ABSTRACT

Background: Low muscular strength is associated with decline in ambulatory function. Progressive strength training has been demonstrated to improve physical functional outcomes. Because eccentric exercise is a potent stimulus for increasing muscle size, strength, and power, it has the potential to serve as a time-effective intervention to improve ambulatory function at a lower metabolic cost compared with traditional strength training. We examined the effect of a 6-week eccentric cycling training intervention on walking economy in healthy individuals.

Methods: Eleven healthy individuals (age = 24 ± 3 years; body weight = 71 ± 9 kg; height = 1.7 ± 0.1 m) trained on an eccentric ergometer for 6 weeks (3×/week; 10–30 min; 54%–66% of maximum heart rate). The metabolic cost of walking was assessed 1 week prior to and 1 week following eccentric cycling training. Cost of walking was determined as the net energy cost (J·kg−1·s−1), divided by walking speed (m·s−1) during steady-state walking at 5 walking speeds (0.7, 1.11, 1.39, 1.67, and 1.9 m·s−1)

Results: Posttraining cost of walking was significantly improved across all 5 walking speeds (0.7, 1.11, 1.39, 1.67, and 1.9 m·s−1; all P < 0.01) following eccentric cycling training.

Conclusion: These results demonstrate that 6 weeks of chronic eccentric cycling training was effective in improving walking economy and can be safely administered and tolerated by healthy individuals. Enhancing ambulatory function through eccentric cycling ergometry would be beneficial for both athletic and mobility-limited populations.

INTRODUCTION

The capacity to maintain functional independence while performing activities of daily living is related to an increased quality of life (1,2). Judge and colleagues (3) examined the factors that influence physical independence and reported associations between increased physical function (i.e., balance, gait speed, and muscular strength) and the ability to perform activities of daily living. Implicitly, individuals with reduced physical function because of physical inactivity, low muscle mass reserves and quality, and age-related decline, often exert considerably greater effort and/or experience higher metabolic costs while performing physical tasks such as walking, compared with healthier or younger persons (4). Therefore, implementing appropriate interventions to counteract the reduction in physical function is imperative. Traditional resistance exercise can attenuate decline in physical function. Indeed, previous investigators reported that conventional resistance exercise improved muscular strength (58), neuromuscular performance (5,7), balance (8,9), and ambulatory function (6,10). However, traditional resistance exercise (involving a combination of concentric and eccentric contractions) that requires elevated levels of perceived exertion may represent an obstacle in exercise tolerability and compliance in healthy sedentary individuals with low muscle mass reserves and quality.

In contrast to conventional resistance exercise, eccentric exercise is a potent stimulus for eliciting improvements in muscle size (1115), strength (11,14,1619), and power (12,15,20), at a substantially lower metabolic cost (17,2125). Recently, several investigators have demonstrated that eccentric cycling can serve as a repetitive, high-force, low-metabolic cost training modality effective in producing significant hypertrophy (11,12,14), increased leg spring stiff ness (20,26,27), and power (12,15,20). While these findings demonstrate the use of eccentric cycling training to improve muscle structure and muscular function, the potential for eccentric cycling training to improve ambulatory function measured as walking economy, has not been investigated. Further, exploring a training intervention with the potential to improve metabolic efficiency and ambulatory function at a relatively low metabolic cost may have use in both sedentary and active populations.

The purpose of this study was to examine the effect of 6 weeks of eccentric cycling training on walking economy in healthy individuals. We hypothesized that this training would be a tolerable and effective intervention that improves walking economy in healthy individuals.

METHODS

Experimental Approach to the Problem

In this investigation, we implemented a 6-week eccentric cycling training intervention and evaluated pretraining to posttraining changes in walking economy, measured as the metabolic cost of walking (Cw) (Figure 1). One week prior to the start of the training, participants reported to the laboratory for pretraining assessment of Cw across 5 random ordered walking speeds of 0.7, 1.11, 1.39, 1.67, and 1.9 m·s−1 (described below). Following the pretraining assessment of Cw, participants performed eccentric cycling training 3 times a week for 6 consecutive weeks (see training protocol below). Participants returned for the posttraining assessment of Cw 1 week after the final training session.

