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Balance training improves static stability and gait in chronic incomplete spinal cord injury subjects: a pilot study

BACKGROUND: Walking is considered the most important goal after an incomplete spinal cord injury (SCI). Only recently it has been demonstrated that balance is a key factor of walking recovery, but no data on the efficacy of balance training in
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   Vol. 49 - No. 3 EUROPEAN JOURNAL OF PHYSICAL AND REHABILITATION MEDICINE 353 Balance training improves static stability and gait in chronic incomplete spinal cord injury subjects: a pilot study  strated by clinical and instrumental evaluation; the improvement was maintained at follow-up examina- tions. Further, in the EXP group, the enhancement in balance that existed at T1 preceded the improve-ment in gait, and significant correlations between the improvements in gait and balance were observed. In comparison with H data, vBFB treatment demonstrat-ed a significant higher level of effectiveness than con- ventional Rehab. Conclusion.  vBFB training is effective in improving  balance and gait in chronic SCI subjects. Clinical Rehabilitation Impact. Inclusion of vBFB in rehabilitation protocols for chronic SCI subjects ef-fects greater improvements in gait than conventional rehabilitation alone. K  EY     WORDS : Spinal cord injuries - Biofeedback, phsycology - Postural balance - Gait. E pidemiological studies have shown that approxi-mately 50% of patients with traumatic spinal cord damage suffer an incomplete lesion ( e.g  ., with sensory and motor preservation below the level of the lesion). 1  Depending on the severity of the lesion, most patients have the potential to recover walking function. 2  Further, walking recovery is one of the principal goals after a spinal cord injury (SCI) and is considered the most important objective by patients  with incomplete lesions. 3  Thus, recovery of ambu-lation is the target of several pharmacological and rehabilitative approaches. 4-6 Spinal Cord Unit, IRCCS Santa Lucia Foundation  Rome, Italy  EUR J PHYS REHABIL MED 2013;49:353-64 F. TAMBURELLA, G. SCIVOLETTO, M. MOLINARI  Background.  Walking is considered the most impor- tant goal after an incomplete spinal cord injury (SCI). Only recently it has been demonstrated that balance is a key factor of walking recovery, but no data on  the efficacy of balance training in supporting walking function in SCI subjects are available.  Aim.  The object of the study was to determine the efficacy of visual biofeedback task-specific balance  training (vBFB) in improving balance performance and gait in SCI subjects compared with conventional over-ground rehabilitation (Rehab).  Design. Open-case study with retrospective matched control. Setting. Chronic SCI outpatients and healthy subjects (H).  Population.  Twelve SCI subjects with ASIA impair-ment scale grade D-6 in the vBFB group (EXP) and 6 in the Rehab group (CTRL)-and 6 H.  Methods.  Data from H were used as reference for phys-iological balance and gait parameters. CTRL and EXP groups underwent 8 weeks of rehabilitation 5 times/  week (CTRL group: 60 minutes devoted to Rehab; EXP group: 40 minutes of Rehab plus 20 of vBFB). At base-line (T0), every 10 vBFB sessions (T1-T2-T3), at the end of training (T4) and 1 and 2 months after vBFB  was halted, data on the following parameters were collected and compared between groups and training steps: Berg Balance Scale, Walking Index for Spinal Cord Injury, 6-minute walking, 10-meter walk and  timed up and go tests, balance performance (assessed  with a stabilometric platform), and kinematic spatio- temporal gait parameters (collected using a 2-dimen-sional motion analysis system).  Results.  