Eccentric Cycle Exercise in Severe COPD: Feasibility of Application

Abstract

Eccentric cycling may present an interesting alternative to traditional exercise rehabilitation for patients with advanced COPD, because of the low ventilatory cost associated with lengthening muscle actions. However, due to muscle damage and soreness typically associated with eccentric exercise, there has been reluctance in using this modality in clinical populations. This study assessed the feasibility of applying an eccentric cycling protocol, based on progressive muscle overload, in six severe COPD patients with the aim of minimizing side effects and maximizing compliance. Over 5 weeks, eccentric cycling power was progressively increased in all patients from a minimal 10-Watt workload to a target intensity of 60% peak oxygen consumption (attained in a concentric modality). By 5 weeks, patients were able to cycle on average at a 7-fold higher power output relative to baseline, with heart rate being maintained at ∼85% of peak. All patients complied with the protocol and presented tolerable dyspnea and leg fatigue throughout the study; muscle soreness was minimal and did not compromise increases in power; creatine kinase remained within normal range or was slightly elevated; and most patients showed a breathing reserve > 15 L.min⁻¹. At the target intensity, ventilation and breathing frequency during eccentric cycling were similar to concentric cycling while power was approximately five times higher (p = 0.02). This study showed that an eccentric cycling protocol based on progressive increases in workload is feasible in severe COPD, with no side effects and high compliance, thus warranting further study into its efficacy as a training intervention.

Keywords: :

• Eccentric exercise
• Muscle contraction
• Ventilatory constraint
• Pulmonary rehabilitation.

INTRODUCTION

Endurance exercise training is widely considered the cornerstone of pulmonary rehabilitation (1), traditionally performed on a cycle ergometer or treadmill involving concentric muscle contractions. The resulting increase in exercise capacity in Chronic Obstructive Pulmonary Disease (COPD) patients has been related to physiological adaptations within trained skeletal muscle (2) in response to the biological overload. However, ventilatory constraints and locomotor muscle weakness in patients with advanced COPD may limit their participation in traditional exercise rehabilitation (3), or the extent to which their peripheral muscles may be overloaded, thus curtailing the magnitude of benefits. A need exists to develop more tailored exercise approaches or modalities for severe COPD.

Eccentric (ECC) as opposed to concentric (CON) endurance exercise has recently been proposed as an appealing alternate rehabilitation strategy for patients with low exercise tolerance (4). The rationale relates to the lower metabolic cost and associated cardiorespiratory responses associated with lengthening (ECC) compared to shortening (CON) muscle actions as well as the unique ability of ECC contractions to generate significantly greater forces than CON contractions for the same metabolic cost (4,5,6). Given the stimulus-response relationship between the force of a muscle contraction and degree of strength development, ECC exercise training may be expected to result in greater muscle strength (7,8) with a lesser overload of the ventilatory system (3,4), as compared to traditional CON exercise.

To date however, ECC exercise has not been adopted for use in patients with COPD, likely due to the common perception that such high-force contractions will cause notable muscle pain and injury (8, 9). Structural damage and delayed onset soreness are inherent characteristics of muscle unaccustomed to ECC contractions (9). However, studies in healthy individuals have shown that when ECC power is increased gradually and progressively, adverse responses are attenuated and adaptations occur to increase muscle size and strength (7, 8, 10). Given the potential training advantages, it is important to minimize the risk and extent of muscle damage and related symptoms in order for this modality to be considered as a desirable training alternative.

This implies understanding the framework for inducing biological overload through progressive increases in ECC power; however guidelines for dynamic ECC exercise prescription are generally lacking. Moreover, in contrast to conventional exercise prescription, determination of ECC exercise intensity is complicated by the inability to assess peak ECC exercise capacity due to the potential for inducing injury in muscle unaccustomed to such contractions. Thus far, only one study has applied ECC exercise as a training modality to COPD patients (11); however little information about the framework for developing and applying the exercise protocol, including absolute workloads and progression over time, was provided.

Therefore, the aim of the present study was to develop a framework for applying muscle overload using ECC cycle exercise in patients with severe COPD, and examine the related muscle tolerance and cardiorespiratory responses with a view to recommend this exercise modality for pulmonary rehabilitation purposes. In this feasibility study, a protocol of progressively increasing work rate was designed to achieve a target intensity of 60% peak oxygen consumption () attained in a concentric modality, while minimizing potential side effects and maximizing patient compliance.

MATERIALS AND METHODS

Subjects

Six male patients with severe COPD (12), without recent exacerbation, not on home oxygen or oral steroids were included in the study. Patients were excluded if they had co-morbidities that were medically uncontrolled, presented any contraindication to exercise and had participated in a rehabilitation program within the previous six months. The study was approved by the institutional ethics review board and all subjects provided informed consent.

