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Feasibility of sensory tongue stimulation combined with task-specific therapy in people with spinal cord… Chisholm, Amanda E; Malik, Raza N; Blouin, Jean-Sébastien; Borisoff, Jaimie; Forwell, Susan; Lam, Tania Jun 6, 2014

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METHODOLOGY Open AccessFeasibility of sensory tongue stimulation combinedwith task-specific therapy in people with spinalcord injury: a case studyAmanda E Chisholm1,3*, Raza Naseem Malik1,3, Jean-Sébastien Blouin1, Jaimie Borisoff3,4, Susan Forwell2,3and Tania Lam1,3AbstractBackground: Previous evidence suggests the effects of task-specific therapy can be further enhanced when sensorystimulation is combined with motor practice. Sensory tongue stimulation is thought to facilitate activation of regions inthe brain that are important for balance and gait. Improvements in balance and gait have significant implications forfunctional mobility for people with incomplete spinal cord injury (iSCI). The aim of this case study was to evaluate thefeasibility of a lab- and home-based program combining sensory tongue stimulation with balance and gait training onfunctional outcomes in people with iSCI.Methods: Two male participants (S1 and S2) with chronic motor iSCI completed 12 weeks of balance and gait training(3 lab and 2 home based sessions per week) combined with sensory tongue stimulation using the PortableNeuromodulation Stimulator (PoNS). Laboratory based training involved 20 minutes of standing balance with eyesclosed and 30 minutes of body-weight support treadmill walking. Home based sessions consisted of balancing witheyes open and walking with parallel bars or a walker for up to 20 minutes each. Subjects continued daily at-hometraining for an additional 12 weeks as follow-up.Results: Both subjects were able to complete a minimum of 83% of the training sessions. Standing balance with eyesclosed increased from 0.2 to 4.0 minutes and 0.0 to 0.2 minutes for S1 and S2, respectively. Balance confidence alsoimproved at follow-up after the home-based program. Over ground walking speed improved by 0.14 m/s for S1 and0.07 m/s for S2, and skilled walking function improved by 60% and 21% for S1 and S2, respectively.Conclusions: Sensory tongue stimulation combined with task-specific training may be a feasible method for improvingbalance and gait in people with iSCI. Our findings warrant further controlled studies to determine the added benefitsof sensory tongue stimulation to rehabilitation training.Keywords: Standing balance, Functional mobility, Rehabilitation, Robotic gait training, Sensory tongue stimulation,Spinal cord injury, Task-specific trainingIntroductionThere has been a great deal of interest on rehabilitationstrategies such as task-specific training and sensory stimu-lation for facilitating neuroplasticity and enhancing motorrecovery following neurological injury [1,2]. Task-specifictraining is built on the concept that motor output can beshaped and re-trained by relevant sensory cues, and in-volves a large number of repetitions based on motor learn-ing principles [3]. For example, therapies that providerepeated practice of standing balance have been shown tobe beneficial for people with incomplete spinal cord injury(iSCI [4,5]). As well, improved balance from task-specifictraining has resulted in better gait and functional inde-pendence for people with chronic stroke [6]. In peoplewith SCI, improvements in mobility and ambulatory func-tion are further associated with better health and socialoutcomes [7].* Correspondence: achisholm@icord.org1School of Kinesiology, University of British Columbia, Vancouver, Canada3International Collaboration on Repair Discoveries, Vancouver Coastal HealthResearch Institute, Vancouver, British Columbia, Canada V5Z 1M9Full list of author information is available at the end of the articleJ N E R JOURNAL OF NEUROENGINEERINGAND REHABILITATION© 2014 Chisholm et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the CreativeCommons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, andreproduction in any medium, provided the original work is properly credited.Chisholm et al. Journal of NeuroEngineering