Short-term Maximal-Intensity Resistance Training Increases Volitional Function and Strength in Chronic Incomplete Spinal Cord Injury: A Pilot Study

Transcription

1 RESEARCH ARTICLES Short-term Maximal-Intensity Resistance Training Increases Volitional Function and Strength in Chronic Incomplete Spinal Cord Injury: A Pilot Study Arun Jayaraman, PT, PhD, Christopher K. Thompson, PT, PhD, William Z. Rymer, MD, PhD, and T. George Hornby, PT, PhD Background and Purpose: Recent research shows that individuals with an incomplete spinal cord injury (SCI) have a reserve of forcegenerating capability that is observable during repeated intermittent maximal volitional effort contractions. Previous studies suggest that increased neural drive contributes to the enhanced short-term forcegenerating capabilities. Whether this reserve can be harnessed with repeated training is unclear. The purpose of this pilot study was to investigate the effects of 4 weeks of maximal-intensity resistance training, compared with conventional progressive resistance training, on lower extremity function and strength in chronic incomplete SCI. Methods: Using a randomized crossover design, 5 individuals with chronic (>1 year postinjury) SCI American Spinal Injury Association Impairment Scale classification C or D were tested before and after 4 weeks of both maximal-intensity training and progressive resistance training paradigms. Outcomes measures included the 6-Minute Walk Test, the Berg Balance Scale, and peak isometric torque for strength of lower extremity muscles. Results: Maximal-intensity resistance training was associated with an average increase of ± 8.29 m on the 6-Minute Walk Test, 4 ± 1.9 points on the Berg Balance Scale, 4 ± 4.5 points on the lower extremity motor score), while no changes on the above scores were seen with conventional training. Furthermore, significant increases in peak volitional isometric torques (mean increase = 20 ± 8Nm) were observed following maximal-intensity resistance training when Center for Bionic Medicine, Rehabilitation Institute of Chicago (A.J.), Sensory Motor Performance Program, Rehabilitation Institute of Chicago (C.K.T., W.Z.R., T.G.H.), Department of Physical Therapy, University of Illinois at Chicago (T.G.H.), Departments of Kinesiology and Nutrition, University of Illinois at Chicago (T.G.H., C.K.T.), Department of Physical Medicine and Rehabilitation, Northwestern University (A.J., W.Z.R., T.G.H.), and Max Nader Center for Rehab Technologies and Outcomes Research(A.J.), Chicago, Illinois. This work was supported by the Paralyzed Veterans of America (grant 2627). The Paralyzed Veterans of America had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Supplemental digital content is available for this article. Direct URL citation appears in the printed text and is provided in the HTML and PDF versions of this article on the journal s Web site ( The authors declare no conflict of interest. Correspondence: Arun Jayaraman, PT, PhD, Department of Physical Medicine and Rehabilitation, Northwestern University, 1771, 345 E Superior St, Chicago, IL (a-jayaraman@northwestern.edu). Copyright C 2013 Neurology Section, APTA. ISSN: /13/ DOI: /NPT.0b013e a1 compared with conventional training (mean increase = 0.12 ± 3 Nm, P = 0.03). Discussion and Conclusions: Maximal-intensity training paradigm may facilitate rapid gains in volitional function and strength in persons with chronic motor-incomplete SCI, using a simple short-term training paradigm. Video Abstract available (see Video, Supplemental Digital Content 1, for more insights from the authors. Key words: intensity, spinal cord injury, strength training (JNPT 2013;37: ) INTRODUCTION To regain the ability to walk is one of the primary goals for individuals following motor incomplete spinal cord injury (SCI). 1 Therefore, rehabilitation focuses on compensating for the compromised neuromuscular system with assistive technology, 2 functional training using body-weight supported treadmill training, or functional electrical stimulation to restore ambulatory function. 3,4 Recovery of lower extremity strength is one of the primary determinants of ambulatory function following SCI. 5 Long-standing data in neurologically intact individuals suggest that various strength training regimens can increase lower extremity muscle strength using maximum volitional effort (MVE) contractions. 6 However, few studies have demonstrated similar benefits from strength training regimens for the lower extremities in persons with incomplete SCI. 6,7 The highly atrophied and fatigable neuromuscular system with various degrees of spasticity often makes volitional strength training regimens less practical and rewarding for rehabilitation focused on ambulation. 