Subjects

We recruited healthy volunteers to participate in this investigation. Volunteers needed to be considered recreationally active as characterized by Rhea (28) (i.e., consistently active for at least 1 year, but less than 5 years). Experimental procedures used in this investigation were reviewed and approved by the Central Connecticut State University Human Studies Council. Experimental procedures were verbally explained, and all participants provided written informed consent. Prior to testing all participants were screened for potential risk factors for various cardiovascular, pulmonary, and metabolic diseases, as well as orthopedic limitations with Physical Activity Readiness Questionnaire and the American Heart Association/American College of Sports Medicine Health/Fitness Facility Preparticipation Screening Questionnaire (29). Participant characteristics are shown in Table 1.

Procedures

Eccentric Cycling Training

Participants performed eccentric cycling training on an isokinetic eccentric cycle ergometer constructed using a recumbent cycle ergometer frame (Stairmaster 3800, Core Health & Fitness, Vancouver, Washington) with a 2238 kW motor (Leeson Electric, Grafton, Wisconsin) that powered the cranks in reverse (Figure 1). Pedaling rate was controlled with a variable frequency drive and set at 60 rpm. Participants were instructed to resist the reverse moving pedals of the eccentric cycle ergometer at a specified training intensity based on a percentage of the participant's age-predicted maximum heart rate (HRmax). Specifically, training intensity progressed from 54% to 66% of HRmax, while training duration increased from 10 min in the first week to 30 min in the final week. This progression of eccentric cycling training protocol was adapted from previous studies (14,17,20) and is summarized in Table 2.

During each training session, mean power and total work was determined using a power meter (Schoberer Rad Messtechnik, Julich, Germany) and average heart rate (HR) was monitored using an HR monitor (Polar, FT1, Polar Electro Oy, Kempele, Finland). In addition, during the final minute of each training session, rating of perceived exertion (RPE) for the whole body and legs only was recorded using the Borg 6–20 scale (30). To ensure that the progressive training protocol was well tolerated and safely administered to avoid unnecessary muscle damage, we implemented the eccentric-negative progression algorithm recommended by LaStayo and colleagues (31). Prior to subsequent sessions of eccentric cycling, participants indicated leg muscle soreness during a static bilateral squat movement. Soreness was assessed using a visual analog scale (0–10) with 10 representing the worst pain imaginable (15,20). Reported sore ness values of 0 to 4 were used as an indication that the eccentric exposure was deemed tolerable enough for the participant to continue with the progressive training program (31).

Walking Economy

Gas exchange data were measured using open circuit spirometry (True Max 2400, Parvo Medics, Sandy, Utah). The metabolic system was calibrated using room air and a calibration gas concentration (16.00% O2, 4.00% CO2, balanced N2). Oxygen consumption (O2), carbon dioxide production (CO2), minute ventilation (E), respiratory exchange ratio, and HR were recorded breath-by-breath and averaged to 15-s intervals. Prior to walking, resting metabolic cost was recorded for 5 min. Following the metabolic sampling at rest, participants performed walking on a treadmill (Track-Master, TMX428CP, Full Vision Inc., Newton, Kansas). Participants walked at 5 randomized speeds (0.7, 1.11, 1.39, 1.67, and 1.9 m·s−1) while gas exchange data were measured. Each walking speed was maintained for 5 min to assure a metabolic steady-state was achieved (32,33), while participants reported their walking rating of perceived exertion (RPEw) using Borg 6–20 scale during the final minute at each walking speed (30). Walking heart rate (HRw) was recorded as the HR averaged over the final minute of each walking speed. Walking economy, defined as the energy cost of moving 1 kg of body mass 1 m (J·kg−1·m−1), was measured as the and metabolic Cw derived from metabolic averages of O2 and CO2 collected during the final minute of each walking speed. Specifically, Cw was calculated using the Brockway equation, which determines energy cost (J·kg−1·s−1) at rest and during steady-state walking. The net energy cost of walking is determined by subtracting the energy cost at rest from the energy cost calculated for each walking speed. Finally, Cw expressed as (J·kg−1·m−1) is obtained by dividing net energy expenditure (J·kg−1·s−1) by walking speed (m·s−1) (34).