At T4, only the EXP group experienced a significant improvement in balance and gait demon- Corresponding author:F. Tamburella, Spinal Cord Unit - IRCCS S. Lucia Foundation, via Ardeatina 306, 00179 Rome, Italy. E-mail:  TAMBURELLA BALANCE TRAINING 354  EUROPEAN JOURNAL OF PHYSICAL AND REHABILITATION MEDICINE June 2013  Age and lower extremity muscle strength are con-sidered the chief factors that affect walking function in SCI patients, 7  and most rehabilitation approaches aim to reinforce the lower extremities. However, evi-dence from other pathologies indicates that balance is a significant factor for walking recovery. 8, 9 In SCI patients there are only few reports address-ing balance issue, and suggesting its importance in determining gait performance. 10-12  Re-education of balance function in SCI patients by task-specific ori-ented training 13  has been examined, focusing on sit-ting balance recovery 13-15  and standing balance. 16, 17 There are no data on the efficacy of task-specific biofeedback balance training in supporting walk-ing functions in chronic motor incomplete SCI pa-tients. Thus, the object of this open-case study with a prospective control was to determine the efficacy of visual biofeedback task-specific standing balance (vBFB) training in improving balance performance and gait in subjects with chronic motor incomplete SCI compared with conventional over-ground reha-bilitation. Materials and methods Study design Six consecutive SCI subjects who were referred to the FSL spinal cord unit as outpatients between  January 2009 and April 2010 and met inclusion cri-teria reported below were enrolled into the study as the experimental group (EXP). Subsequently, bal-ance and gait data for 6 SCI patients with matching epidemiological, clinical, and neurological features, satisfying the same inclusion criteria, were extracted from our database, 10  constituting the control group (CTRL). Balance and walking features were also col-lected from 6 healthy subjects who were compara-ble with regard to gender, height, weight, and age-constituting the healthy group (HEALTHY).The demographics and clinical features of the HEALTHY, CTRL, and EXP subjects are reported in Table I.  Population The inclusion criteria comprised chronic SCI (at least 12 months post-injury), level D on the ASIA Im-pairment Scale, 18  the ability to maintain a standing position unsupported for at least 1 minute, and the ability to walk at least 10 meters. 19  During the study, subjects did not participate in other rehabilitation or research interventions that might have influenced the outcome of this study.The local Ethics Committee approved this study, and all subjects gave informed consent to participate (Prot. CE/AG.4-PROG.231-65).  Intervention: CTRL and EXP group training  Fort CTRL and EXP patients, the rehabilitation program comprised an 8-week regimen, 5 times per  week for 60 minutes each day. For the CTRL group, all 60 minutes were devoted to over-ground conven-tional rehabilitation, including balance and walking training, per Alexeeva et al  . 12  and Harkema. 6  Reha-bilitation training followed that proposed by Harke-ma et al  . 6  aimed to maximize weight bearing on the legs, optimize sensory cues appropriate to improve balance and gait, optimize posture and kinematics, maximize recovery and minimize compensation. EXP participants underwent 40 minutes of the same rehab protocol as for CTRL patients, followed by 20 minutes of specific vBFB training.In the vBFB training, patients stood on the force plate with a monitor at eye level approximately at 1.5 m away. For safety reasons force plate was placed between parallel bars, but patients were in-structed to maintain standing position unsupported during vBFB training. The center of pressure (COP) position signal was used as visual biofeedback in real-time mode during the exercises. vBFB training addressed the 3 primary aspects of balance recov-ery for stroke patients per Nichols: 20  steadiness (the ability to maintain a given posture with minimal ex-traneous movements), symmetry (equal weight dis-tribution between the weight-bearing components), and dynamic stability (the ability to move within a given posture without losing balance). For all SCI subjects, the exercises in the vBFB protocol were the same. After familiarization, balance training was based on five different exercises of increasing