and Rehabilitation 2014, 11:96http://www.jneuroengrehab.com/content/11/1/96There is evidence that the effects of task-specific motortraining can be further enhanced by sensory stimulation, ashas been shown for gait disorders following stroke [8,9],hand function in people with stroke [10] or iSCI [11], anddysphagia following stroke [12]. Specifically in the SCI popu-lation, these effects include better upper extremity motorfunction and muscle strength [11]. One type of sensorystimulation is the administration of prolonged, tonic periph-eral nerve stimulation at intensities high enough to recruitsensory nerve fibers but low enough to avoid activation ofmotor fibers. Although the stimulus activates only sensory fi-bers, corticospinal excitability can also be enhanced [13-15],consistent with concepts about the role of sensory input onmotor output and learning throughout the central nervoussystem [16,17]. The somatosensory cortex may have an im-portant underlying role in cortical reorganization after injury.If sensory stimulation can enhance motor training out-comes, it might be possible that a higher volume of sen-sory input results in an additive effect [18]. For example,Conforto et al. showed that improvements in hand musclestrength were correlated with the intensity of somatosen-sory stimulation in individuals with stroke [19]. Enhancedstimulation volume could also be achieved by targetingdifferent regions of the body. Perhaps the most sensitivearea in humans is the tongue, which contains a high dens-ity of sensory receptors [20] with a large somatosensorycortical representation [21]. Somatosensory stimulation ofthe tongue can lead to changes in brainstem and cerebel-lum activation [22,23] in areas associated with the controlof balance and gait [24,25]. Indeed, recent studies havedemonstrated that sensory tongue stimulation can improvepostural control in patients with balance disorders [26] andwhen combined with motor training, can improve balanceand walking in patients with multiple sclerosis [27]. Sensorystimulation to peripheral nerves in other areas of the bodymay be difficult to regulate due to impaired sensation afteriSCI (e.g. poor sensory perception and altered supraspinalsensorimotor interactions), whereas the tongue is usuallynot affected. These considerations make the tongue an in-viting target for sensory stimulation in combination withtask-specific training for the SCI population.Thus, the primary purpose of this study was to test thefeasibility of combining sensory tongue stimulation withbalance and gait training on functional outcomes inpeople with iSCI. We present a case report of two individ-uals with motor-iSCI to show the feasibility as well as thepotential effectiveness of this combined training approachwith a lab-to-home based program on balance, functionalambulation, and quality of life in people with iSCI.Materials and methodsSubjectsTwo men with a motor-iSCI (American Spinal Injury Asso-ciation [28]; ASIA C) due to trauma participated in thisstudy after giving written consent. Subject 1 (S1) was 31-years old at 9.5-years post C5 level injury, while subject 2(S2) was 30-years old at 12 years post T5-6 level injury.The body-weight for S1 and S2 was 65 kg and 72 kg, re-spectively. Subjects were able to ambulate over groundfor at least 10 m unassisted with a wheeled walker andfoot lifter (on the more affected side). However, bothsubjects relied on a power wheelchair for their dailymobility. Subjects had adequate range of motion to walkwith the Lokomat robotic gait orthosis (Hocoma AG,Volketswil, Switzerland), and did not present with se-vere lower limb contractures or spasticity restrictingpassive range of motion. Neither of the subjects wereparticipating in any formal rehabilitation program at thetime of this study, and were free of other musculoskeletalor neurological conditions affecting mobility. All proce-dures were approved by the University of British Columbiaand Vancouver Coastal Health Research Institute ethicscommittees.PoNS stimulatorThe Portable Neuromodulation Stimulator (PoNS)™ is asmall electrode array (3 × 3 × 0.1 cm, and 100 g) that isheld in place on the tongue’s surface with light pressure tothe roof of the