| | Sensory Stimulation Augments the Effects of Massed Practice Training in Persons With TetraplegiaPreliminary results of this study were presented to the American Paraplegia Society, September 2005, in Las Vegas, NV. Abstract Beekhuizen KS, Field-Fote EC. Sensory stimulation augments the effects of massed practice training in persons with tetraplegia. ObjectiveTo compare functional changes and cortical neuroplasticity associated with hand and upper extremity use after massed (repetitive task-oriented practice) training, somatosensory stimulation, massed practice training combined with somatosensory stimulation, or no intervention, in persons with chronic incomplete tetraplegia. DesignParticipants were randomly assigned to 1 of 4 groups: massed practice training combined with somatosensory peripheral nerve stimulation (MP+SS), somatosensory peripheral nerve stimulation only (SS), massed practice training only (MP), and no intervention (control). SettingUniversity medical school setting. ParticipantsTwenty-four subjects with chronic incomplete tetraplegia. InterventionsIntervention sessions were 2 hours per session, 5 days a week for 3 weeks. Massed practice training consisted of repetitive practice of functional tasks requiring skilled hand and upper-extremity use. Somatosensory stimulation consisted of median nerve stimulation with intensity set below motor threshold. Main Outcome MeasuresPre- and post-testing assessed changes in functional hand use (Jebsen-Taylor Hand Function Test), functional upper-extremity use (Wolf Motor Function Test), pinch grip strength (key pinch force), sensory function (monofilament testing), and changes in cortical excitation (motor evoked potential threshold). ResultsThe 3 groups showed significant improvements in hand function after training. The MP+SS and SS groups had significant improvements in upper-extremity function and pinch strength compared with the control group, but only the MP+SS group had a significant change in sensory scores compared with the control group. The MP+SS and MP groups had greater change in threshold measures of cortical excitability. ConclusionsPeople with chronic incomplete tetraplegia obtain functional benefits from massed practice of task-oriented skills. Somatosensory stimulation appears to be a valuable adjunct to training programs designed to improve hand and upper-extremity function in these subjects. IMPAIRED HAND FUNCTION severely limits the ability of people with cervical spinal cord injury (SCI) to perform manual activities of daily living (ADLs)1; a majority of the people with cervical SCI surveyed by Snoek et al2 expected a significant improvement in their quality of life with improved hand function. Incomplete cervical SCI is currently the most common form of SCI (34.3% of all SCI cases).3 Because approximately 61% of people with cervical SCI have functionally incomplete injuries,3 varying degrees of arm and hand function may be possible regardless of the level of the lesion. Recovery of function after SCI largely depends on the preservation of some anatomic connections, and may also depend on the physiologic reorganization of the brain and spinal cord.4 Massed practice (repetitive task-oriented training) and somatosensory stimulation are 2 interventions that may maximize transmission effectiveness of descending motor commands. There is evidence that massed practice (of which constraint-induced therapy is 1 form) promotes cortical reorganization and improved upper-extremity function after stroke5, 6, 7, 8, 9, 10, 11 and after SCI.12, 13 Several neuroimaging and transcranial magnetic stimulation studies have shown that massed practice training produces an extensive use-dependent cortical reorganization in animals with cortical lesions14 and people with stroke.7, 8, 9, 10 Increased scores on tests that demonstrate improvement in functional use of the affected extremity are associated with the cortical reorganization that follows massed practice training.5, 6, 11, 15 It has been suggested that the recovery of upper-extremity dexterity following a hemi-section of the cervical spinal cord in macaques is dependent on the ability to optimally use the limited information that is being transmitted via spared corticospinal connections.16 Investigators have concluded that it is the reduced rate of transmission of relevant information from the motor cortex to the spinal cord that limits performance.16 Hoffman and Field-Fote12 found that bimanual massed practice training combined with somatosensory stimulation resulted in increased area and volume of the cortical motor map in a subject with complete C6 tetraplegia, indicating an increase in cortical excitability in this subject. This cortical change was associated with improvements in upper-extremity function, strength, and sensation.12 These findings support the use of massed practice