Strength and Step Activity After Eccentric Resistance Training in Those With Incomplete Spinal Cord Injuries

Apparently healthy males and females (N = 11) completed the ERT program. These individuals had cervical (n = 6), thoracic (n = 4), or lumbar (n = 1) iSCI for an average of 9.5 ± 4.7 years and were an average age of 39.1 ± 15.9 years. Exclusion criteria included musculoskeletal injury during or within 1 year of training and participation in other structured resistance training for the lower extremities. Participant characteristics are presented in Tables 1 and 2. This study was approved by the university Institutional Review Board, and participants signed a written consent form prior to the pretesting days.

Body mass was measured in gym clothing with shoes removed to the nearest tenth of a kilogram (Health o meter 753KL, McCook IL, or Seca 674, Hamburg, Germany). General lower extremity pain or soreness was assessed at the beginning of each day. Individuals marked a vertical line representing lower extremity pain or soreness on a 10-cm visual analog scale (VAS) where the left end of the scale equaled zero (no pain) and the right end of the scale equaled 10 (pain as bad as it could possibly be).13 Initial pain measures on days 1 and 2 were averaged to establish a baseline for future comparisons. In the instance that pain or soreness increased more than 3 cm from baseline, training was postponed or any increase in training load was delayed until the next session.

Isometric strength was assessed using a hand-held, digital dynamometer (JTech Commander PowerTrack II, Midvale, UT). The validity (R² = .66 to .76) and reliability (r = .81 to .93) of this dynamometer have been confirmed,14 and the use of hand-held dynamometry is highly correlated with the gold standard isokinetic testing in those with neurological impairments.15,16 Isometric strength was measured on both pretesting days, midway through the ERT, and after the ERT. The flexors and extensors of the knees and hip and plantar- and dorsiflexors were assessed based on their positive relationship with ambulation in individuals with frailty or neurological disorders.17–20 

For hip extensor strength, the participant was supine on a cushioned table with one leg fully extended and the other flexed to 90° at the hip and knee joints. The investigators assisted the participant in holding this leg position to prevent muscular fatigue. Once hip and knee angles were established based on goniometry validation, the investigator placed the dynamometer's sensor immediately proximal to the knee. When ready, the participant used his or her hamstrings and gluteal muscles to press against the sensor in the investigator's hand for approximately 4 seconds, establishing a maximal voluntary contraction (MVC) for hip extension. After resting, the participant repeated this procedure until there was no improvement. The testing procedure was then repeated on the other limb. While in this position, the investigator moved the sensor to the anterior portion of the thigh, proximal to the knee to capture forces exerted during hip flexion. Next, the participant sat upright with both legs off the table, again, with the hips and knees at 90°. One at a time, the participant attempted to extend the shank with the quadriceps to obtain a knee extension MVC. The sensor was located directly above the ankle on the anterior portion of the shin. Testing was repeated on the contralateral leg. To assess knee flexion, the sensor was moved to the posterior portion of the shank directly above the calcaneus tendon. The sensor was then moved to the bottom of the foot and the participant was asked to plantarflex. For comparison, a single, summed isometric strength score (in newtons and relative to the participant's mass = N/kg) was created using the best recordings on day 2.

Eccentric strength testing was completed on a recumbent, motor-driven stepper (Eccentron, BTETech, Hanover, MD). The participant was seated in a chair that was adjusted so that when both feet were on the pedals one leg was extended (knee flexion between 45° and 55°) and the other was flexed (knee at approximately 90°). After familiarization and a 1-minute warm-up, participants were asked to allow the pedals to move through several repetitions without exerting force, allowing the investigators to determine resting tone (or involuntary resting muscular tension). After familiarization with the function of the machine and an eccentric warm-up, the participant completed two bilateral, three repetition maximum (RM) attempts (left leg, then the right leg, and so on21) at 12 revolutions per minute (rpm). A 1RM for eccentric strength was calculated from the peak force of the more impaired limb for subsequent exercise prescription22 (see Table 3). Although readily used as a training tool, the Eccentron has yet to be evaluated against other criterion, isokinetic dynamometers (likely due to its unique movement and muscle recruitment pattern).

Daily step PA was captured by the validated and reliable23 Step Activity Monitor (SAM). Validity and reliability for the SAM was established in a sample of individuals with iSCI with similar gait capacity as the current sample (intraclass correlation [ICC] comparing a 10-meter walk test and SAM was 0.97).23 Calibration for expected gait characteristics followed procedures outlined by previously published reports.24 The participant affixed the SAM with a Velcro strap around the less-impaired leg.23 Daily step counts began the day after the participant received the SAM and continued for three consecutive weekdays and one weekend day (excluding bathing activities). Data were collected in 1-minute epochs.

