or contractures preventing safe ambulation on the treadmill, any
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history of ischemic heart disease, known cardiovascular, pulmonary, or metabolic
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diseases, HIV infection or use of antiretroviral therapy, severe psychiatric disease, illicit
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drugs, tobacco use, or pregnancy. Participants were asked to refrain from engaging in
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any structured locomotor training activities at least 48 hours prior to the initial exercise
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testing session and during their time enrolled in the study.
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Participants
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Testing
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114 Participants performed two testing visits: pretest and posttest. Each participant’s height
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and weight was obtained prior to the start of testing. Resting blood pressure and heart
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rate were taken with the participant in a seated position. Each testing visit consisted of a
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10-meter walk test (10MWT) and a constant work-rate (CWR) submaximal treadmill test
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while walking at a self-selected walking speed. All tests were performed under volitional
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control while bearing full-weight.
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121 10 Meter Walk Test (10MWT)
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Overground walking speed was determined via the 10 meter walk test (10MWT) in
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accordance with the Common Data Elements for Spinal Cord Injury.17 The 10MWT was
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performed overground on a level, uncarpeted surface. Participants were asked to walk a
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distance of 10 meters using their preferred walking aids, as safely and as quickly as
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possible while attempting to maintain quality gait mechanics. Participants stood quietly
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for several seconds prior to receiving a “go” command. Participants were instructed to
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come to a complete stop immediately upon passing the 10 meter mark and to stand still
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for several seconds. The same preferred walking aids were used at both testing time
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points. The 10MWT protocol was a standardized built-in protocol of a mobility software
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packagea.
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Overground Walking Speed
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All participants wore pressure-mapping insolesb and the time taken to complete the
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10MWT was calculated from the start and stop times from the measured ground
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reaction force. Data were filtered with a 4th order, low-pass, Butterworth filter and
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individual steps were identified. A custom MATLABc script determined mean force
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amplitude over all steps. For the purposes of this study gait initiation was defined as the
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first moment force on either foot achieved at least 85% of the mean amplitude while the
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opposite foot reached less than 20% of the mean amplitude. Gait termination was
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defined as the final time point where one limb achieved at least 85% of the mean
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amplitude while the opposite foot was less than 20% of the mean amplitude. At no point
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during quiet standing before or after the 10 meter walk did force amplitudes meet the
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proposed criteria. Minimally important difference (MID) was estimated for changes in
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overground walking speed using the 0.2 standard deviation approach as proposed by
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Musselman (2007), where s2 is the pretest and posttest pooled standard deviation and
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0.2 is the defined effect size for MID.18
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Eq. 1
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Constant Work-Rate (CWR) Submaximal Treadmill Test
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The CWR test included a 6-minute bout of walking at a self-selected speed on a
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standardized treadmilld. A 3-minute bout of static standing prior to the 6-minute walking
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bout was performed to obtain baseline values in pulmonary gas exchange and heart
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rate measures. Prior to the start of the CWR treadmill test, a familiarization period was 7
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completed which included walking on the treadmill at a variety of speeds for several gait
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cycles to ensure all participants could safely perform the test and to determine each
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participant’s self-selected walking speed. Each participant was instructed to select a
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speed which best approximated their preferred walking speed while walking on a
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treadmill or a speed which they felt most comfortable walking at for 6-minutes. The
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treadmill was capable of increasing speed by 0.1 mph. The self-selected speed chosen
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at baseline was the same speed used during the post-testing session. All participants
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were allowed to use the handrails for balance but were asked not to unload the lower
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extremity during the test.
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Pulmonary Gas Exchange and Heart Rate
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Pulmonary gas exchange was measured continuously using a breath-by-breath open
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circuit gas analysis systeme. Heart rate (HR) was measured by a 12-lead
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electrocardiogram (ECG). Baseline oxygen consumption (VO2), carbon dioxide
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production (VCO2), respiratory exchange ratio (RER) and HR were determined by
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averaging data over the 3-minute standing rest period. If participants were unable to
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stand for the duration of 3-minutes the protocol was modified according to their
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tolerance. VO2, VCO2, RER and HR during exercise were determined by averaging the
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last 2-minutes of the 6-minute CWR bout. RER was calculated by dividing breath-by-
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breath VO2 (ml·min) over VCO2 (ml·min). All data averaging was calculated using raw
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data. Walking economy was assessed using a 6-minute CWR treadmill test to allow us
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to compare the VO2 required for the same self-selected work intensity at both pre-test
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and post-test time points. Walking economy was determined by subtracting baseline
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VO2 from exercise VO2.
185 Estimated VO2 of Treadmill Walking
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The estimated VO2 of treadmill walking can be determined by the following equation:
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VO2 (ml·kg·min) = 3.5 + 0.1 x speed (m·min) + 1.8 x speed (m·min) x grade.16
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Eq. 2
For the purposes of this study, this equation was modified to allow for comparison of the
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estimated VO2 required above rest by removing the resting component (i.e. 3.5) and
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excluding the grade component (i.e. 1.8 x speed (m·min) x grade) since all CWR tests
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were performed with zero percent grade.
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VO2 (ml·kg·min) = 0.1 x speed (m·min)
Overground Locomotor Training (OLT)
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The OLT protocol consisted of two 90-minute training sessions per week. Three
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participants performed 15-weeks of OLT (30 sessions) and three participants performed
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12-weeks of OLT (24 sessions). Unlike training methods that focus exclusively on
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forward stepping, we also emphasized lateral stepping, cross-over stepping, backward
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stepping, and rotational stepping. One training session per week was devoted to
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uniplanar movement and the other session to multiplanar movement drills. Each
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movement emphasis was deconstructed into subcomponents using task analysis.
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These subcomponents were then organized into part-practice and whole-practice
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sequences.14,15,19 Each training session was comprised of five segments: joint mobility;
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volitional muscle activation; task-isolation; task-integration; and activity rehearsal as
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outlined in Table 2. The exercises selected for the joint mobility and volitional muscle
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activation segments were chosen based on the participant’s primary impairments of
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body structures and functions, as defined by the International Classification of
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Functioning, Disability, and Health.20 During segments of task-isolation and task-
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integration, part-practice was used to progressively introduce the actions (e.g. hip
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flexion, knee extension) and tasks (e.g. terminal swing) specific to the activity focus
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(e.g. swing phase) of that session. Following task-isolation and task-integration, whole-
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practice of the activity was performed while continuing to emphasize the components
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practiced during task-isolation and task-integration.14 All exercises were performed
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under volitional control without the assistance of body-weight support harnesses, robotic
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devices, or electrical stimulation. To ensure treatment fidelity, all training sessions were
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implemented by physical therapists and or exercise physiologists who were previously
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trained in the methodology of the OLT program developed for this study. The content of
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each session was planned in advance and executed according to the written plan for
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that session. Example session plans are provided in appendix A and appendix B.
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Sessions were standardized across the duration of the program. Table 3 outlines the
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sequencing of sessions across a 12-week period.
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Data Analysis
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using paired t-tests. All data were inspected visually for signs of non-normality. If data
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distribution appeared to be non-normal then Mann-Whitney tests were used instead of
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paired t-tests. Effect sizes were calculated using Cohen’s d (effect size = d). Statistical
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significance was set at a level of p<0.05 for two-tailed hypotheses. All values are
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expressed as means ± SD. All statistical analyses were performed using SPSS version
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19f.
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Results
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In the six individuals with chronic cervical iSCI AIS C and D that were studied, the time
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between injury and study enrollment ranged from 2 to 5 years. All subjects had been
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discharged from any in-hospital and community-based rehabilitation programs in which
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they participated. At the time of enrollment four participants relied on a wheelchair, one
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participant relied on a walker, and one participant walked independently as their primary
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mode of community locomotion. OLT did not result in any adverse events.