mouth (Figure 1). The stimulation consistsof 19-V pulses delivered at a rate of 200 Hz with everyfourth pulse removed [29]. The 143 electrodes are pulsedsequentially in groups of nine. Subjects were instructed toincrease stimulation to a moderate-high level (pulse widthadjustable from 0.4 to 60 μs) that was tolerable and notpainful.Training programSubjects completed 12 weeks of balance and gait training(3 laboratory and 2 home based sessions per week) com-bined with sensory tongue stimulation using the PoNS[30], followed by an additional 12 weeks of home basedtraining with the stimulator at 5 times per week (Figure 2).In the lab, balance training consisted of four bouts of 5-minute of standing practice with 1-minute rest breaks be-tween bouts. Subjects were instructed to focus on tryingto stand for as long as possible with their eyes closed. Sub-jects wore a body weight support (BWS) harness for safetyand to assist with upright standing. An easy BWS levelwas used as warm-up in the first bout; this was defined asthe minimum BWS to maintain an upright posture forwalking (e.g. no excessive knee flexion during stance ortoe dragging). BWS was lowered by 10 kg for the secondbout (difficult BWS level), and then raised by 5 kg (moder-ate BWS level) for the third and fourth bouts. Subjectswere instructed to close their eyes when balanced withtheir hands off the parallel bars. Instructors provided ver-bal feedback on their performance and recorded the dur-ation for which they could maintain their eyes closed withChisholm et al. Journal of NeuroEngineering and Rehabilitation 2014, 11:96 Page 2 of 9http://www.jneuroengrehab.com/content/11/1/96a stopwatch. Verbal feedback focused on different align-ment issues in the lower and upper body on alternatingdays (e.g. shift weight evenly over both legs, keep a slightbend at the knee, keep heels on the ground, keep shouldersaligned with hips, etc.). Balance training was progressed be-tween sessions by lowering BWS levels by 5 kg for eachbout when 4 minutes of eyes closed could be consistentlyachieved in a single bout, and progressing to more challen-ging foot positions (e.g. narrow and tandem stance) when0 kg BWS was achieved (Additional file 1).Gait training consisted of six bouts of 5-minutes ofwalking with the Lokomat robotic gait orthosis, with restbreaks provided as required. The goal was to increasespeed and decrease the amount of Lokomat guidanceforce on alternating sessions (e.g. if speed was increased,then force was held constant) for 30 minutes of continu-ous walking. BWS was set at the minimum level requiredto maintain an upright posture for walking (10 kg - S1 and15 kg - S2). Subject’s reported their rate of perceived exer-tion (RPE) on the Borg CR10 Scale at the end of each bout[31]. If the RPE was < 5, walking speed was increased orLokomat guidance force was decreased for the next boutby 0.1-0.2 km/h or 5-10%, respectively [32]. Gait trainingwas progressed by using the previous session’s speed orforce level reported with an RPE of 4 in the first bout forthe next session.For home-based sessions, subjects were instructed topractice balancing and walking for up to 20 minutes eachusing a walker at home or parallel bars at their local fitnessgym for safety. Specific instructions for balance practice in-cluded keep eyes open, use tongue stimulator, and remem-ber the verbal feedback tips provided during the laboratorysessions (see examples above). For walking practice, sub-jects were encouraged to limit rest breaks if possible and towalk at a moderate to fast pace. Subjects reported the dur-ation of balance and gait training, and number of stepstaken for gait training. An average and standard deviationwas calculated for these parameters to describe the quantityof all home-based training sessions.Outcome measuresStatic balance was assessed by recording the duration oftime the subject could stand on a flat surface with eyesopened and closed with the feet positioned hip width apart.We also used the Activities-Specific Balance Confidence(ABC) scale to evaluate balance self-efficacy. Subjects ratedtheir confidence in performing each activity (16 items) on ascale from 0 (no confidence) to 100% (complete confi-dence) without