8,9 A previous study suggests that repeated, intermittent, isometric MVEs that generate substantial neuromuscular fatigue in intact individuals 10 elicit short-term increases in peak volitional torques in persons with incomplete SCI. 11 Specifically, during a single session of 5 repeated MVEs, individuals with SCI consistently demonstrate 15% to 23% increases in peak volitional torques with concomitant increases in pooled electromyographic activity. 11,12 This contrasts sharply with data from neurologically intact control subjects, who demonstrate an immediate decrease in peak torque during a similar protocol. 10 Electromyographic and low-amplitude 112 JNPT Volume 37, September 2013

2 JNPT Volume 37, September 2013 Maximal-Training Augments Function in SCI variable-frequency neuromuscular electrical stimulation assessment techniques suggest that the increased peak torques appear to be due in part to increased spinal excitability, possibly through modulatory influences on intrinsic motoneuron properties. 12 However, the effects of this increased peak torques have been quantified only in a single session, and it is unclear whether sustained increases in strength and function can be realized with training paradigms for the incomplete spinal cord injury population. The objective of this small crossover pilot study was to investigate whether the neural excitation elicited with 5 repeated, intermittent, isometric MVEs can be adapted into a short-term training program to harness the potential functional benefits and improve strength. The aim was to study the effects of a 4-week, maximal-intensity resistance training protocol using the intermittent isometric repeated MVE contractions on lower extremity function and volitional strength in chronic incomplete SCI, versus using conventional progressive resistance (CON) training. We hypothesized that the maximalintensity resistance training would show significantly greater increases in lower extremity function than CON training in individuals with chronic incomplete SCI. METHODS Five men (50 ± 12 years old) with chronic (>1 year) SCI, with a lesion level between C2-T7 and an American Spinal Injury Association Impairment Scale (AIS) Classification of C or D, 13 participated in the protocol (see Table 1). Exclusion criteria included a medical history of multiple CNS lesions, lower limb peripheral nerve injury, or an orthopedic injury that may limit maximal effort contractions, as determined through examination of medical records. Ethical approval for this study was provided by Northwestern University s institutional review board. Following written informed consent, subjects were randomly assigned to 4 weeks (12 sessions) of either maximal-intensity intermittent resistance training or CON training. All subjects acted as their own controls and participated in each training paradigm with a 2-month washout between protocols (Figure 1). Targeted muscle groups included bilateral knee flexors/extensors and ankle dorsiflexors/plantarflexors. Training Protocols Maximal-Intensity Resistance Training All participants were trained by a physical therapist who was not involved with the other aspects of the study. The Maximal-Intensity Resistance (MAX) resistance training protocol was conducted using an isokinetic dynamometer (Biodex Rehabilitation and Testing System 3, Biodex, Medical Systems Inc, Shirley, New York). Muscle groups trained included bilateral knee flexors and extensors, ankle dorsiflexors, and plantar flexors, with subjects repositioned to ensure that the tested joint axis was aligned along the axis of the isokinetic dynamometer motor/load cell. Training of knee muscle groups was performed with subjects seated in an upright position with hips flexed to 80 to 85. Knee extension trials were performed at 90 knee flexion and knee flexion trials at 30 flexion. Training of ankle muscle groups was performed with the subjects seated with their hips flexed to 80 to 90 and their knees flexed to 5 to 10. The foot of the leg to be trained was secured to a footplate with a strap placed at the forefoot and ankle. Trials for plantarflexors were performed at 0 plantarflexion, and trials for dorsiflexors were performed at 30 of plantarflexion. Subjects were instructed to perform 3 to 5 initial trials of each exercise to accommodate to the training paradigm and facilitate muscle potentiation. Subjects then performed 3 sets of 10 repetitions of MVE of isometric contractions, each repetition lasting 