Participants were instructed not to engage in strenuous exercise for 2 days prior to pre-, mid-, and posttesting. When entering the laboratory on day 1, participants completed the VAS, isometric strength, and eccentric strength testing protocols for familiarization. On day 2, the participants repeated the procedures to establish baseline. On the third visit, participants began training on the eccentric stepping ergometer. Participants trained two times a week for 12 weeks with a minimum of 48 hours between training sessions. Exercise prescription progression is presented in Table 3. Muscle strength measures and step PA were repeated at the end of weeks 6 and 12. The ERT was designed to target muscular strength and hypertrophy according to guidelines presented by the National Strength and Conditioning Association.25 If, however, the calculated training workload outlined in Table 3 was less than the previously evaluated tone, the same intensity progression was followed wherein the investigator added to the tone value serving as the training workload (eg, tone + 35% and tone + 17%). When participants could complete two additional repetitions in the last two sets of a training day, exercise intensity was increased in accordance to the training guidelines presented in Table 3. However, if participants were unable to reach target workloads for more than 30% of repetitions, the intensity was reduced. Efforts were made to ensure that mid and post assessments and training occurred at approximately the same time of day.

An a priori power computation indicated that the analyses would be powered at 80% when 10 participants completed the ERT (G^*Power, Version 3.1) based on measured effect sizes reported previously in a similar participant pool.26 IBM Statistics for Windows, Version 23.0 (IBM Corp., Armonk, NY) was used to analyze data. Three one-way repeated measures analyses of variance (ANOVAs) were used to evaluate the impact of ERT (baseline, midtraining, and posttraining) on isometric strength, eccentric strength, and average daily step PA. An a priori familywise alpha of p < .05 was used.

Statistics characterizing the participants are provided in Tables 1 and 2. The study included 14 individuals, however 3 discontinued participation for personal reasons prior to completing the familiarization period. Analyses included the 11 individuals who finished the ERT, completing an average of 98% of training sessions (see Table 2). Step PA data were lost for one participant due to a monitor clearing error. As such, all analyses involving step PA included 10 individuals. Average step PA did not differ following ERT [F(2.00, 18.00) = 2.73, MSE = 216,836.78, H-F p = .092]. Significant improvements were documented for eccentric strength [F(1.27, 12.71) = 8.42, MSE = 1738.35, H-F p = .009] and isometric strength [F(1.97, 19.77) = 7.10, MSE = 11.29, H-F p = .005]. Post hoc comparisons with Sidak corrections indicated that eccentric strength improved from pretest to midtest (p = .034) and from pretest to posttest (p = .038). No change was noted between midtest and posttest (p = .15). Differences in isometric strength occurred from pretest to posttest data (p = .031). See Figure 1 for means, standard deviations, and individual participant responses on study variables.

The current investigation was designed to determine how ERT affected eccentric strength, isometric strength, and daily step PA for those with chronic iSCI. Eccentric strength improved as a result of the ERT (~38%), with most improvements occurring during the initial 6 weeks of training (~23%). Isometric strength improved an average of 65%. While not statistically significant, step PA, on average, increased 32% across the ERT.

In support of previous work,26 data from the current study support the contention that individuals with iSCI have the capacity to improve neuromuscular function of the affected limbs similarly to unimpaired individuals. Our participants with iSCI showed similar improvements as young, healthy men who completed 35 ERT training sessions on a knee extension machine (~39%)27 and neurologically intact men who completed 8 weeks of unilateral knee extensors (~29%) ERT.28 These investigations varied in ERT design in regard to training intensity, sets, repetitions, and total volume. Seynnes et al27 designed the ERT so that participants completed four sets of seven maximal eccentric muscle actions. Weir and colleagues28 allowed for a familiarization period, wherein participants increased from three to five sets across the first 3 weeks with the final 5 weeks consisting of six sets of six repetitions at 80% 1RM. While the current investigation also measured eccentric strength, it should be noted that the assessment devices differed. Investigators are cautioned against making direct comparisons between eccentric strength typically assessed via criterion measures (Cybex II or Biodex System 3) and the Eccentron as the validity is still being juried.29,30 

A sample of individuals with Parkinson's disease showed improvements ranging from 13% to 29% after 12 weeks of ERT on a recumbent, eccentrically driven cycle ergometer.31 These individuals progressed from 3 to 5 minutes per session to 15 to 20 minutes per session while mediating intensity through ratings of perceived exertion.31 The more dramatic improvements observed in the current study may be due to the higher intensities and the overall program design.

Previously, Stone et al26 utilized the same training ergometer in a sample of individuals with iSCI who would be described as daily ambulators (one cervical and two thoracic iSCIs). Here, improvements in eccentric strength averaged 79% following an 8-week ERT. These participants completed three training sessions per week where the first 4 weeks emphasized muscular endurance and the second 4 weeks targeted muscular strength and hypertrophy. The eccentric strength improvements might be higher than in the current study because of the variability in iSCI severity (ie, the inclusion of wheelchair users) and differences in overall training volume. Data are not available to determine whether the variance between these two ERT protocols derives from neurological or architectural origins. Future investigations may consider directly comparing the available ERT programs to determine the value of each design relative to local muscular adaptations.

Summed isometric strength improved from pre-ERT to post-ERT. It is likely that the nearly 72% improvement from pretest to midtest and 29% change from mid- to posttesting failed to reach statistical significance because of the variance in interparticipant performance. For example, if one participant improved from 100 N/kg to 150 N/kg, this individual response would equate to a 50% improvement. Similarly, another participant who improved from 1 N/kg to 3 N/kg would improve by 300%. Future investigations may consider separating samples into groups of those who are primarily wheelchair users and community ambulators to achieve a more refined statistic. Despite this, the effect of the ERT was large enough to detect improvement in isometric strength from pre-ERT to post-ERT.