losing balance or becoming unsteady [33].Walking function was evaluated by the 10-meter walktest (10MWT), 6-minute walk test (6MWT), and the SpinalCord Injury-Functional Ambulation Profile (SCI-FAP). Forthe 10MWT, subjects walked along a 12-m walkway at thefastest speed they felt safe. Walking speed was calculatedusing the time required to traverse the middle 10 m, asmeasured by a stopwatch. For the 6MWT, subjects wereFigure 1 A picture of the Portable Neuromodulation Stimulator(PoNS)™ used by the subjects during training. The Up and Downbuttons adjust the pulse width parameter to increase and decreasethe stimulation intensity.Figure 2 A timeline of the training protocol and functional assessments. The weekly progress evaluation included the 10 meter walk test(10MWT) and standing balance with eyes closed (and eyes opened for S2).Chisholm et al. Journal of NeuroEngineering and Rehabilitation 2014, 11:96 Page 3 of 9http://www.jneuroengrehab.com/content/11/1/96asked to walk for 6 minutes at a self-selected speed aroundthe edge of a gymnasium (25 m × 16 m), taking rest breaksif required. The total distance covered over 6 minutes wasrecorded. Both measures are valid and have excellent test-retest reliability (r = 0.983 and 0.981, respectively) in peoplewith SCI [34,35].Subjects also performed the SCI-FAP, a timed test of 7walking tasks reflecting walking skills necessary foreveryday mobility (e.g. obstacle crossing, stairs) [36].The time required to complete each subtask is multi-plied by a factor corresponding to the assistive device orlevel of manual assistance needed. The 7 sub-scores arethen summed to provide a total score.The Life Satisfaction Questionnaire (LSQ) was used tomeasure various aspects of overall life satisfaction that in-cluded 9 items on a 6-point scale [37]. Quality of life wasassessed with the Impact on Participation and AutonomyQuestionnaire (IPAQ), Functional Independence Measure(FIM) Activities and Participation, and the Spinal Cord In-dependence Measure (SCIM). The IPAQ focuses on theability to participate in an activity and how their disabilityimpacts their ability to participate, with 39 questions in 5domains ranked from 0 (very good) to 4 (very poor) [38].The FIM measures the level of a patient's disability and in-dicates how much assistance is required for the individualto carry out activities of daily living based on 15 items withscores ranging from 13 (lowest) to 91 (highest). The SCIMwas developed specifically to evaluate self-care, respirationand sphincter management, and mobility for people withSCI, with a total score out of 100 [39].Evaluations of static balance, walking function, and qual-ity of life were conducted at 3 time points: pre-training(T0), after the initial 12-weeks of lab based training (T1),and follow-up (T2) after 12-weeks of home based training(Figure 2). We also assessed the duration of standing witheyes-closed (Additional file 1) and the 10 MWT everyweek to monitor progress throughout the training program.S2 was unable to stand with eyes-closed at the beginning ofthe study, so his duration of standing with eyes-open wasalso monitored weekly.ResultsWeekly progression tracked during lab- and home-basedtraining shows improved performance of balance witheyes closed and walking speed on the 10MWT (Figure 3).Laboratory-based training progressionSubjects completed 83% (S1) and 100% (S2) of the trainingsessions. S1 experienced a study-related skin abrasion dueto friction from the Lokomat cuffs during gait training.Manual treadmill-training was conducted for the following7 sessions to allow the injury to heal. For balance training,S1 started at 10 kg BWS (1st bout) and progressed to noBWS (all bouts) by the 20th in-lab session, and moredifficult stance positions by the 24th in-lab session. Duringthe 34th in-lab session, S2 progressed to trying no BWSfrom starting at 20 kg in the first session, and achieved2.5 min of standing balance with eyes closed on the lastsession at 0 kg BWS. During Lokomat training, averagetreadmill speed increased by 0.5 km/h for both subjects,while guidance force contribution decreased by 37% (S1)and 24% (S2) by the end of the 12-week in-lab program.Home-based training progressionSubjects