5 seconds with a 5-second rest between repeated MVEs. 11,12 A 2-minute rest period was given between each set of 10 repetitions. Verbal encouragement, asking the participants to give their maximal effort with every contraction and visual feedback through a computer screen showing their torque curves, was provided during the training. Conventional Progressive Resistance Training Conventional Progressive Resistance training was conducted using specific strength training machines designed for the targeted muscle groups (Pulse Fitness Systems Inc., Winnipeg, Manitoba, Canada). The exercise regimen was developed using the American College of Sports Medicine s general recommendations for physical rehabilitation interventions for individuals with neurological injuries. 14 Participants began their first training session by performing up to 12 repetitions at 60% to 65% of their predetermined 1-repetition maximum. After completing 3 sets of 10 to 12 repetitions, a 5% to 10% increase in weight was added for the next training session. 15 Verbal encouragement and rest breaks between exercise sets were similar to the MAX training condition. Participants were trained by licensed athletic trainers specializing in exercise training for individuals with disabilities. Outcome Measures Functional measures included modified Ashworth score (measure of spasticity) 16 on bilateral knee extensors/flexors which were summed into a single value, 6-Minute Walk Test 17 (assistive device kept constant before and after), lower extremity motor score and Berg Balance Scale (BBS). 18 All tests were conducted by a physical therapist, who was blinded to the order of condition assignment, 1 day before and 1 day after the training protocols. Strength-related measures included mean peak isometric torque of bilateral knee flexors/ extensors and ankle dorsiflexors/plantarflexors and central activation ratio (CAR) of the knee extensors. As described previously for SCI subjects, 11,12,15,16 peak isometric torques were collected using the isokinetic dynamometer. Subjects were seated in an adjustable chair with the lower extremity being tested securely strapped to an attachment that was mounted on a 6 degrees-of-freedom load cell (ATI Inc, Apex, North Carolina) attached to the biodex. Subjects were asked to produce 3 isometric MVEs of the lower extremity muscles. Reliability and consistency tests for isometric strength measuring in the SCI individuals have been previously established. 11,12,19,20 In addition, the strength measures were repeated both within the same session and on the next day in a subset of three subjects. We found no significant variability in the torque measures within, or between, sessions and days. C 2013 Neurology Section, APTA 113

3 Jayaraman et al JNPT Volume 37, September 2013 Table 1. Subject Demographics and Baseline Functional Scores Subject Sex Age, y Level of Injury Time Since Injury, mo Exercise Condition Randomized to First AIS Classification 6-Minute Walk Scores, m 1 M 31 C3 84 Con D M 54 C2 48 Max D M 50 C6 192 Con C M 63 T7 396 Max C M 53 C5 336 Con D Abbreviations: AIS, American Spinal Injury Association (ASIA) Impairment Scale; BBS, Berg Balance Scale. BBS CAR, a measure of volitional muscle activation, was determined as the peak MVE torque divided by the torque generated with supramaximal neuromuscular stimulus trains (10 pulses, 100 Hz, 135 V) superimposed during single MVEs. 11 STATISTICAL ANALYSIS The Wilcoxon-Mann-Whitney test (nonparametric test) was used to compare differences between MAX training versus CON training conditions. The conditions were compared using the difference in pre- and posttraining values for each subject in the MAX condition versus the difference in preand posttraining values for the same subjects in the CON condition. This test was chosen for statistical analysis, as the assumption of normality could not be confirmed with the dependent variable (ie, the difference) owing to the small sample size. For measures of isometric strength, multiple comparisons were performed. The between-condition and within-condition comparisons for strength were performed between the moreaffected sides (weaker sides), the less-affected (stronger sides), and overall lower extremity muscle strength of the MAX condition and the CON condition. For the within-condition comparison, a signed rank sum test (nonparametric test) was used. Statistical significance for both tests was set at P < RESULTS Comparison of the MAX vs CON Training Conditions Average raw values of all the outcome variables have been summarized in Table 2. The BBS of the MAX condition was the only functional outcome measure that showed a significant increase when compared with the CON condition, indicating significant improvements in the overall balance of Figure 1. Study Design. A flowchart on the progression of the randomized cross-over pilot study. 114 C 2013 Neurology Section, APTA