after incomplete SCI to maximize the effectiveness of corticospinal drive onto spinal motoneurons. Prolonged, repetitive peripheral nerve stimulation can induce changes in the excitability of the cortical projections of hand muscles in nondisabled persons17; in people with stroke, repetitive peripheral nerve stimulation has increased pinch strength18 and improved functional performance.19 Furthermore, people who received repetitive peripheral nerve stimulation before a motor training session maintained improved levels of functional performance when re-tested 30 days later.19 Afferent information may change cortical representations and/or improve motor performance in people with SCI, just as it does in nondisabled people and people with stroke. A possible underlying mechanism is that the somatosensory cortex has an important role in cortical reorganization after injury.4, 20 Therefore, afferent input may contribute to cortical reorganization and, ultimately, to functional recovery via increased communication between the cortex and the corticospinal tract in SCI subjects. Traditional rehabilitation interventions focus on the use of compensatory strategies that emphasize the use of stronger muscles rather than on the restoration of function in the weaker muscles. Unfortunately, such interventions may not subsequently maximize motor and sensory recovery.21 Preliminary investigations that compared the effects of massed practice training combined with somatosensory stimulation (MP+SS) with the effects of massed practice (MP) only found that MP+SS produced a significant improvement in upper-extremity function test scores and pinch grip force while MP only did not. The effects of somatosensory stimulation only remain unknown, however. Our purpose in this study was to examine the effects of MP+SS, MP only, and SS only on upper-extremity function, pinch grip force, sensory function, and cortical excitability in subjects with incomplete cervical SCI. We hypothesized that the intervention combining MP and SS would result in greater changes in the previously mentioned outcomes than would the interventions involving only MP or SS. Methods  Research Design Subjects were randomly assigned to 1 of 4 groups: MP+SS, MP only, SS only, or the control group. Subjects in the intervention groups received the assigned intervention 5 times a week for 3 weeks, for 2 hours per session. The intervention was directed at the upper extremity having the lower motor score (n=11 subjects). If, however, the extremity with the lower motor score had no voluntary thumb contraction, we used the extremity with the higher motor score (n=13 subjects). Subjects were tested before and after the training. Testing Procedures Our outcome measures included: (1) the Jebsen-Taylor Hand Function Test (JTHFT) scores, (2) Wolf Motor Function Test (WMFT) timed task scores, (3) maximal pinch grip force, (4) Semmes-Weinstein monofilament sensory testing, and (5) the intensity of the cortical stimulation required to evoke a motor threshold response (50−100μV) in thenar muscles. Functional tests The JTHFT is a standardized measure for assessment of hand function that is reliable and valid for use with SCI subjects.23 This timed test consists of 7 functional tasks that require finger and hand movement. Time to complete each of the 7 timed subtests was summed to produce a total JTHFT score. The WMFT is a laboratory-based upper-extremity function test, involving 15 timed measures and 2 force-based measures. The test items progress in complexity from engaging individual joints to use of the entire upper extremity.24, 25 The WMFT has high interrater reliability, internal consistency, and test-retest reliability in people with stroke.24, 25 Scores for the 15 timed measures are summed to produce a total time score, referred to as WMFT for performance time.26 Pinch grip force We tested maximal key pinch force with a MicroFet 4a digital dynamometer. The dynamometer was held between the lateral aspect of the middle phalanx of the index finger and thumb pad and subjects were instructed to squeeze as hard as possible for 3 seconds. We obtained 5 consecutive pinch force measurements from each subject and calculated the average of the 5 trials. Sensory monofilament testing We used Semmes-Weinstein monofilaments to test sensation at 3 sites in the median nerve distribution of the target hand: the tips of the thumb and index finger, and the base of the phalanx of the index finger.27 Testing began with the largest diameter monofilament and continued in order of decreasing diameter until sensation was perceived in fewer than 5 of 10 applications of a particular monofilament. The sensory scores for each site ranged from 0 to 5, corresponding to the smallest monofilament perceived by the subject at that site: 0, 4 or fewer responses to the largest monofilament; 1, filament 