Procedures

In an initial visit, patients underwent standard pulmonary function testing and body plethysmography (MediSoft body box 5500), a venous puncture for a baseline level of creatine kinase (UniCel DxC 800 Synchron Clinical System) and a standard CON peak incremental (5–10 Watts.min⁻¹) cycling test for determination of peak work capacity, and ventilation () (MediSoft) with constant monitoring of electrocardiogram, peripheral oxygen saturation and blood pressure. Patient ratings of perceived exertion for dyspnea and leg fatigue were assessed using the modified Borg scale (13). Maximal voluntary ventilation was predicted by 40 × forced expiratory volume in 1 sec (14). After cardiorespiratory parameters and dyspnea and leg fatigue ratings were back to baseline (>30 min after peak cycling test), a 10-minute CON submaximal cycling bout was performed to establish the workrate corresponding to 60%peak. During this assessment, and were continuously measured. These tests were performed on the same cycle ergometer used for ECC exercise, but in the forward (CON) pedaling modality.

Eccentric Exercise Protocol

A custom-built, recumbent cycle ergometer (Strasbourg, France) allowing for both CON and ECC pedaling and thigh muscle recruitment was used. For ECC exercise, an electric motor drives the pedals in a reverse direction from conventional pedaling, while the patient attempts to slow down the moving pedals to achieve a predetermined power (5). Direct visual feedback about maintaining pedaling frequency of 60 rpm and measured mechanical power output are provided through computer software.

The protocol was designed to have patients achieve a target intensity of 60% CONpeak within 15 sessions (20 minutes per session, 3 times per week), with gradual and progressive increases in ECC power each session. To estimate the ECC power that would correspond to the target intensity for each patient, we drew upon previous reports in healthy subjects (5, 6) where power was approximately 4 times higher in ECC compared to CON cycling for the same and used this similar factor to multiply with the power obtained from the 60% CON cycling bout. This estimation was necessary due to the inability to directly measure peak ECC cycling workload without prior ECC-induced muscle adaptation. The ECC cycling intensity was confirmed through weekly assessments of during a 10-min ECC steady state exercise bout, along with measurement of , heart rate (HR) and peripheral oxygen saturation (SpO₂).

For the first session in each patient, ECC cycling was performed at a minimal power of 10 Watts for familiarization. Thereafter, the protocol was to increase power every session by 5 to 10% of the estimated target power of each patient, respecting the muscle soreness reported before each exercise session and on the patient's ECC cycling motor coordination capacity. Each exercise session was carried out at the same time of day separated by 2–3 days of recovery. HR, SpO₂, blood pressure and Borg ratings were continuously assessed during each session. Throughout the 5-week study period, possible side effects were assessed by plasma creatine kinase (CK) levels and muscle soreness, reported in 10-cm visual analog scale (15).

Figure 1  ECC power (black squares) was progressively increased over the course of 5 weeks, while heart rate (presented as % peak achieved in the incremental peak CON exercise test) measured during a 10-minute steady state ECC exercise remained fairly constant (p > 0.05). The target intensity (not shown) corresponding to 60% peak CON

was achieved between 3 and 5 weeks for all patients. Data for each week represent the average of up to 3 exercise sessions per patient. Error bars = 1 SD. * = Different from Week 1; † = Different from Week 2; ♮ = Different from Week 3. # = Different from week 4 (p < 0.05, Friedman for repeated measurements).

Table 1  Patient group mean ± standard deviation of serum creatine kinase levels, muscle soreness, leg fatigue and dyspnea measured each week

	Week
Measurement	1	2	3	4	5
CK (U.L^−1)*	118 ± 51	110 ± 77	116 ± 35	121 ± 67	113 ± 42
Muscle soreness (VAS 0–10)	1.2±2.1	1.7 ± 2.1	2.1 ± 2.3	2.2 ± 2.3	1.6 ± 1.8
Leg fatigue (Borg 0–10)	0.9 ± 0.9	1.8 ± 1.7	2.6 ± 2.1	2.9 ± 2.0	2.8 ± 2.0
Dyspnea (Borg 0–10)	0.7 ± 0.7	1.3 ± 1.4	1.8 ± 1.5	2.2 ± 2.0	1.7 ± 1.7

CK: Creatine Kinase; VAS: Visual Analog Scale.