dif-ficulties:1. in “steadiness exercise” subjects had to keep the COP position signal in the center of a target mini-mizing external movements;2. in “symmetry exercise” subjects were asked to reach a physiological weight distribution, 50% for each side, 40% on the forefoot and 60% on rearfoot,  BALANCE TRAINING TAMBURELLA Vol. 49 - No. 3 EUROPEAN JOURNAL OF PHYSICAL AND REHABILITATION MEDICINE 355 Set up and evaluation of outcomes   At baseline (T0) and at the end of the training ses-sion (T4) and every 10 vBFB sessions (T1, T2, T3), EXP subjects underwent a battery of clinical and instrumental evaluations. Follow-up examinations  were performed one month (C1) and two months (C2) after the end of the training. From our data-base, we extracted clinical and instrumental balance and gait data for CRTL subjects at baseline (T0) and after 8 weeks of conventional rehab (T4). HEALTHY subjects underwent the same clinical/instrumental assessment once, and their data were used as a ref-erence of physiological balance and gait parameters. For all groups, the balance and gait evaluations were performed in the following order: instrumental bal-ance and gait examinations and clinical assessments using scales and time tests.Neurological status was assessed using the Ameri-can Spinal Injury Association (ASIA) and ASIA Im-pairment Scale (AIS), 18  and balance impairments  were evaluated using the Berg balance scale (BBS). 21  To examine walking level and performance, we used and execute postural and reaching tasks: eyes clos-ing/opening and object reaching;3. in “target exercise” subjects had to keep COP in the center of a target, at an equal distance between feet, without losing the correct weight distribution;4. in “hunting exercise – random targets” subjects had to move COP indicator within the boundaries of a target appearing on the screen in random loca-tions by shifting weight along the anteroposterior or mediolateral axes;5. in “hunting exercise – planned targets” subjects  were asked to move COP indicator toward four tar-gets in clockwise and anticlockwise directions.Each session lasted 20 minutes for a total of 8 rounds. Every 8 minutes a sitting pause of 2 min-utes was allowed. Each round lasted a maximum of 2 minutes. If the subject declared fatigue, rest  was allowed and training resumed afterwards. For each exercise, 3 consecutive rounds were pro-posed. Only when 3 consecutive rounds of an exer-cise were performed successfully unsupported and  without rest, the following more complex exercise  was proposed. T  ABLE  I.— Clinical features of HEALTHY, CTRL, and EXP SCI subjects (all patients are ASIA level D, according to the inclusion crite-ria of the study). SCI: incomplete spinal cord injury; HEALTHY: healthy subjects; EXP: experimental SCI patients; CTRL: control SCI  patients; M: male; F: Female; NT: non-traumatic SCI lesion; T: traumatic SCI lesion.  Age (years)SexHeight (cm)Weight (kg)EtiologyLesion levelDuration of injury (months) HEALTHY150M17587HEALTHY239F17661HEALTHY356F17564HEALTHY461F16865HEALTHY537M16659HEALTHY659M16773 HEALTHY (mean±SD)   50.33±10.26   3 M-3 F   170.67±4.13   68.17±10.40  CTRL154M16968NTT 1226CTRL236F17758NTT 924CTRL361F15860NTL 549CTRL463F15980NTT 723CTRL539M17586TL 329CTRL668M16774NTT 514 CTRL (mean±SD)   53.50±13.21   3 M-3 F   167.50±7.89   71.00±11.08  EXP152M16968NTT 1229EXP237F17660NTT 924EXP354F16870NTL 551EXP466F17266NTL 428EXP540M17788NTL 326EXP663M16078TT 527 EXP (mean±SD)   52.00±11.74   3 M-3 F   170.33±6.21   71.67±9.91    TAMBURELLA BALANCE TRAINING 356  EUROPEAN JOURNAL OF PHYSICAL AND REHABILITATION MEDICINE June 2013 ble-time support phase (DTS: mean of right and left stride) expressed as the percentage of gait cycle. In this study, we defined STRIDE as the event between 2 successive instances of foot-ground contact, ST as the event from foot-ground contact to liftoff, and DTS as the time for which both feet were in contact  with the ground. 