Statistical analysis

Paired sample t tests (IBM SPSS Statistics, v 22.0; IBM Corp, Armonk, New York) were used to evaluate the pre training to posttraining changes in physiological variables (Cw, RPEw, and HRw). Effect sizes (ESs) were calculated and ES magnitudes of <0.80, 0.80 to 1.50, and >1.50, were interpreted as small, moderate, and large effects, respectively, according to the training status of the participants (28). Values are reported as mean± standard deviation (SD) and alpha was set at 0.05.

RESULTS

We recruited 11 participants (10 male and 1 female). During the 6-week eccentric cycling training period, participants' average power progressed from 134± 49 W to 261 ± 26 W and total work progressed from 83± 32 kJ to 477 ± 145 kJ (Figure 2). Training HR, RPEbody, and RPElegs increased in response to the progressive eccentric cycling training intervention (Figure 2). Participants reported low (0.8± 0.6 to 1.2± 0.8 out of 10) levels of muscle soreness throughout the eccentric cycling training period (Figure 2).

Following eccentric cycling training, posttraining Cw was significantly reduced by 15% ± 15%, 11% ±11%, 12%± 6%, 7% ± 7%, and 10% ± 10%, across all 5 walking, speeds of 0.7, 1.11, 1.39, 1.67, and 1.9 m·s−1 respectively, compared with pretraining values (all P < 0.01; Table 3). Posttraining HRw was significantly reduced by 8%±11%, 9%±11%, and 10%±12% while walking at 0.7, 1.11, and 1.39 m·s−1, respectively (all P < 0.05; Table 3). RPEw was also significantly reduced by 15%±10% and 14%±8% while walking at 1.67 and 1.9 m·s−1, respectively (both P < 0.01; Table 3).

DISCUSSION

Researchers and clinicians have traditionally prioritized strength or resistance training in a rehabilitative plan to maintain, restore, and/or improve ambulatory function. However, traditional resistance exercise may represent an unattractive option for individuals with limited cardiovascular exercise tolerance. In contrast, eccentric exercise has been demonstrated to be a desirable alternative that allows high muscular loading with resulting low metabolic demand. Although extensive reviews by previous investigators (35,36) highlighted the superior neuromuscular adaptations elicited by eccentric training, reports of the potential for eccentric training to improve ambulatory function are limited. In this investigation, we evaluated the effect of 6 weeks of eccentric cycling training on walking economy in healthy individuals. Our main finding was that 6 weeks of eccentric cycling training improved walking economy across a spectrum of walking speeds (0.7, 1.11, 1.39, 1.67, 1.9 m·s−1). These data demonstrate that our training intervention (3×/week, 10–30 min at 54%–66% HRmax) served as a safe and tolerable strategy for improving walking economy in healthy individuals.

A possible mechanism underlying the reductions in walking metabolic cost and HR following chronic eccentric cycling training is likely due to neuromuscular adaptations involving compliant leg stiffness (37). Previous investigators (20,27,38) using protocols like that implemented in our investigation reported increases in leg spring stiffness. These investigators suggest a strong link between leg spring stiff ness and stretch reflex mechanisms (i.e., neural adaptations associated with stretch-shortening cycle), with the stretch-shortening cycle being implicated in improved efficiency and performance in running (27). Because the dynamics of running and walking can be explained by spring-mass (39,40) and bipedal spring-mass models (37), respectively, the stretch-shortening cycle allows the temporary storage and subsequent recovery of elastic energy during cyclic movements. Effective stretch-shortening cycle during cyclic movements (characterized by accentuated muscle preactivation and a short-latency stretch reflex component) regulates stiffness in the eccentric part of the stretch-shortening cycle (41,42). Thus, an increase in leg spring stiffness following chronic eccentric training might indicate an enhanced elastic strain energy storage and recovery by this cyclic stretch-shorten use of muscles during locomotion (27,43), contributing to improved efficiency during running and walking.