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Following OLT, no significant changes in standing VO2 at rest (4.5±1.1 vs 4.8±1.3
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ml·kg·min, p=0.068); VCO2 (314.3±74.6 vs 312.6±47.7 ml·min; p=0.927); RER
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(0.90±0.05 vs 0.84±0.03, p=0.113); or HR (93±15 vs 91±16 bpm, p=0.825) were
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observed. No significant changes in BMI (23.8±4.5 vs 23.8±4.0, p=0.947) were
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observed over the study period.
253 The range of overground walking speed prior to training was 0.15 m·s to 0.67 m·s. After
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training, overground walking speed was significantly increased during the 10MWT
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(0.36±0.20 vs 0.51±0.24 m·s; p<0.001, d=0.68) (Figure 1) with a range of overground
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walking speeds of 0.24 m·s to 0.88 m·s. All participants increased their overground
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walking speed at the completion of training above the calculated MID of 0.04 m·s, with a
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mean improvement of 0.15 m·s (Figure 2).
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Cardiorespiratory data during 6-minutes the CWR treadmill test are presented in Table
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4. The average preferred walking speed for the CWR treadmill test was 0.9 mph. The
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VO2 during treadmill walking was significantly lower after training than before training
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(6.6±1.3 vs 5.7±1.4 ml·kg·min; p=0.038, d=0.67). Furthermore, VCO2 was significantly
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reduced during CWR treadmill walking after OLT (753.1±125.5 vs 670.7±120.3 ml·min;
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p=0.036, d=0.67). The VO2 required above standing rest during self-selected walking
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was significantly greater than the estimated VO2 both before (6.6±1.3 vs 1.9±0.78
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ml·kg·min, p<0.05) and after training (5.7±1.4 vs 1.9±0.78 ml·kg·min; p<0.05). There
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were no significant changes in HR (104±15 vs 98±14 bpm, p=0.135, d=0.41) or RER
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(0.87±0.05 vs 0.82±0.04, p=0.147, d=1.1) during CWR treadmill walking following
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training as a result of OLT.
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Discussion
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274 This study investigated the effects of a standardized OLT program on walking speed
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and economy in people with chronic cervical iSCI. All participants demonstrated
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increased overground walking speeds during the 10MWT. Significant improvements in
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the walking economy of all participants was also observed at the completion of training
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reflecting a reduction in VO2 required during CWR self-selected treadmill walking. In
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addition, there was a reduction in VCO2 after OLT possibly suggesting improved aerobic
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contributions to walking performance.
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The OLT training program used in this study resulted in a significant increase in
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overground walking speed corroborating previous studies investigating OLT approaches
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in this population.9,10 After 12-weeks of OLT a mean gait velocity of 0.43 m·s was
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achieved which is just below the proposed minimal walking speed of 0.45 m·s to be
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categorized as assisted walkers or better.22 Training also led to a mean improvement of
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0.15 m·s in overground walking speed which is above the estimated MID of 0.04 m·s
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calculated from the pre-test post-test overground walking speed for the iSCI sample in
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this study.18 Sharp et al. (2014) reported significant improvements in overground
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walking speed using a part-to-whole practice approach which emphasized skill
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acquisition through repetitive practice of the components of ambulation.10 The part-to-
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whole OLT program developed for the current study included lateral, cross-over,
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backward, and rotational stepping in addition to forward stepping which we believe
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provides a valuable stimulus for motor learning as previously proposed.3,23 Collectively,
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our results support the inclusion of structured stepping variability within the part-whole
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practice paradigm for the improvement of overground walking speed which could
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increase the potential for persons with chronic cervical iSCI to transition into higher
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ambulatory categories.
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following spinal cord injury.24,21,25 An improvement in walking economy following 12-
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weeks of treadmill-based and overground locomotor training using transcutaneous
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electrical stimulation in individuals with iSCI has been previously reported.26 Walking
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economy was measured during 2 to 3 minutes of overground walking by dividing
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walking velocity by VO2.26 VO2 measured during the self-selected treadmill walking pace
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in the current study was significantly reduced following OLT reflecting what may be
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biomechanical and or bioenergetic adaptations associated with the task-specific nature
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of the OLT. The reduction in VO2 during treadmill walking likely suggests an overall
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improvement in walking economy. Despite this improvement, the steady state VO2
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requirement for self-selected walking for the individuals in our study was still above the
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estimated VO2 demands.
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Beneficial training adaptations to endurance exercise in able-bodied individuals include
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reductions in VCO2 for a given exercise intensity.16 The decrease in VCO2 is in part
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suggestive of a shift from the reliance of anaerobic metabolism to an increased
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contribution on aerobic metabolism, and thus a more economical and sustained
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movement pace.16 Our results are consistent with these adaptations showing that the
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OLT developed for this study had a significant effect on the reduction of VCO2 during a
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bout of CWR self-selected treadmill walking. The lowering of RER from 0.87 to 0.82
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further supports the reduction of VCO2 for a given amount of VO2. Therefore, the novel
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OLT developed for this study also seems to offer beneficial metabolic adaptations in
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addition to functional improvements and may provide a useful practice template to guide
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the structuring of other OLT programs which aim to improve both functional and
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metabolic aspects of walking performance.
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Practice includes the structuring of training activities with a specific goal of improving
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task performance.27 Many variables must be considered when organizing, structuring,
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and sequencing task-practice to improve walking performance following spinal cord
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injury. The training paradigm used in the current study was a part-to-whole practice
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approach guided by motor learning theory and principles of adaptation. These key
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principles can aid in selecting the content, complexity, intensity and volume as well as
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the most appropriate environment for which a treatment should be administered.
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Study Limitations
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This study had several limitations. First, the sample was small and all participants were
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traumatic chronic cervical iSCI, functioning at a relatively high level post-rehabilitation
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with partial ambulatory abilities. Thus, the homogeneity regarding the similarity of the
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injury makes generalization of our findings to a range of other spinal cord injuries at
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different points in recovery difficult. Second, the changes in length of training periods
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(i.e. 12-15 weeks) may have influenced the dose-response relationship and therefore
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the magnitude of change experienced across participants. Third, changes in gait
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characteristics were not assessed directly, circumventing more definitive determination
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of whether the changes in walking economy were the result of improved
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cardiorespiratory fitness or enhanced gait quality or perhaps both. Fourth, because
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walking economy was assessed on a treadmill we were unable to determine if changes
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in walking economy translated to overground walking. Last, the lack of a comparison
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group does not allow for direct comparison to other locomotor intervention treatments
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and determination of its superiority, equivalence, or inferiority to other locomotor
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approaches.
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354 Conclusion
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In summary, these data suggest that the OLT program used in this pilot study is feasible
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and improved both overground walking speed and walking economy in a small sample
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of people with chronic cervical iSCI. Future studies are necessary to establish the
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efficacy of this OLT program as well as to differentiate among potential mechanisms
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contributing to enhanced walking performance in people with iSCI following OLT.
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References
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Waters RL, Yakura JS, Adkins RH. Gait performance after spinal cord injury. Clin Orthop. 1993;(288):87-96.
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Bassett DR, Howley ET. Limiting factors for maximum oxygen uptake and determinants of endurance performance. Med Sci Sports Exerc. 2000;32(1):70-84.
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3.
Ranganathan R, Newell KM. Changing up the routine: intervention-induced variability in motor learning. Exerc Sport Sci Rev. 2013;41(1):64-70. doi:10.1097/JES.0b013e318259beb5.
374 375 376
4.
Lay BS, Sparrow WA, Hughes KM, O’Dwyer NJ. Practice effects on coordination and control, metabolic energy expenditure, and muscle activation. Hum Mov Sci. 2002;21(5-6):807-830.