4 JNPT Volume 37, September 2013 Maximal-Training Augments Function in SCI Table 2. Summary of Raw Values of Outcome Measures MAX Training Condition (Mean ± SD) CON Training Condition (Mean ± SD) Pre Post Pre Post BBS 26 ± ± 16 a 24 ± ± 23 6-minute walk, m 122 ± ± 108 a 124 ± ± 111 mash 5 ± 4 2 ± 3 4 ± 4 4 ± 4 CAR (ratio) 0.4 ± ± ± ± 0.2 LEMS 33 ± ± 7 31 ± ± 16 Overall peak torque, Nm 34 ± ± 28 a 32 ± ± 13 Abbreviations: BBS, Berg Balance Scale; CAR, central activation ratio; LEMS, lower extremity motor score; mash, modified Ashworth score. a P < MAX training was also associated with improvements in gait and balance outcomes, with a trend toward reduced spasticity and increased voluntary activation, although changes in these measures were not significantly different when compared with CON training. The short duration of training (4 weeks) suggests that neural adaptations contributed to the improvements in strength as long-standing scientific evidence suggests that the strength gains during initial weeks of resistance training are due to increased neural excitability, which is later accompanied by skeletal muscle hypertrophy. 12,21 Previous studies, using a similar volitional muscle activation protocol of repeated intermittent MVE contractions, have suggested that acute changes incomplete-sci participants following maximal-intensity resistance training (P = 0.05; Figure 2C). As previously described, multiple comparisons of isometric strength were performed comparing the more affected sides (weaker sides) and the less affected sides (stronger sides) individually and finally with overall lower extremity muscle strength between the training conditions (Figure 3B). The MAX training condition showed a significant increase in their peak isometric torque levels compared with the CON training condition in both their more-affected (P = 0.03) and lessaffected sides (P = 0.03) sides. Furthermore, the MAX condition showed significant improvements in the overall lower extremity muscle strength compared with the CON condition (P = 0.03). Comparison Within Condition (Pretraining vs Posttraining) Conventional progressive resistance did not show any within-condition difference for the either the functional or the strength measures following training. However, with the MAX condition, the 6-minute walk test showed significant increases in the distance walked following training (P = 0.03; Figure 2B) and BBS also showed significant increases in the balance scores following MAX training (P = 0.01; Figure 2C). Clinical measures of spasticity showed a trend toward reduced spasticity levels (modified Ashworth score; P = 0.06), and CAR scores also showed an increase following MAX training (P = 0.08), suggesting a trend toward increased central activation of the tested muscle groups. Subjects who participated in MAX training demonstrated graduated increases in strength each week of training for 4 weeks (Figure 3A). Peak isometric torques measured for overall lower extremity muscles and individually for the more-affected and less-affected side muscle groups significantly increased following MAX training (P = 0.05). DISCUSSION In this pilot study, 4 weeks of MAX training performed by individuals with motor incomplete SCI resulted in significant increases in balance and improvements in isometric volitional strength across multiple muscle groups compared with CON training. Changes in strength were observed in both weaker and stronger side muscles of the study participants. The Figure 2. Effects of exercise training on clinical outcome measures. Changes in raw scores in clinical outcomes measures compared between the maximal-intensity training condition (MAX) and the conventional training condition (CON): (A) Modified Ashworth Score, (B) 6-Minute Walk Test, and (C) Berg Balance Scale. a Significant difference between or within conditions as indicated in the figures (P < 0.05); values are mean ± SD. C 2013 Neurology Section, APTA 115