6.65; 2, filament 4.56; 3, filament 4.31; 4, filament 3.61; and 5, filament 2.83. We summed the scores from all sites to calculate a total score ranging from 0 to 15, with a higher score representing higher sensory discriminatory function. Cortical excitability assessed via motor evoked potential threshold Motor evoked potentials (MEPs) from the thenar muscles were elicited using transcranial magnetic stimulation (TMS) applied over the scalp with a Magstim 200 stimulatorb (maximum magnetic field strength, 2T), with a figure-8 shaped coil. TMS evokes a contralateral motor response that can be recorded from the muscle of interest using surface electromyography. Recordings from the thenar muscles, obtained from closely spaced pairs of surface Ag-AgCl disk electrodesc placed over the thenar eminence of the target hand, were used to record the MEPs. Electrode placement was as follows: active electrode over the center of the abductor pollicis brevis, reference electrode over the metacarpophalangeal joint of the thumb, and ground electrode over the olecranon process. Skin impedance between the electrodes was maintained below 5kΩ. Signals were amplified (×1000), filtered (bandpass, 5Hz−1kHz), sampled at 2kHz with a data acquisition system (CED 1401d) and analyzed off-line with customized software (Signal Data Acquisition Softwared). We followed a published protocol28 using motor threshold to measure cortical excitability of the target muscle at rest. The electromyography recordings included a 200-ms period prior to the TMS stimulus pulse. The records were examined before analysis to ensure that there was no electromyographic activity in the target muscle before the stimulation. Trials demonstrating electromyographic activity in the target muscle were discarded. To measure motor threshold, the coil was placed over the frontoparietal region contralateral to the target muscle. With an initial stimulus intensity of 90% of maximum stimulator output, the coil was moved in small increments to identify the site at which the largest MEP could be evoked. The intensity of the magnetic stimulation was decreased progressively in 5% increments until a level was reached that induced reliable threshold level MEPs (peak-to-peak amplitude, 50−100μV) in 5 to 7 out of 10 consecutive stimuli. This level of stimulus intensity is considered motor threshold for the target muscle (expressed as a percentage of maximum stimulator output).28 Training Procedures Somatosensory stimulation protocol Subjects in the MP+SS and the SS groups received 2 hours of median nerve stimulation (applied at the level of the wrist) 5 times a week for 3 weeks following a previously published protocol.12, 13, 18 The protocol for somatosensory stimulation was based on that used by Conforto et al18 in persons with stroke. Ag/AgCl electrodes were placed on the distal forearm with the anode at the wrist crease and the cathode placed 2cm proximal to the anode. Trains of electric stimulatione (frequency, 10Hz; on/off duty cycle, 500/500ms; pulse duration, 1ms) were delivered at 1Hz. The stimulation intensity was adjusted to elicit a visible twitch of the thumb muscles, the intensity was then reduced to a level at which no visible twitch was observed. These stimulation parameters are believed to preferentially activate large cutaneous and proprioceptive sensory fibers.29 The low stimulation intensity does not interfere with the massed practice for subjects in the MP+SS group (with MP as described in the previous section). Subjects in the SS group received only the somatosensory stimulation protocol and were told not to move the stimulated forearm and hand during the sessions. Control group Subjects in the control group participated in 2 testing sessions 3 weeks apart. They did not participate in any organized therapy or research in the 3 weeks between their pre- and post-testing and were instructed to continue their typical daily routines. Statistical Analysis We used Stataf for our data analysis. All descriptive data are presented as mean ± standard error of the mean (SEM). Significance levels were accepted at P less than .01 for all analyses. Before the analysis, we checked all data to verify that the assumptions of normality of distribution and homogeneity of variance were met and that there were no significant between-group differences in the pretest data. Data that did not have a normal distribution were log transformed before the analysis. Data that had heterogeneity of variance were analyzed using regression analysis with robust standard errors. There were no significant between-group differences in pretest values for any of the outcome measures. Scores for the JTHFT, WMFT, and pinch grip force were assessed using 1-way analyses of covariance (ANCOVA) to evaluate pre- and post-test differences in outcome measures. We used ANCOVA to diminish the