377 378
5.
Sparrow WA, Newell KM. Metabolic energy expenditure and the regulation of movement economy. Psychon Bull Rev. 1998;5(2):173–196.
379 380 381
6.
Dobkin B, Apple D, Barbeau H, et al. Weight-supported treadmill vs over-ground training for walking after acute incomplete SCI. Neurology. 2006;66(4):484-493. doi:10.1212/01.wnl.0000202600.72018.39.
382 383 384
7.
Musselman KE, Fouad K, Misiaszek JE, Yang JF. Training of Walking Skills Overground and on the Treadmill: Case Series on Individuals With Incomplete Spinal Cord Injury. Phys Ther. 2009;89(6):601-611. doi:10.2522/ptj.20080257.
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8.
Alexeeva N, Sames C, Jacobs PL, et al. Comparison of training methods to improve walking in persons with chronic spinal cord injury: a randomized clinical trial. J Spinal Cord Med. 2011;34(4):362-379. doi:10.1179/2045772311Y.0000000018.
389 390 391
9.
Field-Fote EC, Roach KE. Influence of a locomotor training approach on walking speed and distance in people with chronic spinal cord injury: a randomized clinical trial. Phys Ther. 2011;91(1):48-60. doi:10.2522/ptj.20090359.
392 393 394 395
10. Sharp KG, Gramer R, Butler L, Cramer SC, Hade E, Page SJ. Effect of Overground Training Augmented by Mental Practice on Gait Velocity in Chronic, Incomplete Spinal Cord Injury. Arch Phys Med Rehabil. 2014;95(4):615-621. doi:10.1016/j.apmr.2013.11.016.
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11. Morawietz C, Moffat F. Effects of Locomotor Training After Incomplete Spinal Cord Injury: A Systematic Review. Arch Phys Med Rehabil. 2013;94(11):2297-2308. doi:10.1016/j.apmr.2013.06.023.
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12. Morawietz C, Moffat F. Effects of Locomotor Training after Incomplete Spinal Cord Injury: A Systematic Review. Arch Phys Med Rehabil. 2013;94(11):2297-2308. doi:10.1016/j.apmr.2013.06.023.
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13. Behrman AL, Harkema SJ. Physical rehabilitation as an agent for recovery after spinal cord injury. Phys Med Rehabil Clin N Am. 2007;18(2):183-202, v. doi:10.1016/j.pmr.2007.02.002.
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14. Carr JH, Shepherd RB. Movement Science: Foundations for Physical Therapy in Rehabilitation. 2nd edition. Gaithersburg, MD: Pro-Ed; 2000.
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15. Davids KW, Button C, Bennett SJ. Dynamics of Skill Acquisition : A Constraints-Led Approach. Champaign, Illinois: Human Kinetics; 2008. http://www.humankinetics.com/products/showproduct.cfm?isbn=9780736036863. Accessed November 14, 2015.
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16. Brooks GA. Exercise Physiology: Human Bioenergetics and Its Applications. 4th ed. Boston: McGraw-Hill; 2005.
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17. Biering-Sørensen F, Alai S, Anderson K, et al. Common data elements for spinal cord injury clinical research: a National Institute for Neurological Disorders and Stroke project. Spinal Cord. 2015;53(4):265-277. doi:10.1038/sc.2014.246.
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18. Musselman KE. Clinical significance testing in rehabilitation research: what, why, and how? Phys Ther Rev. 2007;12(4):287-296. doi:10.1179/108331907X223128.
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19. Shumway-Cook A, Woolacott MH. Motor Control: Translating Research into Clinical Practice. 4th edition. Philadelphia: LWW; 2011.
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20. World Health Organization. International Classification of Functioning, Disability and Health. 1 edition. Geneva: World Health Organization; 2001.
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21. Waters RL, Lunsford BR. Energy cost of paraplegic locomotion. J Bone Joint Surg Am. 1985;67(8):1245-1250.
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22. Hedel HJA van. Gait Speed in Relation to Categories of Functional Ambulation After Spinal Cord Injury. Neurorehabil Neural Repair. 2009;23(4):343-350. doi:10.1177/1545968308324224.
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23. Shah PK, Gerasimenko Y, Shyu A, et al. Variability in step training enhances locomotor recovery after a spinal cord injury: Limits to task-specific training. Eur J Neurosci. 2012;36(1):2054-2062. doi:10.1111/j.1460-9568.2012.08106.x.
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24. Cavanagh PR, Kram R. The efficiency of human movement--a statement of the problem. Med Sci Sports Exerc. 1985;17(3):304-308.
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25. Waters RL, Mulroy S. The energy expenditure of normal and pathologic gait. Gait Posture. 1999;9(3):207-231.
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26. Kressler J, Nash MS, Burns PA, Field-Fote EC. Metabolic responses to 4 different body weight-supported locomotor training approaches in persons with incomplete
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spinal cord injury. Arch Phys Med Rehabil. 2013;94(8):1436-1442. doi:10.1016/j.apmr.2013.02.018. 27. Schmidt R, Lee T. Motor Control and Learning: A Behavioral Emphasis. 5th edition. Champaign, IL: Human Kinetics; 2011.
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Suppliers a. APDM Wearable Technologies, The OPAL, (Portland, OR)
c. The Mathworks, MATLAB (Natick, MA) d. Trackmaster, TMX22 (Newton, KS)
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b. Novel, Pedar pressure-mapping insoles (Munich, DE)
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f. IBM Inc, SPSS version 19 (Armonk NY).
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e. Medical Graphics Corp, Medgraphics, Cardio 2 Ultima (St Paul, MN)
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Figure Legend
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1. Figure 1: Changes in group mean overground walking speed following OLT in people with chronic cervical motor-incomplete SCI. Bars represent mean walking
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speed as assessed during the 10 meter walk test. Error bars represent standard
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deviations. Significance was set at p≤0.05.
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2. Figure 2: Mean improvements in overground walking speed for each participant
following OLT in people with chronic cervical motor-incomplete SCI. Bars represent
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mean change in walking speed as assessed during the 10 meter walk test.
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Table 1: Participant Characteristics (N=6).
Gender
19 to 67 5 1
Etiology of injury Fall Motor vehicle accident Diving Other
1 1 3 1
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Age, years (range) Race/ethnicity White Hispanic/Latino
Time since injury, years (range) AIS Classification C D
2 to 5
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Level of injury Cervical 6 Mobility aids used for walking Walker 2 Crutches (bilateral axillary) 3 None 1
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Primary mode of community locomotion Wheelchair 4 Walker 2
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Male Female
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Table 2: Description of an example 12-week OLT program.
Movement Emphasis
Movement Pattern
1
Uniplanar
Stance Phase
2
Multiplanar
Lateral Stepping
3
Uniplanar
4
Multiplanar
5
Uniplanar
6
Multiplanar
7
Uniplanar
8
Multiplanar
9 10 11 12 Phase II
Cross-Over Stepping Stance Phase
Backwards Stepping Swing Phase
Rotational Stepping
Uniplanar
Stance Phase
Multiplanar
Lateral Stepping
Uniplanar
Swing Phase
Multiplanar
Cross-Over Stepping
Uniplanar
Stance Phase Backwards Stepping
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Uniplanar
Swing Phase
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Multiplanar
Rotational Stepping
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Uniplanar
Stance Phase
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Multiplanar
Lateral Stepping
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Uniplanar
Swing Phase
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Multiplanar
Cross-Over Stepping
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Uniplanar
Stance Phase
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Multiplanar
Backwards Stepping
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Uniplanar
Swing Phase
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Multiplanar
Rotational Stepping
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Swing Phase
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Training Phase
Phase III
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Table 3: OLT intra-session segmental breakdown.