5 Jayaraman et al JNPT Volume 37, September 2013 Figure 3. Effects of high-intensity training on strength. (A) Single subjects changes in peak knee extensor torque (Nm) with repeated maximal contractions on the first session of each week of the 4-week MAX training programs. Black traces indicate the average first maximum volitional effort (MVE) over 3 sets, gray bars indicate 2nd 10th MVEs. (B) Changes in peak torque averaged across all 4 muscle groups in both limbs in comparison to pretorque levels for both the MAX and CON conditions. a Significant difference between and within groups as indicated in the figures (P < 0.05); values are mean ± SD. in central (neural) activation, through increased electromyographic activity, partly contributed to short-term, singlesession strength increases. 11,12 The studies also suggested that increased spinal excitability may partly underlie the improvements in volitional activation. 12 Thus in the present study, the short (4-week) training duration and the CAR data suggest that improved central nervous system activation likely accounts for some of the observed strength increases. While it is now widely accepted that strengthening does not increase spasticity, there was a time when high-intensity training was not recommended for individuals with central nervous system pathology for the fear of increasing their spasticity or tone. 22,23 A trend for reduced spastic reflexes seen following MAX training may suggest a relationship between improving volitional control and a decrease in spasticity. The functional improvement seen in the 6-minute walk and BBS after the non task-specific MAX training further supports the suggestion of improved volitional control. Interestingly, strength increased approximately 64% and approximately 80% in the knee extensors and plantarflexors, respectively, following 4 weeks of training. The magnitude of strength increases seen in this study represents greater improvements than reported previously for volitional resistance training. 6,7 Traditionally, strength training for SCI is focused on the upper extremities. This is undertaken to help the individuals transfer from their wheelchair and perform other activities of daily living. 24 Few studies target lower extremity strength training regimens for individuals with incomplete SCI. 6,7 A study by Gregory et al 6 showed an average of approximately 31% increase in strength in the knee extensors (28.9 ± 4.4%) and plantarflexors (35.0 ± 9.1%) muscle groups following 12 weeks of training, while Harvey et al 7 showed an approximately 26% increase in strength in the knee extensors following 8 weeks of resistance training combined with electrical stimulation. We believe that a major factor that contributed to the superior strength gains in the MAX condition was the highintensity, long-duration contraction (5 seconds) with intermittent breaks (5 seconds) and the testing condition essentially replicated the training condition. Finally, the functional and strength improvements seen in this study were achieved in participants with chronic incomplete SCI who had been discharged from therapy and nontraditional SCI recovery programs many years before participating in this study. Results of this study suggest that the approach used in this study may allow persons with SCI to improve their ability to generate volitional force even years after SCI. LIMITATIONS Major limitations of this preliminary study should be acknowledged. These include the small sample size, which clearly limits the ability to generalize the results to the SCI population, and lack of an understanding of specific mechanisms underlying these results. The lack of the understanding of the potential mechanisms clearly undermines the ability to classify specific factors (long-duration maximal effort contractions, intermittent rest) that contributed to the functional and strength gains seen in the MAX condition. Second, the task training-specific nature of the strength outcomes, the subjects in the MAX condition trained isometrically and CON condition trained isotonically and one of our main outcomes, was isometric strength. Therefore, the strength improvements (isometric strength) seen in the MAX condition to a large extent need to be attributed to the specificity (isometric) of training. Finally, the statistical analysis did not include parametric testing and correction for multiple interactions. Despite these limitations, this preliminary study provides some unique findings regarding training strategies. CONCLUSIONS Maximal effort contractions, combined with intermittent rest, may be associated with functional and strength gains in people with incomplete SCI. REFERENCES 1. Dobkin BH. Motor rehabilitation after stroke, traumatic brain, and spinal cord injury: common denominators within recent clinical trials. Curr Opin Neurol. 2009;22(6): Biering-Sørensen F, Hansen RB, Biering-Sørensen J. 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