effect of individual differences in the data. Pretest scores were included as a covariate, along with the group variable. To meet assumptions of normal distribution, the measures related to the JTHFT and WMFT were transformed to natural logs (ln) before analysis. Log transformations resulted in a normal distribution. When between-group differences were identified, we used post hoc Scheffé tests to evaluate the differences between groups. In this analysis, all intervention groups were compared with each other and to the control groups. If pre- and post-test measures for an intervention group(s) differed significantly from that of the control group, we considered this to be a significant effect of the intervention. For measures in which more than 1 intervention group differed from the control group, the intervention group(s) with the greatest difference in pre- and post-test measures were considered to be associated with a larger intervention effect. For the Semmes-Weinstein monofilament testing data, we calculated pre- to post-training percentage change scores for each subject because of the large between-subject differences in the absolute values of outcome measures. We used analysis of variance (ANOVA) to compare the percentage change scores between the 4 conditions. We used the Tukey honestly significant difference test for post hoc analyses if the result of the ANOVA was not significant for differences between groups. Because of unequal variances, we evaluated the MEP threshold data with regression analysis using robust standard errors. We used the Scheffé test to evaluate differences between groups. Pretest measures and group were included in the model to predict post-test values. Results Functional Tests Jebsen-Taylor Hand Function Test The between-groups difference in response to intervention was statistically significant (F=11.24, P<.001). Functional hand use as measured by the JTHFT showed an intervention effect for each of the groups; post hoc testing showed that subjects in the MP+SS, MP, and SS groups had significant improvements in their scores compared with the control group (F=33.69, P<.001; F=8.39, P=.009; F=7.46, P=.01, respectively) (fig 1). Scores for the MP+SS group indicated significantly greater improvements compared with both the MP and SS groups (F=8.59, P=.009; F=9.52, P=.006, respectively). Table 3 shows the pre- and post-test mean differences. Wolf Motor Function Test The WMFT was developed for use with stroke patients. For that reason, we calculated the correlation between the WMFT and the JTHFT (which has been validated in people with SCI) to establish the concurrent validity of the WMFT for use with SCI subjects. There was a statistically significant correlation between the pretraining WMFT and JTHFT scores (r=.915, P<.001), demonstrating concurrent validity of the WMFT for use in people with SCI. The pretest WMFT scores in the control group were also highly correlated (r=.97) with the post-test WMFT scores in this group, indicating high test-retest reliability and stability of this measure in people with incomplete cervical SCI. There was a significant between-groups difference in functional upper extremity use as measured by the WMFT scores (F=12.52, P<.001). Post hoc testing indicated that subjects in the MP+SS and the SS groups had significant improvements in WMFT scores compared with the control group (F=33.92, P<.001; F=7.98, P=.01, respectively) (fig 2). Subjects in the MP+SS group demonstrated significantly greater improvement in WMFT scores compared with the subjects in the MP group and the SS group (F=20, P=.002; F=9.84, P=.005, respectively). Table 3 shows the pre- and post-test mean differences. Pinch grip force There was a significant between-groups difference in pinch grip force measures (F=9.51, P<.001). Post hoc testing showed that subjects in both the MP+SS and the SS groups had significant gains in pinch grip force compared with the control group (mean differences, 2.98kg, P=.004; 3.14kg, P=.003, respectively) (fig 3). Table 3 shows the pre- and post-test mean differences. Sensory (monofilament) testing Between-group differences in percent change scores for Semmes-Weinstein monofilament sensory testing were significant (F=4.699, P=.01) (fig 4). Post hoc testing indicated that the MP+SS differed significantly from the control group (P=.01). No other significant between-group differences were identified. See table 3 for pre- and post-test mean differences. Cortical excitability assessed via MEP threshold One subject in the SS group was excluded from MEP testing due to risk factors for the use of TMS. We identified a significant between-groups difference (F=19.06, P<.001) for the MEP threshold data, with the regression model explaining 78.5% of the variation in the data. All else being equal, both the MP+SS group and the MP group differed significantly from