Joint Mobility
Volitional Neuromuscular Activation
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Task-Isolation
Emphasis Exercises focus on improving joint mobility and muscle flexibility. Exercises focus on enhancing neuromuscular function pertaining to areas of the abdominal, thoracic and lumbar, and pelvic regions. Exercises which are sub-components of the activity of interest which are performed in isolation. Exercises which incorporate the motor patterns practiced during task-isolation into larger more complex movements. Practicing the activity in its entirety.
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Segment
Task-Integration
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Activity Rehearsal
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Table 4: Effect of OLT on cardiorespiratory outcomes. Post-test
P-value
Effect Size (d)
VO2 (ml·kg·min)
6.6 (1.3)
5.7 (1.4)
0.038*
0.67
VCO2 (ml·min)
753.1 (125.5)
670.7 (120.3)
0.036*
0.67
HR (bpm) RER Estimated VO2 (ml·kg·min)
104 (15) 0.87 (0.05) 1.9 (0.78)
98 (14) 0.82 (0.04)
0.135 0.147
0.41 1.1
CWR Walking Speed (mph)
0.9 (0.5)
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Pre-test
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Abbreviations: VO2, steady state oxygen consumption; VCO2, carbon dioxide
production; HR, heart rate; RER, respiratory exchange ratio; CWR, constant work-rate.
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Values are reported as mean (SD). Significance was set at p≤0.05.
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Appendix A – Example Uniplanar OLT Session Plan. Exercise
Sets
Repetitions
Joint Mobility
Passive Hamstring Stretch
1
3 x 30 seconds
Supine Active Hip Mobility
1
5 each leg/each direction
Standing Trunk Rotations
1
10 each direction
Standing Trunk Circles
1
10 each direction
1
10
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Activity Rehearsal
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Task-Integration
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Task-Isolation
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Standing Body Weight Squats Walking (Lofstrand Supported) Weight-Shift (Lofstrand Supported) Even Stance Anterior/Posterior Weight-Shift (Lofstrand Supported) Staggered Stance Anterior/Posterior Weight-Shift (Unsupported) Staggered Stance Anterior/Posterior Small Stepping (Lofstrand Supported) Small Stepping (Lofstrand Supported) Initial & MidSwing Emphasis Small Stepping with Pause (Unsupported) Small Stepping with pause (Unsupported) Walking Forward for 10 meters (Lofstrand Supported)
20 repetitions 20 repetitions 20 repetitions 10 repetitions
2 x 10 meters
10 each direction
60 repetitions
3
10 x 3 sec. holds each direction
60 repetitions
3
10 each direction
60 repetitions
3
10 each direction
60 repetitions
3
10 each direction
60 repetitions
3
5 steps each direction
3
10 each direction
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Volitional Neuromuscular Activation
Volume
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Segment
30 repetitions 60 repetitions
Perform for the remainder of the session
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Appendix B – Example Multiplanar OLT Session Plan. Exercise
Sets
Joint Mobility
Passive Hamstring Stretch
1
Supine Active Hip Mobility
1
Standing Trunk Rotations
1
10 each direction
Standing Trunk Circles
1
10 each direction
1
10
Weight-Shift (Unsupported)
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Activity Rehearsal
20 repetitions 20 repetitions 20 repetitions 10 repetitions
2 x 10 meters
3
10 each direction
60 repetitions
3
10 x 3 sec. holds each direction
60 repetitions
3
10 each direction
60 repetitions 60 repetitions
Lateral Stepping (Lofstrand 3 10 each direction Supported) Lateral Stepping with Trailing Leg Push-Off 60 3 10 each direction Emphasis (Lofstrand repetitions Supported) Lateral Stepping with 5 steps each 30 3 Pause (Unsupported) direction repetitions Lateral Stepping with 60 3 10 each direction pause (Unsupported) repetitions Lateral Stepping to Walking Forward for 10 meters Perform for the remainder of the session (Lofstrand Supported)
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Volume
1
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Task-Isolation
Standing Body Weight Squats Walking (Lofstrand Supported) Weight-Shift (Lofstrand Supported) Even Stance Medial/Lateral Weight-Shift (Lofstrand Supported) Even Stance Medial/Lateral with Single Leg Balance
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Volitional Neuromuscular Activation
Repetitions 3 x 30 seconds each leg 5 each leg/each direction
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Segment
S0003-9993(16)31292-8
DOI:
10.1016/j.apmr.2016.10.022
Reference:
YAPMR 56733
To appear in:
ARCHIVES OF PHYSICAL MEDICINE AND REHABILITATION
Received Date: 19 May 2016 Revised Date:
21 October 2016
Accepted Date: 29 October 2016
Please cite this article as: Gollie JM, Guccione AA, Panza GS, Jo PY, Herrick JE, Effects of Overground Locomotor Training on Walking Performance in Chronic Cervical Motor-Incomplete Spinal Cord Injury: A Pilot Study, ARCHIVES OF PHYSICAL MEDICINE AND REHABILITATION (2017), doi: 10.1016/ j.apmr.2016.10.022. 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.
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Running Head
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Effects of Overground Locomotor Training
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3 Title
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Effects of Overground Locomotor Training on Walking Performance in Chronic Cervical
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Motor-Incomplete Spinal Cord Injury: A Pilot Study
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Authors
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Jared M. Gollie, PhD, Andrew A. Guccione, PT, PhD, DPT, FAPTA, Gino S. Panza, MS,
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Peter Y. Jo, MS, DC, Jeffrey E. Herrick, PhD
Institution where study was performed and author affiliation
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Department of Rehabilitation Science, George Mason University, Fairfax VA. All
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authors are affiliated with the Department of Rehabilitation Science.
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Acknowledgments
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The authors thank Randall E. Keyser, PhD, Lisa M.K. Chin, PhD, and John P. Collins,
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PhD, for their review and feedback of the manuscript. The authors would also like to
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express their appreciation to all those who assisted in the development and
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implementation of the training protocol.
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Andrew A. Guccione, PT, PhD, DPT, FAPTA Department of Rehabilitation Science George Mason University 4400 University Drive MS2G7 Fairfax, VA 22030 [email protected]
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Reprints: Not available.
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Corresponding Author:
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Conflicts of interest: None.
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Abstract
2 Objective: To determine the effects of a novel overground locomotor training (OLT)
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program on walking performance in people with chronic cervical motor-incomplete
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spinal cord injury (iSCI).
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Design: Before-After Pilot Study.
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Setting: Human performance research laboratory.
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Participants: Adults (n=6; age>18 years) with chronic cervical iSCI C & D according to
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the American Spinal Injury Association Impairment Scale (AIS).
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Intervention: OLT included two 90-minute sessions per week for 12-15 weeks.
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Training sessions alternated between uniplanar and multiplanar stepping patterns.
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Each session was comprised of five segments: joint mobility; volitional muscle
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activation; task-isolation; task-integration; activity rehearsal.
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Main Outcome Measures: Overground walking speed, oxygen consumption (VO2),
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carbon dioxide production (VCO2).
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Results: OLT increased overground walking speed (0.36±0.20 vs 0.51±0.24 m·s;
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P<0.001, d=0.68). Significant decreases in VO2 (6.6±1.3 vs 5.7±1.4 ml·kg·min;
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P=0.038, d=0.67) and VCO2 (753.1±125.5 vs 670.7±120.3 ml·min; P=0.036, d=0.67)
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during self-selected constant work-rate treadmill walking was also noted after training.
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Conclusions: OLT program used in this pilot study is feasible and improved both
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overground walking speed and walking economy in a small sample of people with
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chronic cervical iSCI. Future studies are necessary to establish the efficacy of this OLT
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program as well as to differentiate among potential mechanisms contributing to
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enhanced walking performance in people with iSCI following OLT.