completed 86% (S1) and 88% (S2) of the home-based sessions, and reported that it was easy to trainwith the tongue stimulator at home. The average quan-tity of training within a session was 21 ± 5 minutes ofbalance and 16 ± 10 minutes of walking (234 ± 72 steps)for S1, and 17 ± 5 minutes of balance and 17 ± 6 minutesof walking (368 ± 121 steps) for S2.Balance outcomesWeekly training outcomes for balance with eyes closed aredisplayed in Figure 3A. Standing balance with eye closedimproved in S1 from 10.5 s at T0 to 122.1 s at T1 and240.1 s at T2 (Table 1). S2 was unable to stand without sup-port and eyes open at T0 and T1, but he could stand un-supported with eyes open for 35.5 s and eyes closed for9.2 s by T2. ABC scores increased in both subjects from T1to T2 appointments indicating greater confidence (Table 1).Gait outcomes10MWT scores for weekly training outcomes are displayedin Figure 3B and performance on each task of the SCI-FAPis presented in Figure 4. 10MWT scores improved by0.08 m/s and 0.03 m/s from T0 to T1, and 0.06 m/s and0.04 m/s from T1 to T2 for S1 and S2, respectively(Table 1). Similarly, 6MWT scores improved by 30.1 m and15.7 m from T0 to T1, and 3.2 m and 13.6 m from T1 toT2 for S1 and S2, respectively (Table 1). Total score on theSCI-FAP test improved by 410 and 151 points from T0 toT2 for S1 and S2, respectively, indicating better skilledwalking function (Table 1). Figure 4 shows performance onthe SCI-FAP for each task.Quality of lifeFIM scores did not change from T0 to T1 (Table 1). SCIMscores increased from T0 to T2 by 12 points for S1, andby 1 point for S2 (Table 1). Slightly higher LSQ scoreswere reported at T2 compared to T0 for both subjects in-dicating greater satisfaction. IPAQ scores improved duringthe training from 61 at T0 to 42 at T1 and regressed up to70 at T2 for S1, while S2 regressed from 33 at T0 to 25 atT1 and improved to 20 by T2 (Table 1).Chisholm et al. Journal of NeuroEngineering and Rehabilitation 2014, 11:96 Page 4 of 9http://www.jneuroengrehab.com/content/11/1/96DiscussionThis case study demonstrates three important findings;1) the training program was feasible as subjects wereable to safely complete at least 83% of the training ses-sions, 2) sensory tongue stimulation combined withtask-specific training in persons with iSCI can improvebalance and functional ambulation, and 3) these im-provements were maintained for an additional 12 weekswith a home-based program. Also, subjects were able tomaintain the tongue stimulator in position during trainingwithout any difficulty. Our results provide preliminary evi-dence in support of combining these rehabilitation strat-egies to improve balance and walking function in personswith chronic iSCI.The results of this case study suggest that task-specifictraining with sensory tongue stimulation could improvebalance as well as over ground walking speed and distance.Although we lacked a control group, the magnitude ofsome of the functional changes we measured here are com-parable to the results of other studies in SCI. Standing bal-ance with and without visual input improved over thetraining program, which corresponded with an increase of7.8% for S1 and 9.8% for S2 on the ABC scale with 12 weeksof home-based training, indicating greater confidence to0501001502002503003500 4 8 12 16 20 24Time(s)WeekBalanceS1-EC S2 - EC S2 - EO0.00.10.20.30 4 8 12 16 20 24Speed(m/s)Week10MWTS1 S2A)B)Figure 3 Progression of A) balance and B) walking speed over the course of the laboratory-based (Weeks 0–12) and home-based(Weeks 12–24) training. Balance was timed with eyes closed (EC) for both subjects, and eyes open (EO) only for S2. There was missing data atweek 20 for S2 because balance with eyes closed was not attempted due to a headache and discomfort.Table 1 Summary of balance, gait and quality of lifeoutcome measuresS1 S2T0 T1 T2 T0 T1 T2BalanceEyes closed (s) 10.5 122.1 240.1 0 0 9.2Eyes open (s) 24.0 >600 >600 0 2.2 35.5ABC —— 15.0 22.8 —— 21.3 31.0Gait10 MWT (m/s) 0.10 0.18 0.24 0.18 0.21 0.256 MWT (m) 22.3 52.4 55.6 53.0 68.7 82.3SCI-FAP 684.3 294.7 274.1 723.2 595.4 572.2Quality of LifeFIM 85 85 86 86 86 86SCIM 66 77 78 81 81 82LSQ 35.5 29 37 45 46 48IPAQ 61 42 70 25 33 