27  Foot-ground contact and liftoff  were assessed using KineView. Statistical analysis  No participant withdrew from the trial, and all outcome measures were obtained for all SCI and HEALTHY subjects. For each subject, the mean val-ues of stabilometric parameters were calculated by averaging three trials for each visual condition (OE-CE). Gait variables were averaged from the kine-matic data of the three trials. Descriptive statistics  were performed for all variables. Before statistical comparisons were made, Kolmogorov-Smirnov test  was performed to evaluate distribution of the data.One-way analysis of variance (ANOVA) was per-formed to compare balance and gait data between groups (with HEALTHY, EXP, and CTRL as inde-pendent variables) at T0 and T4. When the ANOVA results were significant, Bonferroni  post hoc  test was performed. K independent sample was applied at T0 and T4 to assess intergroup differences for non-parametric scale scores (BBS-WISCI).Paired t  -test was used to compare the effects of re-hab approaches, evaluated as T4- vs  .-T0 data, for the CTRL and EXP groups. For BBS and WISCI, we used  Wilcoxon test. For each balance and gait parameter, the percentage of improvement between T4 and T0 data was calculated. To compare the percentages of improvement after training between the CTRL and EXP groups, independent t  -test was used. For BBS and WISCI, as nonparametric measures, group data  were compared by Mann-Whitney U test.To identify improvements during rehabilitation, the effectiveness 28  of each balance and gait pa-rameter was calculated for both SCI groups per the following formula, using healthy data as reference scores, reflecting highest level of performance:[(SCI data T4 – SCI data T0)/ (medium HEALTHY data – SCI data T0)]* 100.Differences in efficacy between the CTRL and EXP groups were analyzed by independent t  -test or Mann-Whitney U test when appropriate.the walking index for spinal cord injury (WISCI), 22  10-meter walk test (TMWT), 23  6-minute walking test (SMWT), 24  and the timed up-and-go test (TUG). 25 Balance and vBFB training were evaluated using a 320 cm x 75 cm static force platform (BPM 120 - Physical Gait Software Vv. 2.66, Rome, Italy). During the assessment of static stability patients stood bare-foot in a natural and relaxed position, arms at their sides, with the heels lined up and apart at a com-fortable distance, fixed throughout the sessions, and forefoot open to 30 degrees with eyes open (OE) facing a target 1.5 m away and eyes closed (CE). To calculate the mean values of each stabilometric COP parameter, 3 trials were performed for each condi-tion, each lasting 51.2 s, according to platform speci-fications. The following parameters were examined:  — length indicators: COP sway path (SP), the distance covered by the moving instantaneous COP as a vertical projection on the ground (mm), COP mean velocity (VEL), anteroposterior (V   AP ) and me-diolateral (V  ML ) components of COP mean velocity (mm/s);  — surface indicators: COP sway area (SA), 90% confidence ellipse of the dispersion of COP posi-tions (cm 2 ), mean COP position referred to the cent-er of confidence ellipse, in along the antero-poste-rior (COP  AP ) and medio-lateral axis (COP ML ) (cm).Locomotion variables were recorded and analyzed by using the KineView Motion System® (Kineview, Hafnarfjordur, Iceland). In the experimental setup,  we performed a bidimensional gait analysis of 3 strides on the sagittal plane. All subjects were in-structed to walk OE at a comfortable, self-selected  velocity, 3  walking 2 m ahead of the mat and continu-ing 2 m past the end. Before data were collected, subjects performed the walking trials to familiarize themselves with the procedure.Kinematic data were recorded at 50 frames/s with a digital camera (Cyber-Shot DSC P73, Sony, Tokyo,  Japan). Spatial movements of the lower extremity segments were determined, based on the position of passive markers that were placed per the Helen Hayes biomechanical model. 