25 Keywords
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Exercise; Oxygen Consumption; Spinal Cord Injuries; Rehabilitation
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29 Abbreviations
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31 iSCI – motor-incomplete spinal cord injury
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OLT – overground locomotor training
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BWS – body-weight support
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FES – functional electrical stimulation
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AIS - American Spinal Injury Association Impairment Scale
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10MWT - 10-meter walk test
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CWR - constant work-rate
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MID - minimally important difference
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VO2 – oxygen consumption
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VCO2 – carbon dioxide production
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HR – heart rate
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RER – respiratory exchange ratio
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Decrements in gait velocity and walking performance are associated with increased
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energetic costs of walking in people who have motor-incomplete spinal cord injury
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(iSCI).1 This combination of less economical motor patterns and loss of
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cardiorespiratory fitness has a direct influence on endurance performance.2 Specific to
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walking economy, practice has been shown to reduce the energetic cost of task
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performance independent of changes in cardiorespiratory fitness.3,4 These changes in
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the metabolic cost of locomotion may be the result of improvements in mechanical
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efficiency, or conversely, improved gait mechanics may lower metabolic demands. The
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relationship between the amount of work done to move and the energy cost to perform
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it is dynamic in nature.5 Although improvements in walking speed have been reported
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following overground locomotor training (OLT), the effects of OLT on walking economy
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and metabolic adaptations in individuals with chronic iSCI are not entirely clear.6,7,8,9,10
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OLT is defined as any therapeutic exercise program aimed at promoting walking
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improvements through intense practice of walking performed overground.11 Approaches
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to OLT are diverse and have included body-weight supported (BWS) exercise,
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functional electrical stimulation (FES), and manual assistance, in addition to
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conventional gait training.12 Training methods using such approaches most often
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emphasize training volume and movement specificity in an attempt to promote
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neuroplasticity and motor learning.13 Movement variability has also been identified as
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an essential element influencing the motor learning process. However, the inclusion of
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additional treatment modalities in the training program has made it difficult to
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identification of the singular impact of locomotor training on walking difficult.
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In the present study an OLT program consisting solely of patterned movement routines
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based on phases of the gait cycle was developed and performed exclusively in the
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environmental context of overground walking. OLT was based on motor learning theory
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using three fundamental principles of adaptation (i.e. task-specificity, progressive
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overload, task-variation) and structured within a part-to-whole practice
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paradigm.14,15,3,16 It was hypothesized that OLT would improve walking performance as
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determined by increased walking speed and enhanced walking economy in this
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particular sub-group of the iSCI population.
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Ethical Approval
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The protocol and procedures were approved by George Mason University Institutional
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Review Board. Informed consent was obtained from all participants prior to voluntary
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participation in this study. The consent process included verbal and written explanations
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of the experimental protocol, human subjects’ rights, and risks related to testing
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procedures and were given to each participant prior to their enrollment.
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Study Design
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The study used a single arm pre-experimental group with two testing time points; at
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baseline (pretest) and immediately following the OLT regimen (posttest). Participants
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were recruited from the greater Washington D.C. metropolitan area. Each participant
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completed 12-15 weeks of OLT two times per week for 90-minutes each session.
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Testing was performed at the same time of day for pre- and post-testing and
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participants were asked to refrain from eating at least 2 hours prior to testing.
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Participants included a convenient sample of individuals with chronic cervical motor-
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incomplete SCI C & D according to the American Spinal Injury Association Impairment
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Scale (AIS) (Table 1). Participants were considered for study inclusion if they were 18
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years of age or older, at least 12-months post-injury, able to stand with minimal
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assistance from one other person and initiate and complete at least one step
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independently with or without assistive walking aids, and demonstrate the ability to walk
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safely on a treadmill. Exclusion criteria included individuals with complete spinal cord
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injury (AIS A) and incomplete spinal cord injury AIS B, any significant orthopedic
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complications, spasms or contractures preventing safe ambulation on the treadmill, any
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history of ischemic heart disease, known cardiovascular, pulmonary, or metabolic
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diseases, HIV infection or use of antiretroviral therapy, severe psychiatric disease, illicit
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drugs, tobacco use, or pregnancy. Participants were asked to refrain from engaging in
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any structured locomotor training activities at least 48 hours prior to the initial exercise
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testing session and during their time enrolled in the study.
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Participants
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Testing
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114 Participants performed two testing visits: pretest and posttest. Each participant’s height
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and weight was obtained prior to the start of testing. Resting blood pressure and heart
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rate were taken with the participant in a seated position. Each testing visit consisted of a
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10-meter walk test (10MWT) and a constant work-rate (CWR) submaximal treadmill test
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while walking at a self-selected walking speed. All tests were performed under volitional
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control while bearing full-weight.
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121 10 Meter Walk Test (10MWT)
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Overground walking speed was determined via the 10 meter walk test (10MWT) in
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accordance with the Common Data Elements for Spinal Cord Injury.17 The 10MWT was
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performed overground on a level, uncarpeted surface. Participants were asked to walk a
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distance of 10 meters using their preferred walking aids, as safely and as quickly as
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possible while attempting to maintain quality gait mechanics. Participants stood quietly
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for several seconds prior to receiving a “go” command. Participants were instructed to
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come to a complete stop immediately upon passing the 10 meter mark and to stand still
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for several seconds. The same preferred walking aids were used at both testing time
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points. The 10MWT protocol was a standardized built-in protocol of a mobility software
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packagea.
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Overground Walking Speed
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All participants wore pressure-mapping insolesb and the time taken to complete the
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10MWT was calculated from the start and stop times from the measured ground
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reaction force. Data were filtered with a 4th order, low-pass, Butterworth filter and
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individual steps were identified. A custom MATLABc script determined mean force
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amplitude over all steps. For the purposes of this study gait initiation was defined as the
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first moment force on either foot achieved at least 85% of the mean amplitude while the
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opposite foot reached less than 20% of the mean amplitude. Gait termination was
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defined as the final time point where one limb achieved at least 85% of the mean
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amplitude while the opposite foot was less than 20% of the mean amplitude. At no point
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during quiet standing before or after the 10 meter walk did force amplitudes meet the
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proposed criteria. Minimally important difference (MID) was estimated for changes in
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overground walking speed using the 0.2 standard deviation approach as proposed by
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Musselman (2007), where s2 is the pretest and posttest pooled standard deviation and
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0.2 is the defined effect size for MID.18
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Constant Work-Rate (CWR) Submaximal Treadmill Test
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The CWR test included a 6-minute bout of walking at a self-selected speed on a
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standardized treadmilld. A 3-minute bout of static standing prior to the 6-minute walking
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bout was performed to obtain baseline values in pulmonary gas exchange and heart
159
rate measures. Prior to the start of the CWR treadmill test, a familiarization period was 7
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completed which included walking on the treadmill at a variety of speeds for several gait
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cycles to ensure all participants could safely perform the test and to determine each
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participant’s self-selected walking speed. Each participant was instructed to select a
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speed which best approximated their preferred walking speed while walking on a
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treadmill or a speed which they felt most comfortable walking at for 6-minutes. The
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treadmill was capable of increasing speed by 0.1 mph. The self-selected speed chosen
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at baseline was the same speed used during the post-testing session. All participants
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were allowed to use the handrails for balance but were asked not to unload the lower
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extremity during the test.