20Note: T0, pre-training; T1, post-training; T2, follow-up after home-basedtraining. The ABC scale was implemented at T1 because S2 was unable tostand supported with eyes open in the first 11 weeks of training. LowerSCI-FAP scores indicate better performance.Chisholm et al. Journal of NeuroEngineering and Rehabilitation 2014, 11:96 Page 5 of 9http://www.jneuroengrehab.com/content/11/1/96perform balance related activities. These changes are closeto the minimal detectable change level in response to ther-apy at 11.1% on the ABC scale reported for the Parkinson’sdisease population [40]. As we did not implement thismeasure until the end of the laboratory-based training pro-gram, it is possible that we could have captured greaterchanges in the ABC scale if it had been administered at T0.The improved performance on the 10 MWT in both sub-jects was also comparable to other studies reportingchanges of 0.04 to 0.16 m/s after treadmill or over groundgait training [32,41-43], as was the change on the 6 MWT[43]. Further, S1 met the minimal detectable change level of0.13 m/s for the 10 MWT [44]. Both subjects also exceededthe 92 points determined as 95% minimal detectablechange on the SCI-FAP after laboratory-based training [45].Our subjects continued to improve balance and walkingfunction with an additional 12-week home-based program.In other studies with sensory stimulation, retention offunctional gains over 1–2 months following the end oftraining has also been reported [8,46]. In a study by Field-Fote, participants who completed 12-weeks of manual-assisted body-weight support treadmill training (BWSTT)or functional electrical stimulation-assisted BWSTT main-tained their functional improvements (e.g. 0.07 m/s fastergait velocity) even 6 months after the end of training [32].However, in the same study, participants who trained withfull assistance (100% guidance force) from the Lokomat didnot retain improvements in gait speed [32]. In comparison,our subjects continued to show improvements (e.g. 0.04-0.06 m/s faster gait velocity) over 12 weeks with a home-based training program.In the SCI literature, clinical studies have focused on re-habilitation strategies for improving gait, while less atten-tion has been given to balance-specific training programsfor standing [4,5]. Previous studies have demonstrated thatpeople with iSCI can use sensory cues combined withFigure 4 The score for each task in the SCI-FAP test is plotted for each assessment (T0 - pre-training, T1 - post-training andT2 - follow-up). The score represents the time to complete the task multiplied by a factor representing the amount of assistance required. Lowerscores indicate improved functional ambulation. If the person cannot complete the task, the maximum score of 300 is assigned for that sub-task.Chisholm et al. Journal of NeuroEngineering and Rehabilitation 2014, 11:96 Page 6 of 9http://www.jneuroengrehab.com/content/11/1/96motor practice to improve standing balance [4,5]. Sayenkoet al. reported reduced fluctuations in the anterior-posterior and medial-lateral directions of the centre ofpressure during 1 minute of standing with eyes closed, in-dicating improved postural stability after visual biofeed-back training [5]. In comparison to these studies, oursubjects’ initial standing balance ability was more impairedat the onset of training, as they were unable to stand un-supported for over 1 minute with eyes open. Although wedid not measure centre of pressure, our findings reflectimproved postural stability as the duration of balancingwith eyes closed continued to increase throughout thetraining program. Results from the weekly progress evalu-ation of balance during the at-home phase of the programshows more variability in performance for S1, while asteady increase for S2. Examination of S1’s training logsdid not yield any insights into possible reasons for this in-creased variability. The results also highlight importantconcepts that influence balance and gait performance,such as confidence and fear of falling. Both subjects ini-tially scored low on the ABC scale indicating poor confi-dence in performing balance related activities withoutfalling, but the scores improved after training. Thisemphasizes