26  Kinematic data were reconstructed offline using Matlab (Mathworks, Inc.,  version 7.1, Natick, MA, USA) after digitalization of the markers with the KineView Motion System.The following kinematic data were considered: speed (m/s); cadence (N. step/min); stride length (STRIDE: mean of right and left stride in m); stance phase (ST: mean of right and left stride); and dou-  BALANCE TRAINING TAMBURELLA Vol. 49 - No. 3 EUROPEAN JOURNAL OF PHYSICAL AND REHABILITATION MEDICINE 357 tistical analysis was performed using SPSS for Win-dows (version 9.0, Chicago, IL, USA). Results vBFB training selectively improves balance and gait  performance   As expected by the matching criteria that we adopted, CTRL and EXP subjects had comparable clinical and instrumental balance and gait perform-ance at the beginning of the training ( CTRL vs. EXP   at T0 – Table II). The eight-week treatment (T4 vs  . T0) had a positive effect on the EXP and CTRL groups — but significant only in EXP patients. In the EXP group, the treatment effect was significant for all indices, except for the 10MWT and DTS ( CTRL T4 vs. T0   and  EXP T4 vs. T0   – Table II). The CTRL-EXP One-way repeated measures ANOVA was used to compare performance at T0 versus at the vBFB train-ing steps (T1, T2, T3, T4, C1, C2) in EXP patients, followed by  post hoc  comparison by Bonferroni test.Overall comparisons of balance and gait improve-ment were made at each training time point (T n ) by averaging the percentage of improvement in each index across all balance or gait indices per the fol-lowing formula:Percentage of improvement = (index value at T n  / index value at T0) * 100.Pearson R and Spearman rho correlation coeffi-cients for continuous and ordinal variables, respec-tively, were calculated to quantify the relationship between the improvement in each balance index and walking index in EXP and CTRL subjects, calcu-lated as the difference between T4 and T0 (Δ).For all tests, the significance was set at 0.05. Sta- T  ABLE  II.—  Data±SD of balance and gait clinical and instrumental evaluations for HEALTHY subjects, as physiological references, and EXP and CTRL subjects at baseline (T0) and after 8 weeks of treatment (T4). Statistical values are reported as bold-faced numbers for CTRL vs. EXP comparison at T4, and for T4 vs. T0 comparison for EXP group. CTRL vs. EXP comparison at T0 and T4 vs. T0 comparison for CTRL group were not significant for all balance and gait parameters analyzed. (*: P<0.05, **:P<0.005, ***:P<0.001) n.s.: non-significant data. BALANCEHEALTHY CTRLEXPCTRLEXPCTRL vs. EXPT4 vs. T0T0T0T4T4T4EXP BBS5631±8.9726.00±10.6933.00±8.9041.00±7.8ns 0.028  SP OE92.00±23.20342.17±131.79488.48±283.68299.43±108.19234.56±136.07ns 0.0001  SP CE98.87±34.64649.19±238.89863.11±299.07640.65±164.9509.53±357.94ns 0.007   VEL OE1.83±0.507.24±3.119.54±5.547.12±4.614.58±2.66 0.05   0.00001   VEL CE1.98±0.6514.11±3.3316.86±5.8413.84±4.949.95±6.99ns 0.007   V   AP  OE1.06±0.355.02±2.515.74±3.454.64±3.683.05±2. 20ns 0.0000001   V   AP  CE1.43±0.4310.08±2.7011.94±5.089.62±3.637.22± 5.70ns 0.039   V  ML  OE1.25±0.334.20±1.626.45±3.874.16±2.402.81±1.25 0.041   0.000001   V  ML  CE1.34±0.448.08±2.089.66±2.988.11±3.445.57±3.48 0.035   0.000006  SA OE0.75±0.798.00± 11.438.61±7.305.51± 4.792.21±1.94 0.033   0.002  SA CE0.47±0.4616.96± 9.0727.01±13.2014.50± 9.579.65±10.83 0.020   0.015  COP  AP  OE0.83±0.502.74±1.612.75±1.232.72±0.961.51±0.74 0.011   0.002  COP  AP  CE0.68±0.334.76±1.725.10±1.714.90± 2.572.86±1.82 0.010   0.035  COP ML  OE0.45±0.161.91±0.872.45±1.171.91±1.091.15±0.65 0.16   0.0001  COP ML  CE0.45±0.163.42±1.424.30±1.383.13±1.82.21±1.37ns 0.0003  GAIT WISCI2012.67±0.8214.17±1.8312.67±0.8217.15±1.64 0.020   0.024  10MWT12.00± 1.1628.79±15.8021.02± 9.5327.04±12.3219.31±9.18nsns6MWT167.33± 20.19178.28±78.09193.18±68.08177.35±75.45259.64±82.84ns 0.017  TUG12.67± 1.3542.18±36.0621.70± 10.738.18±31.2615. 22±6.14ns 0.025  SPEED0.84±0.160.36±0.170.37±0.140.36±0.190.46± 0.15 0.015   0.0003  CADENCE83.99±10.3755.09±21.6056.10±12.1254.99±23.0965.47±16.77ns 0.001  STRIDE1.19±0.150.72±0.140.78±0.170.73±0.140.85±0.13 0.010   0.0001  ST64.03±1.8978.11±7.1473.75±5.2376.48± 6.8471.49±4.22ns 0.018  DTS13.92±2.2124.57±6.3425.16±5.6524.55± 6.3423.77±5.77nsns
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