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Pulmonary Gas Exchange and Heart Rate
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Pulmonary gas exchange was measured continuously using a breath-by-breath open
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circuit gas analysis systeme. Heart rate (HR) was measured by a 12-lead
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electrocardiogram (ECG). Baseline oxygen consumption (VO2), carbon dioxide
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production (VCO2), respiratory exchange ratio (RER) and HR were determined by
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averaging data over the 3-minute standing rest period. If participants were unable to
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stand for the duration of 3-minutes the protocol was modified according to their
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tolerance. VO2, VCO2, RER and HR during exercise were determined by averaging the
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last 2-minutes of the 6-minute CWR bout. RER was calculated by dividing breath-by-
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breath VO2 (ml·min) over VCO2 (ml·min). All data averaging was calculated using raw
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data. Walking economy was assessed using a 6-minute CWR treadmill test to allow us
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to compare the VO2 required for the same self-selected work intensity at both pre-test
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and post-test time points. Walking economy was determined by subtracting baseline
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VO2 from exercise VO2.
185 Estimated VO2 of Treadmill Walking
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The estimated VO2 of treadmill walking can be determined by the following equation:
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VO2 (ml·kg·min) = 3.5 + 0.1 x speed (m·min) + 1.8 x speed (m·min) x grade.16
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Eq. 2
For the purposes of this study, this equation was modified to allow for comparison of the
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estimated VO2 required above rest by removing the resting component (i.e. 3.5) and
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excluding the grade component (i.e. 1.8 x speed (m·min) x grade) since all CWR tests
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Eq. 3
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VO2 (ml·kg·min) = 0.1 x speed (m·min)
Overground Locomotor Training (OLT)
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The OLT protocol consisted of two 90-minute training sessions per week. Three
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participants performed 15-weeks of OLT (30 sessions) and three participants performed
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12-weeks of OLT (24 sessions). Unlike training methods that focus exclusively on
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forward stepping, we also emphasized lateral stepping, cross-over stepping, backward
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stepping, and rotational stepping. One training session per week was devoted to
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uniplanar movement and the other session to multiplanar movement drills. Each
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movement emphasis was deconstructed into subcomponents using task analysis.
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These subcomponents were then organized into part-practice and whole-practice
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sequences.14,15,19 Each training session was comprised of five segments: joint mobility;
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volitional muscle activation; task-isolation; task-integration; and activity rehearsal as
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outlined in Table 2. The exercises selected for the joint mobility and volitional muscle
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activation segments were chosen based on the participant’s primary impairments of
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body structures and functions, as defined by the International Classification of
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Functioning, Disability, and Health.20 During segments of task-isolation and task-
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integration, part-practice was used to progressively introduce the actions (e.g. hip
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flexion, knee extension) and tasks (e.g. terminal swing) specific to the activity focus
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(e.g. swing phase) of that session. Following task-isolation and task-integration, whole-
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practice of the activity was performed while continuing to emphasize the components
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practiced during task-isolation and task-integration.14 All exercises were performed
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under volitional control without the assistance of body-weight support harnesses, robotic
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devices, or electrical stimulation. To ensure treatment fidelity, all training sessions were
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implemented by physical therapists and or exercise physiologists who were previously
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trained in the methodology of the OLT program developed for this study. The content of
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each session was planned in advance and executed according to the written plan for
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that session. Example session plans are provided in appendix A and appendix B.
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Sessions were standardized across the duration of the program. Table 3 outlines the
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sequencing of sessions across a 12-week period.
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Data Analysis
230 Differences in overground walking speed, VO2, VCO2, RER and HR were analyzed
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using paired t-tests. All data were inspected visually for signs of non-normality. If data
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distribution appeared to be non-normal then Mann-Whitney tests were used instead of
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paired t-tests. Effect sizes were calculated using Cohen’s d (effect size = d). Statistical
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significance was set at a level of p<0.05 for two-tailed hypotheses. All values are
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expressed as means ± SD. All statistical analyses were performed using SPSS version
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19f.
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Results
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In the six individuals with chronic cervical iSCI AIS C and D that were studied, the time
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between injury and study enrollment ranged from 2 to 5 years. All subjects had been
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discharged from any in-hospital and community-based rehabilitation programs in which
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they participated. At the time of enrollment four participants relied on a wheelchair, one
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participant relied on a walker, and one participant walked independently as their primary
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mode of community locomotion. OLT did not result in any adverse events.
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Following OLT, no significant changes in standing VO2 at rest (4.5±1.1 vs 4.8±1.3
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ml·kg·min, p=0.068); VCO2 (314.3±74.6 vs 312.6±47.7 ml·min; p=0.927); RER
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(0.90±0.05 vs 0.84±0.03, p=0.113); or HR (93±15 vs 91±16 bpm, p=0.825) were
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251
observed. No significant changes in BMI (23.8±4.5 vs 23.8±4.0, p=0.947) were
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observed over the study period.
253 The range of overground walking speed prior to training was 0.15 m·s to 0.67 m·s. After
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training, overground walking speed was significantly increased during the 10MWT
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(0.36±0.20 vs 0.51±0.24 m·s; p<0.001, d=0.68) (Figure 1) with a range of overground
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walking speeds of 0.24 m·s to 0.88 m·s. All participants increased their overground
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walking speed at the completion of training above the calculated MID of 0.04 m·s, with a
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mean improvement of 0.15 m·s (Figure 2).
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Cardiorespiratory data during 6-minutes the CWR treadmill test are presented in Table
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4. The average preferred walking speed for the CWR treadmill test was 0.9 mph. The
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VO2 during treadmill walking was significantly lower after training than before training
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(6.6±1.3 vs 5.7±1.4 ml·kg·min; p=0.038, d=0.67). Furthermore, VCO2 was significantly
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reduced during CWR treadmill walking after OLT (753.1±125.5 vs 670.7±120.3 ml·min;
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p=0.036, d=0.67). The VO2 required above standing rest during self-selected walking
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was significantly greater than the estimated VO2 both before (6.6±1.3 vs 1.9±0.78
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ml·kg·min, p<0.05) and after training (5.7±1.4 vs 1.9±0.78 ml·kg·min; p<0.05). There
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were no significant changes in HR (104±15 vs 98±14 bpm, p=0.135, d=0.41) or RER
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(0.87±0.05 vs 0.82±0.04, p=0.147, d=1.1) during CWR treadmill walking following
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training as a result of OLT.
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Discussion
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274 This study investigated the effects of a standardized OLT program on walking speed
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and economy in people with chronic cervical iSCI. All participants demonstrated
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increased overground walking speeds during the 10MWT. Significant improvements in
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the walking economy of all participants was also observed at the completion of training
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reflecting a reduction in VO2 required during CWR self-selected treadmill walking. In
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addition, there was a reduction in VCO2 after OLT possibly suggesting improved aerobic
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contributions to walking performance.
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The OLT training program used in this study resulted in a significant increase in
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overground walking speed corroborating previous studies investigating OLT approaches
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in this population.9,10 After 12-weeks of OLT a mean gait velocity of 0.43 m·s was
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achieved which is just below the proposed minimal walking speed of 0.45 m·s to be
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categorized as assisted walkers or better.22 Training also led to a mean improvement of
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0.15 m·s in overground walking speed which is above the estimated MID of 0.04 m·s
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calculated from the pre-test post-test overground walking speed for the iSCI sample in
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this study.18 Sharp et al. (2014) reported significant improvements in overground
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walking speed using a part-to-whole practice approach which emphasized skill
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acquisition through repetitive practice of the components of ambulation.10 The part-to-
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whole OLT program developed for the current study included lateral, cross-over,
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backward, and rotational stepping in addition to forward stepping which we believe
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provides a valuable stimulus for motor learning as previously proposed.3,23 Collectively,
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our results support the inclusion of structured stepping variability within the part-whole
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practice paradigm for the improvement of overground walking speed which could
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increase the potential for persons with chronic cervical iSCI to transition into higher
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ambulatory categories.