the potential clinical implications of our task-specific training program for individuals with severe bal-ance impairments after iSCI to achieve meaningful gainsin functional mobility. Since balance control plays an im-portant role in performance of walking and daily activities[47], developing effective rehabilitation protocols to en-hance balance practice may lead to improvement in otherfunctional domains.Functional ambulation refers to the ability to performtasks that are frequently encountered in daily walking in-cluding walking on different surfaces, carrying objects, ne-gotiating doors and obstacles, and ascending/descendingcurbs and stairs [36]. The lower scores on the SCI-FAPafter training reflects improved ability to perform thesetasks due to reduced time and amount of assistance re-quired. Specifically, S1 demonstrated the greatest improve-ment in time on the obstacles, step, stairs and TUG tasks,while S2 was faster at the stairs, TUG and carry tasks. Inaddition, the ability to perform functional tasks with less as-sistance demonstrates improved dynamic balance, strengthand locomotor control [35,48]. For example, both subjectswere able to perform the sit-to-stand aspect of the TUG in-dependently at post-training compared to the personal as-sistance they required at pre-training. These findings alsosuggest a change in strategy to perform the task more inde-pendently. Although S2 completed the obstacle task withno change in time at post-training, we observed that hewas able to clear both obstacles with his less affected sidewith greater lower limb flexion rather than engaging com-pensatory movements and hitting the obstacle. Improve-ments on the SCI-FAP highlight important changes instrategy and independence of functional ambulation beyondthe ability to walk faster after task-specific training com-bined with sensory tongue stimulation.While the best rehabilitation strategy for gait traininghas been a debate (e.g. over ground vs. BWS treadmilltraining) [49,50], the optimum parameters for BWS tread-mill training have not been established for individuals withSCI. Although the optimal dosage of the training programis beyond the scope of this study, in terms of frequency,duration and intensity, we demonstrated 5 days a week at20–30 minutes of moderately intense training (RPE of 5)can improve balance and gait function. Our protocol usedthe RPE scale to determine the appropriate progressionfor speed and force contribution, reflecting the intensity ofgait training. Our findings show the feasibility of using thisapproach to progress gait training on the Lokomat withthe goal of increasing speed and reducing force contribu-tion during 30 minutes of continuous walking. In addition,reducing BWS and changing stance positions effectivelyprogressed the standing balance training. Furthermore, wedemonstrated that 20 minutes of practice at home 5 daysa week with sensory tongue stimulation could maintain oreven facilitate continued improvements in balance andfunctional ambulation. The retention of our positive re-sults and compliance rate with the home-based programindicates that this approach is a feasible option for peoplewith chronic SCI.Sensory stimulation techniques used during practice arethought to have an important role in cortical reorganizationleading to the recovery of motor function after injury [18].Afferent input may increase communication betweenthe cortex and the corticospinal tract in people withSCI [13-15]. Stimulation of the somatosensory cortexmay lead to increased efficiency in synaptic transmissionsto the motor cortex, which appears to be important formotor learning [17,51]. Also, the sensory and motor corti-ces project to the cerebellum via the pontine nucleus, thensend information back to the motor cortex [51]. Imagingstudies have shown that somatosensory stimulation of thetongue leads to changes in brainstem and cerebellum acti-vation [22,23]. In addition, post-tongue stimulation pro-duced increased activity in the pontine region, likely fromtransmission via the trigeminal nucleus [22].Although this case report provides important informationregarding the potential benefit of combined task-specifictraining and sensory tongue stimulation