the control group (t=−4.28, P<.001; t=−4.25, P<.001, respectively) (fig 5). See table 3 for pre- and post-test mean differences. Discussion The results of this study indicate that in subjects with incomplete cervical SCI, MP+SS, MP, and SS interventions were associated with significant gains in functional hand use compared with no intervention. Subjects receiving the MP+SS and SS interventions also experienced improvements in upper-extremity function and pinch grip force compared with the control group. The large variability in the WMFT scores for the subjects in the MP group, however, may have obscured an intervention effect in this group for this outcome measure. Our results indicate that practice of functional tasks combined with augmented afferent input was associated with the greatest change in hand and upper-extremity function, pinch strength, and sensory scores. Only those subjects receiving MP+SS had significant improvements in sensory function compared with no intervention. Despite many significant between-groups differences, the stated hypothesis was not fully supported because MP+SS did not differ significantly from SS in several of the outcome measures. The role of somatosensory input in the improvement in function and strength in the MP+SS and SS group warrants further exploration. The finding that there were significant improvements in the group receiving somatosensory stimulation alone suggests that afferent input may be a powerful tool in promoting neural plasticity (for review, see Field-Fote30). We hypothesize that it was the afferent input combined with movement that was the key factor, because the group receiving MP only did not show the extent of improvement achieved by those receiving MP+SS. It is possible that the MP+SS group received the greatest benefits from training inasmuch as they were subjected to 2 forms of afferent input: the naturally occurring afferent input associated with movement, and the augmented sensory input provided by the somatosensory stimulation. The lack of significant improvement in force production and upper-extremity functional test scores in the MP group may be attributed to the development of new movement strategies in this group. Training may result in a more typical and appropriate movement strategy, but because it is newly learned it is performed slower than the previous, more habitual strategy. In a study by Hoffman and Field-Fote,12 a subject with complete C6 tetraplegia approached upper-extremity tasks with a new movement pattern after a 3-week program of bimanual massed practice plus somatosensory stimulation training. These new movement patterns allowed the subject to have more control over the task, yet completion of the task required more time.12 It is also possible that 3 weeks of MP training is not sufficient to achieve functional gains when using a new movement strategy. A longer training period may have resulted in similar force production and functional outcomes in the MP group as in the MP+SS and SS groups. It is puzzling that there was a lack of statistically significant change in cortical excitation threshold in the SS group, because this group had changes in the functional and strength-related outcome measures, and also because the threshold was decreased for both the MP+SS and MP groups after the intervention. This may be explained by changes that occurred in the location of the cortical map that were associated with improvement in function. There is evidence that people exhibit posteriorly shifted cortical motor potentials after SCI20 and as they recover function, the motor potential shifts back to a more anterior position.4, 12 A recent case report12 documents such a shift in association with 3 weeks of MP+SS intervention. Because we measured the threshold of the cortically evoked potential at the same cortical site before and after training, it is possible that there was a change in the location of the site of greatest excitability after training that would have been missed with our MEP protocol. Our results in this study are consistent with those of our previous study13 in that MP+SS significantly increased upper-extremity functional scores and pinch grip force compared with MP only.13 The addition of the SS group to this study provides information on the contribution of SS in recovery of function and force production, and it is evident from the results that SS can induce improvements in function and strength in the absence of movement practice. These results also suggest that although functional gains can be made with SS, the combined approach (MP+SS) resulted in the most robust improvements in functional scores, strength, and sensory function. Study Limitation and Further Investigations There are several areas in which future studies may build on these results. A larger sample size would likely have allowed identification