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following spinal cord injury.24,21,25 An improvement in walking economy following 12-
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weeks of treadmill-based and overground locomotor training using transcutaneous
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electrical stimulation in individuals with iSCI has been previously reported.26 Walking
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economy was measured during 2 to 3 minutes of overground walking by dividing
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walking velocity by VO2.26 VO2 measured during the self-selected treadmill walking pace
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in the current study was significantly reduced following OLT reflecting what may be
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biomechanical and or bioenergetic adaptations associated with the task-specific nature
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of the OLT. The reduction in VO2 during treadmill walking likely suggests an overall
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improvement in walking economy. Despite this improvement, the steady state VO2
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requirement for self-selected walking for the individuals in our study was still above the
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estimated VO2 demands.
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Beneficial training adaptations to endurance exercise in able-bodied individuals include
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reductions in VCO2 for a given exercise intensity.16 The decrease in VCO2 is in part
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suggestive of a shift from the reliance of anaerobic metabolism to an increased
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contribution on aerobic metabolism, and thus a more economical and sustained
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movement pace.16 Our results are consistent with these adaptations showing that the
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OLT developed for this study had a significant effect on the reduction of VCO2 during a
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bout of CWR self-selected treadmill walking. The lowering of RER from 0.87 to 0.82
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further supports the reduction of VCO2 for a given amount of VO2. Therefore, the novel
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OLT developed for this study also seems to offer beneficial metabolic adaptations in
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addition to functional improvements and may provide a useful practice template to guide
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the structuring of other OLT programs which aim to improve both functional and
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metabolic aspects of walking performance.
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Practice includes the structuring of training activities with a specific goal of improving
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task performance.27 Many variables must be considered when organizing, structuring,
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and sequencing task-practice to improve walking performance following spinal cord
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injury. The training paradigm used in the current study was a part-to-whole practice
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approach guided by motor learning theory and principles of adaptation. These key
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principles can aid in selecting the content, complexity, intensity and volume as well as
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the most appropriate environment for which a treatment should be administered.
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Study Limitations
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This study had several limitations. First, the sample was small and all participants were
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traumatic chronic cervical iSCI, functioning at a relatively high level post-rehabilitation
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with partial ambulatory abilities. Thus, the homogeneity regarding the similarity of the
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injury makes generalization of our findings to a range of other spinal cord injuries at
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different points in recovery difficult. Second, the changes in length of training periods
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(i.e. 12-15 weeks) may have influenced the dose-response relationship and therefore
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the magnitude of change experienced across participants. Third, changes in gait
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characteristics were not assessed directly, circumventing more definitive determination
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of whether the changes in walking economy were the result of improved
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cardiorespiratory fitness or enhanced gait quality or perhaps both. Fourth, because
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walking economy was assessed on a treadmill we were unable to determine if changes
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in walking economy translated to overground walking. Last, the lack of a comparison
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group does not allow for direct comparison to other locomotor intervention treatments
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and determination of its superiority, equivalence, or inferiority to other locomotor
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approaches.
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354 Conclusion
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In summary, these data suggest that the OLT program used in this pilot study is feasible
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and improved both overground walking speed and walking economy in a small sample
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of people with chronic cervical iSCI. Future studies are necessary to establish the
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efficacy of this OLT program as well as to differentiate among potential mechanisms
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contributing to enhanced walking performance in people with iSCI following OLT.
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References
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1.
Waters RL, Yakura JS, Adkins RH. Gait performance after spinal cord injury. Clin Orthop. 1993;(288):87-96.
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Bassett DR, Howley ET. Limiting factors for maximum oxygen uptake and determinants of endurance performance. Med Sci Sports Exerc. 2000;32(1):70-84.
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3.
Ranganathan R, Newell KM. Changing up the routine: intervention-induced variability in motor learning. Exerc Sport Sci Rev. 2013;41(1):64-70. doi:10.1097/JES.0b013e318259beb5.
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Lay BS, Sparrow WA, Hughes KM, O’Dwyer NJ. Practice effects on coordination and control, metabolic energy expenditure, and muscle activation. Hum Mov Sci. 2002;21(5-6):807-830.
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Sparrow WA, Newell KM. Metabolic energy expenditure and the regulation of movement economy. Psychon Bull Rev. 1998;5(2):173–196.
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Dobkin B, Apple D, Barbeau H, et al. Weight-supported treadmill vs over-ground training for walking after acute incomplete SCI. Neurology. 2006;66(4):484-493. doi:10.1212/01.wnl.0000202600.72018.39.
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7.
Musselman KE, Fouad K, Misiaszek JE, Yang JF. Training of Walking Skills Overground and on the Treadmill: Case Series on Individuals With Incomplete Spinal Cord Injury. Phys Ther. 2009;89(6):601-611. doi:10.2522/ptj.20080257.
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8.
Alexeeva N, Sames C, Jacobs PL, et al. Comparison of training methods to improve walking in persons with chronic spinal cord injury: a randomized clinical trial. J Spinal Cord Med. 2011;34(4):362-379. doi:10.1179/2045772311Y.0000000018.
389 390 391
9.
Field-Fote EC, Roach KE. Influence of a locomotor training approach on walking speed and distance in people with chronic spinal cord injury: a randomized clinical trial. Phys Ther. 2011;91(1):48-60. doi:10.2522/ptj.20090359.
392 393 394 395
10. Sharp KG, Gramer R, Butler L, Cramer SC, Hade E, Page SJ. Effect of Overground Training Augmented by Mental Practice on Gait Velocity in Chronic, Incomplete Spinal Cord Injury. Arch Phys Med Rehabil. 2014;95(4):615-621. doi:10.1016/j.apmr.2013.11.016.
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11. Morawietz C, Moffat F. Effects of Locomotor Training After Incomplete Spinal Cord Injury: A Systematic Review. Arch Phys Med Rehabil. 2013;94(11):2297-2308. doi:10.1016/j.apmr.2013.06.023.
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12. Morawietz C, Moffat F. Effects of Locomotor Training after Incomplete Spinal Cord Injury: A Systematic Review. Arch Phys Med Rehabil. 2013;94(11):2297-2308. doi:10.1016/j.apmr.2013.06.023.
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13. Behrman AL, Harkema SJ. Physical rehabilitation as an agent for recovery after spinal cord injury. Phys Med Rehabil Clin N Am. 2007;18(2):183-202, v. doi:10.1016/j.pmr.2007.02.002.
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14. Carr JH, Shepherd RB. Movement Science: Foundations for Physical Therapy in Rehabilitation. 2nd edition. Gaithersburg, MD: Pro-Ed; 2000.
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15. Davids KW, Button C, Bennett SJ. Dynamics of Skill Acquisition : A Constraints-Led Approach. Champaign, Illinois: Human Kinetics; 2008. http://www.humankinetics.com/products/showproduct.cfm?isbn=9780736036863. Accessed November 14, 2015.
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16. Brooks GA. Exercise Physiology: Human Bioenergetics and Its Applications. 4th ed. Boston: McGraw-Hill; 2005.
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17. Biering-Sørensen F, Alai S, Anderson K, et al. Common data elements for spinal cord injury clinical research: a National Institute for Neurological Disorders and Stroke project. Spinal Cord. 2015;53(4):265-277. doi:10.1038/sc.2014.246.
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18. Musselman KE. Clinical significance testing in rehabilitation research: what, why, and how? Phys Ther Rev. 2007;12(4):287-296. doi:10.1179/108331907X223128.
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19. Shumway-Cook A, Woolacott MH. Motor Control: Translating Research into Clinical Practice. 4th edition. Philadelphia: LWW; 2011.
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20. World Health Organization. International Classification of Functioning, Disability and Health. 1 edition. Geneva: World Health Organization; 2001.