after iSCI, thereare several limitations to be considered. We only recruitedtwo individuals because this was a pilot study to determinethe feasibility of implementing the training program. Ouroutcome measures did not provide detailed insight onmechanisms of improved balance control or how changesin balance contributed to changes in other functional tasks.For future work, a more comprehensive balance assessment(e.g. biomechanical measures and/or dynamic tasks) mayChisholm et al. Journal of NeuroEngineering and Rehabilitation 2014, 11:96 Page 7 of 9http://www.jneuroengrehab.com/content/11/1/96reveal specific aspects of balance control that improve withtraining. Due to the nature of a case report, it is impossibleto discern how much of the observed adaptations were dueto either the sensory tongue stimulation or task-specifictraining or to the combination of these two therapies. Fu-ture studies with larger samples are required to provideinsight on whether combining the therapies results in anadditive benefit.ConclusionThis case report describes our initial implementation ofsensory tongue stimulation combined with task-specifictraining to enhance balance and gait functions in personswith iSCI. Our findings demonstrate the feasibility of in-corporating sensory tongue stimulation with task-specifictraining to improve balance and gait for laboratory- andhome-based programs for persons with iSCI. The clinicalimplications of this combined therapy protocol along witha continued home-based program to maintain improve-ments for balance and functional ambulation warrants fur-ther investigation.Additional fileAdditional file 1: This video shows our balance assessment witheyes closed at pre-training (T0) and after the initial 12 weeks oftraining (T1), along with our in-laboratory balance training set-up.Abbreviations6MWT: 6 minute walk test; 10MWT: 10 meter walk test; ABC: Activities-specificbalance confidence; ASIA: American Spinal Injury Association; BWS: Body-weightsupport; FIM: Functional independence measure; IPAQ: Impact on participationand autonomy questionnaire; iSCI: incomplete spinal cord injury; LSQ: Lifesatisfaction questionnaire; PoNS: Portable neuromodulation stimulator; RPE: Rateof perceived exertion; SCI-FAP: Spinal cord injury-functional ambulation profile;SCIM: Spinal cord independence measure.Competing interestsThe authors declare that they have no competing interests.Authors’ contributionsAll authors contributed to the concept and project design. AC and TL providedwriting of the manuscript. JSB, JB, SF and RM provided review of manuscriptbefore submission. AC and RM conducted the training and data collection. TLprovided the facility and equipment. TL, JSB, JB and SF completed the grantapplication to fund the project. All authors read and approved the finalmanuscript.AcknowledgementsWe would like to thank the participants, Dr. Zhen Chen and our studentvolunteers (Rachel Cote, Taha Qaiser and Shaolin Rahman) for theircontribution to this project. We also thank Drs. Yuri Danilov, Kurt Kaczmarek,and Mitch Tyler for their assistance and support during this study, and forloaning us the tongue stimulator units. This project was funded by an ICORDSeed Grant. TL is supported by a CIHR New Investigator Award.Author details1School of Kinesiology, University of British Columbia, Vancouver, Canada.2Department of Occupational Science & Occupational Therapy, University ofBritish Columbia, Vancouver, Canada. 3International Collaboration on RepairDiscoveries, Vancouver Coastal Health Research Institute, Vancouver, BritishColumbia, Canada V5Z 1M9. 4Centre for Applied Research and Innovation,British Columbia Institute of Technology, Vancouver, Canada.Received: 10 July 2013 Accepted: 2 June 2014Published: 6 June 2014References1. Hummel FC, Cohen LG: Drivers of brain plasticity. Curr Opin Neurol 2005,18(6):667–674.2. Edgerton VR, Tillakaratne NJ, Bigbee AJ, de Leon RD, Roy RR: Plasticity ofthe spinal neural circuitry after injury. Annu Rev Neurosci 2004, 27:145–167.3. Dietz V, Colombo G: Recovery from spinal cord injury–underlyingmechanisms and efficacy of rehabilitation. Acta Neurochir Suppl 2004,89:95–100.4. 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