of other differences between the intervention groups and the control group, and among the intervention groups, inasmuch as several outcome measures showed trends toward significance. Further, while there were no significant between-group differences in pretest values, the small sample size resulted in unequal distribution of pretest values in some of the outcome measures. A larger sample size would probably provide a more equal distribution of scores among all outcome measures. Follow-up testing should be performed to give subjects an opportunity to consolidate their newly acquired skills. Additionally, a longer training period may have resulted in a larger intervention effect. Mapping studies should be performed to determine whether the cortical map changes in response to the stimulation, which we would have failed to observe in all groups by examining the MEP threshold at a specific cortical site. MEP testing should also be performed at intervals during the training program to assess whether changes in cortical excitability are occurring during initial skill acquisition. Conclusions The findings of this study indicate that the combination of MP+SS may be a beneficial rehabilitative tool for use in the restoration of force production and function in people with incomplete cervical SCI. The finding that SS only produces gains similar to those observed with the combination of MP+SS suggests that the SS protocol may be beneficial in the early stages of rehabilitation, or in situations when the patient may not be able to participate in an intensive exercise program. Although SS was associated with increases in pinch grip force and functional test scores, the finding that the SS group did not show increased cortical excitability suggests that the MP component of the training may be necessary for maximum benefit. The improvements in pinch grip force and functional test scores resulting from MP+SS and SS (and possibly MP) training may contribute to improvements in ADLs and work skills and thereby increase overall independence in people with cervical SCI. Suppliers Acknowledgments We gratefully acknowledge the statistical support of Marion McGregor, PhD, DC. We also thank Rose Rine PhD, PT, Christine Thomas, PhD, and Steve Wolf, PhD, PT, for many constructive suggestions about the manuscript, and Deepa Patel for her assistance in supervising the training sessions. References 1. 1Colyer RA, Kappelman B. Flexor pollicis longus tenodesis in quadriplegia at the sixth cervical level. J Bone Joint Surg Am. 1981;63:376–379. MEDLINE 2. 2Snoek GJ, IJzerman MJ, Hermens HJ, Maxwell D, Biering-Sorensen F. Survey of the needs of patients with spinal cord injury: impact and priority for improvement in hand function in tetraplegics. Spinal Cord. 2004;42:526–532. MEDLINE |
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25. 25Wolf SL, Catlin PA, Ellis M, Archer AL, Morgan B, Piacentino A. Assessing Wolf Motor Function Test as outcome measure for research in patients after stroke. Stroke. 2001;32:1635–1639. 26. 26Whitall J, Waller SM, Silver KH, Macko RF. Repetitive bilateral arm training with rhythmic auditory cueing improves motor function in chronic hemiparetic stroke. Stroke. 2000;31:2390–2395. 27. 27Rosen B, Lundborg G. A model instrument for the documentation of outcome after nerve repair. J Hand Surg [Am]. 2000;25:535–543. Abstract | Full Text |
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29. 29Panizza M, Nilsson J, Roth BJ, Basser PJ, Hallet M. Relevance of stimulus duration for activation of motor and sensory fibers: implications for the study of H-reflexes and magnetic stimulation. Electroencephalogr Clin Neurophysiol. 1992;85:22–29. MEDLINE 30. 30Field-Fote EC. Electrical stimulation modifies spinal and cortical neural circuitry. Exerc Sport Sci Rev. 2004;32:155–160. MEDLINE a The Miami Project to Cure Paralysis, University of Miami Miller School of Medicine, Miami, FL b Department of Veterans Affairs Medical Center, Miami, FL c Department of Physical Therapy, University of Miami Miller School of Medicine, Miami, FL d Department of Physical Therapy, Nova Southeastern University, Ft. Lauderdale, FL.  Reprint requests to Edelle C. Field-Fote, PhD, PT, The Miami Project to Cure Paralysis, University of Miami Miller School of Medicine, 1095 NW 14 Ter (R-48), Miami, FL 33136.
Supported by The Miami Project to Cure Paralysis, University of Miami Miller School of Medicine, and the Department of Veterans Affairs Medical Center, Miami, FL. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the authors or upon any organization with which the authors are associated. PII: S0003-9993(07)01814-X doi:10.1016/j.apmr.2007.11.021 © 2008 American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation. Published by Elsevier Inc. All rights reserved. | |
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