Morphological adaptations involving propulsive power generation during walking (4446) could also have contributed to the improvement in walk economy. Conventionally, multijoint leg extension actions play a role in power generation during walking (45). Thus, an increase in muscular strength has the potential to improve the force or power generating capacity of propulsive leg muscles that influences functional outcomes such as step length, walking speed, and walking economy. Increased muscular strength also allows participants to work at a lower percentage of their maximum strength at a given workload, reducing the reliance on anaerobic mechanisms (44). Previous investigators consistently report increased muscular strength and/or power elicited by muscular hypertrophy following eccentric training (13,15,17,47). Hence, these training-induced increases in hypertrophy and concomitant increase in muscular strength and/or power may account for improvements in walking economy observed in this investigation. Consequently, a future direction of our laboratory will be to quantify the contribution of neuromuscular adaptations to walking economy with direct measures of leg stiffness, muscle structure, and muscular power.

A limitation of our study was that our sample population of healthy individuals constrains direct clinical application of our findings. Nevertheless, previous investigators (13) implementing a similar eccentric cycling protocol reported increased muscle strength and decreased fall risk in a frail elderly population, demonstrating the potential for our findings to be reproduced in patient populations. Additionally, the limited number of commercially available eccentric cycle ergometers, manufacturing constraints, and substantial cost impede the use of eccentric cycling in physical therapy and rehabilitation centers. However, this limitation could be circumvented by constructing an eccentric cycle ergometer in house. Indeed, Elmer and Martin (48) provide a technical note on the construction of an isokinetic eccentric cycle ergometer using commonly available exercise equipment, industrial parts, and a modest amount of custom fabrication, enabling a commercially viable option for researchers and clinicians to employ eccentric cycling as an exercise modality.

Clinical Implications

To the best of our knowledge, this is the first report of improved walking economy following 6 weeks of eccentric cycling training in healthy individuals. Our results expand upon the application of eccentric exercise training for improving variables associated with strength, power, and speed performance in athletic populations (35). Addition ally, our results of improved walking economy in healthy individuals also extends upon previous work (13,15,49,50) that lays the foundation for exploring the prescription of eccentric cycling training for mobility-limited patients, as well as improving a variety of age and/or medical-related conditions associated with muscular dysfunction (31). Indeed, an extensive review by LaStayo and colleagues (31) highlighted more than 20 investigations demonstrating chronic eccentric training to be a safe and feasible rehabilitative intervention for diagnostically diverse patient groups that are traditionally considered exercise intolerant. These groups include patients who are frail and elderly, those with cardiopulmonary disorders, cancer survivors, patients with metabolic disorders, and patients with neurologic conditions. Implicitly, the benefits of improved walking economy allowing for increased mobility, ease of movement, and levels of habitual physical activity, possibly translating to improvements in functional status, over all health, and quality of life, demand that this exercise modality be considered for clinical application and future studies in patient populations.

Acknowledgments

The authors would like to thank the participants who volunteered in this study for their enthusiastic efforts throughout the training intervention and the students (Andrew Weiler, Christopher Sam boy, and Jonathan Huaqui) in the Biomechanics Laboratory for their assistance with the data collection.

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Author notes

1Department of Kinesiology, University of Georgia, Athens, GA 30602 USA

2Department of Physical Education and Human Performance, Central Connecticut State University, New Britain, CT 06050 USA

Conflicts of Interest and Source of Funding: The authors declare that they have no conflicts of interest to report. This study was supported by the New England American College of Sports Medicine (NEACSM) Undergraduate Research Grant (non-Tier 1) 2016 and the Central Connecticut Faculty-Student Research Grant 2016/17.