The improvements in bilateral leg strength in participants with iSCI following the ERT are like those shown following gait training modalities. Stevens et al24 noted a 57% improvement in isometric leg strength following 8 weeks of underwater treadmill training in individuals with chronic iSCI. These individuals were older (average of 47.7 years) and closer in duration to their iSCI (average of 4.8 years) compared to the current sample (average of 9.5 years post-iSCI and 39.1 years old). Weir and colleagues28 noted a 13.5% improvement in isometric strength in healthy men following an 8-week ERT program. The current ERT program may have elicited a greater percent change than previously reported protocols for various reasons: (1) The ERT was performed by individuals with lower levels of baseline function allowing for a greater ability to respond to the training, and (2) the current study had an additional 4 weeks of training than these comparison studies. Knowing that eccentric strength training can translate to isometric strength has clinical implications. Eccentric training may allow improvements in gait mechanics such as stride length and stance support time with lower metabolic demand for patients.

While speculative, the improvements observed for eccentric and isometric strength in participants with iSCI may be derivative of both neural and architectural adaptations. Short duration, high-intensity ERT has resulted in increased cross-sectional area, fascicular length, pennation angle, and muscular activity in healthy adults.27,32 Additionally, evidence is available to support that sarcomeres are added longitudinally to myofibrils in as few as 10 days following repeated exposure to ERT.32 Others have shown that short-term (approximately 1 month) ERT is sufficient to increase agonist activation and attenuate antagonist coactivation.33,34 

Eccentric and isometric strength are valuable musculoskeletal fitness components of gait training after neurological disorders. The potential for neurogenesis and regeneration of muscle microarchitecture following ERT sets the stage for individuals with iSCI to regain neuromotor control and strengthen muscles below the iSCI. Focused training of the muscles involved with standing and ambulation on the recumbent stepper may serve as a starting point for those with iSCI seeking to regain ambulatory capacity. In a different sample, it was shown that in people with cerebral palsy, strengthening of the knee flexors (r = .60) and extensors (r = .68) highly correlated with walking skills.35 Damiano et al35 identified weakness in the quadriceps and lower muscle activity tied to depreciated walking function in cerebral palsy. Specific to the ankle, gait parameters such as speed (r = .58) and single leg support time (r = −.25) are correlated with plantar flexor strength.36 In the current study, plantar flexor strength improved by 124% across the 12-week ERT. Although not specifically defined in a population with iSCI, it is postulated that lower extremity strength is highly correlated with physical function. Future investigations are needed to solidify this theory and to identify the relationship between hip strength and walking function after iSCI.

There were no significant changes in step activity as a result of the ERT. On average, daily step PA improved by 32%. This improvement and effect are smaller than that seen with iSCI after aquatic gait training (120%).2 Unsolicited participant remarks indicated that perceived walking self-efficacy improved following the ERT. However, if there were not sufficient means for the participant to walk at home (walker, braces, physical assistance, etc), the individual may have been limited in translating the improvements in leg strength to home or community walking activity. As such, future investigations seeking to identify the relationship between ERT and daily step PA should limit participation to individuals with the means to perform gait activities at home. The documented change in step activity should be valued because any improvement in PA in a population as sedentary as those with iSCI is worthwhile. However, this method of exercise training is likely not the most effective in eliciting the greatest ambulatory PA changes.

This study was an initial attempt to increase strength and step activity using a novel training modality with individuals with iSCI. Many opportunities for future research can be derived from this investigation. Investigations may consider evaluating applied outcomes such as balance, gait mechanics, and coordination when descending stairs or sitting. Further, due to the documented relationship between isometric and concentric strength and ambulation, respectively, future research aimed at determining how eccentric strength is related to walking speed is warranted.

Although all participants who completed the study met the inclusion criteria, there was a large range of daily step PA among participants (4.5–4,900 steps). This variability may have undermined the power to detect change in step activity resulting from the ERT. Post hoc analyses were conducted to determine whether a minimum WISCI (Walking Index for Spinal Cord Injury) score or level of strength could be identified that would be indicative of thresholds necessary to elicit improvements from the ERT. However, no threshold values were apparent. It would be valuable for forthcoming studies to include nonexercising control groups, larger sample sizes, and/or crossover designs. These additions would allow for smaller changes in outcome variables to be identified, allow greater generalization of findings, and allow for analyses of detraining. Moreover, future investigators may consider dividing the sample between those who primarily ambulate versus wheelchair users or recruiting a more homogenous sample. Lastly, empirical evidence is needed to determine the validity and reliability of the Eccentron as a muscle strength assessment tool.

ERT can serve as a potent stimulus in the development of eccentric and isometric strength in persons with iSCI. Although not studied in the current investigation, it may be speculated that the attained isometric and eccentric strength could translate to specific gait mechanics and walking function and is a valuable avenue for future research.