422 423
21. Waters RL, Lunsford BR. Energy cost of paraplegic locomotion. J Bone Joint Surg Am. 1985;67(8):1245-1250.
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22. Hedel HJA van. Gait Speed in Relation to Categories of Functional Ambulation After Spinal Cord Injury. Neurorehabil Neural Repair. 2009;23(4):343-350. doi:10.1177/1545968308324224.
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23. Shah PK, Gerasimenko Y, Shyu A, et al. Variability in step training enhances locomotor recovery after a spinal cord injury: Limits to task-specific training. Eur J Neurosci. 2012;36(1):2054-2062. doi:10.1111/j.1460-9568.2012.08106.x.
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24. Cavanagh PR, Kram R. The efficiency of human movement--a statement of the problem. Med Sci Sports Exerc. 1985;17(3):304-308.
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25. Waters RL, Mulroy S. The energy expenditure of normal and pathologic gait. Gait Posture. 1999;9(3):207-231.
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26. Kressler J, Nash MS, Burns PA, Field-Fote EC. Metabolic responses to 4 different body weight-supported locomotor training approaches in persons with incomplete
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spinal cord injury. Arch Phys Med Rehabil. 2013;94(8):1436-1442. doi:10.1016/j.apmr.2013.02.018. 27. Schmidt R, Lee T. Motor Control and Learning: A Behavioral Emphasis. 5th edition. Champaign, IL: Human Kinetics; 2011.
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Suppliers a. APDM Wearable Technologies, The OPAL, (Portland, OR)
c. The Mathworks, MATLAB (Natick, MA) d. Trackmaster, TMX22 (Newton, KS)
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f. IBM Inc, SPSS version 19 (Armonk NY).
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Figure Legend
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1. Figure 1: Changes in group mean overground walking speed following OLT in people with chronic cervical motor-incomplete SCI. Bars represent mean walking
459
speed as assessed during the 10 meter walk test. Error bars represent standard
460
deviations. Significance was set at p≤0.05.
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2. Figure 2: Mean improvements in overground walking speed for each participant
following OLT in people with chronic cervical motor-incomplete SCI. Bars represent
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mean change in walking speed as assessed during the 10 meter walk test.
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Table 1: Participant Characteristics (N=6).
Gender
19 to 67 5 1
Etiology of injury Fall Motor vehicle accident Diving Other
1 1 3 1
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Time since injury, years (range) AIS Classification C D
2 to 5
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Level of injury Cervical 6 Mobility aids used for walking Walker 2 Crutches (bilateral axillary) 3 None 1
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Primary mode of community locomotion Wheelchair 4 Walker 2
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Male Female
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Table 2: Description of an example 12-week OLT program.
Movement Emphasis
Movement Pattern
1
Uniplanar
Stance Phase
2
Multiplanar
Lateral Stepping
3
Uniplanar
4
Multiplanar
5
Uniplanar
6
Multiplanar
7
Uniplanar
8
Multiplanar
9 10 11 12 Phase II
Cross-Over Stepping Stance Phase
Backwards Stepping Swing Phase
Rotational Stepping
Uniplanar
Stance Phase
Multiplanar
Lateral Stepping
Uniplanar
Swing Phase
Multiplanar
Cross-Over Stepping
Uniplanar
Stance Phase Backwards Stepping
15
Uniplanar
Swing Phase
16
Multiplanar
Rotational Stepping
17
Uniplanar
Stance Phase
18
Multiplanar
Lateral Stepping
19
Uniplanar
Swing Phase
20
Multiplanar
Cross-Over Stepping
21
Uniplanar
Stance Phase
22
Multiplanar
Backwards Stepping
23
Uniplanar
Swing Phase
24
Multiplanar
Rotational Stepping
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Swing Phase
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Phase III
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Table 3: OLT intra-session segmental breakdown.
Joint Mobility
Volitional Neuromuscular Activation
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Task-Isolation
Emphasis Exercises focus on improving joint mobility and muscle flexibility. Exercises focus on enhancing neuromuscular function pertaining to areas of the abdominal, thoracic and lumbar, and pelvic regions. Exercises which are sub-components of the activity of interest which are performed in isolation. Exercises which incorporate the motor patterns practiced during task-isolation into larger more complex movements. Practicing the activity in its entirety.
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Task-Integration
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Table 4: Effect of OLT on cardiorespiratory outcomes. Post-test
P-value
Effect Size (d)
VO2 (ml·kg·min)
6.6 (1.3)
5.7 (1.4)
0.038*
0.67
VCO2 (ml·min)
753.1 (125.5)
670.7 (120.3)
0.036*
0.67
HR (bpm) RER Estimated VO2 (ml·kg·min)
104 (15) 0.87 (0.05) 1.9 (0.78)
98 (14) 0.82 (0.04)
0.135 0.147
0.41 1.1
CWR Walking Speed (mph)
0.9 (0.5)
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Abbreviations: VO2, steady state oxygen consumption; VCO2, carbon dioxide
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Appendix A – Example Uniplanar OLT Session Plan. Exercise
Sets
Repetitions
Joint Mobility
Passive Hamstring Stretch
1
3 x 30 seconds
Supine Active Hip Mobility
1
5 each leg/each direction
Standing Trunk Rotations
1
10 each direction
Standing Trunk Circles
1
10 each direction
1
10
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Task-Integration
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Task-Isolation
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Standing Body Weight Squats Walking (Lofstrand Supported) Weight-Shift (Lofstrand Supported) Even Stance Anterior/Posterior Weight-Shift (Lofstrand Supported) Staggered Stance Anterior/Posterior Weight-Shift (Unsupported) Staggered Stance Anterior/Posterior Small Stepping (Lofstrand Supported) Small Stepping (Lofstrand Supported) Initial & MidSwing Emphasis Small Stepping with Pause (Unsupported) Small Stepping with pause (Unsupported) Walking Forward for 10 meters (Lofstrand Supported)
20 repetitions 20 repetitions 20 repetitions 10 repetitions
2 x 10 meters
10 each direction
60 repetitions
3
10 x 3 sec. holds each direction
60 repetitions
3
10 each direction
60 repetitions
3
10 each direction
60 repetitions
3
10 each direction
60 repetitions
3
5 steps each direction
3
10 each direction
3
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Volume
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30 repetitions 60 repetitions
Perform for the remainder of the session
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Appendix B – Example Multiplanar OLT Session Plan. Exercise
Sets
Joint Mobility
Passive Hamstring Stretch
1
Supine Active Hip Mobility
1
Standing Trunk Rotations
1
10 each direction
Standing Trunk Circles
1
10 each direction
1
10
Weight-Shift (Unsupported)
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Activity Rehearsal
20 repetitions 20 repetitions 20 repetitions 10 repetitions
2 x 10 meters
3
10 each direction
60 repetitions
3
10 x 3 sec. holds each direction
60 repetitions
3
10 each direction
60 repetitions 60 repetitions
Lateral Stepping (Lofstrand 3 10 each direction Supported) Lateral Stepping with Trailing Leg Push-Off 60 3 10 each direction Emphasis (Lofstrand repetitions Supported) Lateral Stepping with 5 steps each 30 3 Pause (Unsupported) direction repetitions Lateral Stepping with 60 3 10 each direction pause (Unsupported) repetitions Lateral Stepping to Walking Forward for 10 meters Perform for the remainder of the session (Lofstrand Supported)
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Task-Integration
Volume
1
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Standing Body Weight Squats Walking (Lofstrand Supported) Weight-Shift (Lofstrand Supported) Even Stance Medial/Lateral Weight-Shift (Lofstrand Supported) Even Stance Medial/Lateral with Single Leg Balance
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Volitional Neuromuscular Activation
Repetitions 3 x 30 seconds each leg 5 each leg/each direction
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