*Normal reference range: 5–140 U.L⁻¹

RESULTS

COPD patients (n = 6) were on average 63 (range 54–71) years of age with severe airway obstruction, forced expiratory volume in 1 sec of 35 (range 17–49)% predicted. They presented significant pulmonary hyperinflation with functional residual capacity of 195 (range 149–259)% predicted and reduced diffusion capacity with diffusion lung capacity for carbon monoxide of 48 (range 33–65)% predicted. Peak power achieved in the CON peak test was 73±29 (range 35–110) watts. The symptom limiting peak CON exercise was shortness of breath in 4 patients, 3 of whom presented a drop in oxygen saturation below 90%, and a combination of leg fatigue and dyspnea in the other 2. Five patients were ventilatory limited at peak exercise, presenting ventilatory reserve less than 9 L.min⁻¹.

As can be seen in Figure 1, over the course of 5 weeks ECC power was progressively increased, with an average 30-watt increase per week, reaching an average of 146 ± 55 Watts (ranging from 65 to 244 Watts) by the last exercise session. Thus by 5 weeks, the power was increased to yield on average a 7-fold higher workrate relative to baseline. These weekly increases in power were achieved while maintaining the heart rate response at approximately 85% of peak heart rate (Figure 1). All patients reached the target intensity and duration; this was achieved between the fourth and fifth weeks in 4 of the 6 and in week 3 for the other 2. These two patients were able to reach intensity levels higher than our target at the end of the 15 sessions.

The progression in power was not associated with an increase in serum CK levels, as seen in Table 1. CK remained within the normal range throughout the study except for one patient who showed minimally elevated values at baseline (215 U.L⁻¹) and during ECC exercise (243 U.L⁻¹, normal laboratory standard < 140 U.L⁻¹). Most patients reported some muscle soreness and leg fatigue, but this did not compromise the progression in ECC power. Only one patient scored 10 on the visual analog scale for muscle soreness at 2 different time points during the first 6-sessions; however, these 2 scores were likely influenced by other factors as they decreased rapidly by the next session and were associated with normal CK. Dyspnea scores were on average <3 and oxygen saturation higher than 90% (data not shown).

All patients attended 100% of the training sessions, except for one patient who missed 2 sessions for reasons unrelated to health status or the exercise. In general, patients did not demonstrate motor coordination difficulties during ECC cycling, except for one patient at higher workrates (>176 Watts) although this did not prevent the progression in power for subsequent sessions.

Considering the ventilatory data obtained over the 5 weeks, the median (25^th-75^th percentiles) for breathing reserve was 24 (17–27) L.min⁻¹ showing that in 75% of the observations, patients had a breathing reserve higher than 17 L/min. Moreover, in the final week, the breathing reserve was greater than 15 L.min⁻¹ in 4 patients, with low levels of breathlessness (Borg score on average 2) reported in all.

Finally, comparison between CON and ECC exercise at 60% peak (0.63 ± 0.2 vs 0.62 ± 0.2 L.min⁻¹, respectively) showed that (29 ± 8 vs 27 ± 6 L.min⁻¹), ventilatory reserve (16 ± 9 vs 18 ± 9 (L.min⁻¹) and breathing frequency (25 ± 7 vs 25 ± 6 breaths.min⁻¹) were not statistically different (p > 0.05). This is particularly notable given that the mechanical power output at this metabolic intensity was on average 5 times higher during ECC compared to CON exercise (124 ± 74 vs 23 ± 17 Watts) (p = 0.02).

DISCUSSION

The main finding of this study was that patients with severe COPD could safely tolerate and comply with an ECC cycling protocol based on progressive increases in power. All patients achieved the target intensity of 60% peak within 15 sessions by exercising 3 times per week for 20 minutes. The progression in eccentric power resulted in patients achieving relatively high workloads for this population compared to those typically achieved in traditional cycling exercise. Creatine kinase levels remained within the normal range or were only slightly elevated. Although some muscle soreness was reported in most patients, it did not compromise ECC power progression. Furthermore, patients presented tolerable levels of leg fatigue and dyspnea.

The ECC cycling protocol proposed in this study was developed as a framework to avoid muscle injury and soreness such that COPD patients could subsequently participate in an ECC exercise training program. It has been shown in healthy subjects that such gradual and progressive increases in ECC cycling power could attenuate adverse responses and produce significant gains in muscle strength with minimal muscle soreness (7). Our study demonstrated that this approach could also be successfully applied to patients with severe COPD while preventing side effects.

A challenge to the development of an ECC exercise protocol for any clinical population is determination of the intensity component because of the inability to have patients perform an ECC peak incremental test prior to muscle adaptation. Therefore, because ECC peak power cannot be determined at baseline, a percentage of peak oxygen consumption (60%) achieved in the peak CON cycling test was chosen as the index to establish intensity and the corresponding ECC power was estimated as 4 times the power achieved at this intensity, as previously reported in healthy subjects (5, 6). This intensity was selected based on the fact that it has been safely applied in an ECC cycling protocol for cardiovascular disease patients (16), and it is generally considered sufficient to elicit physiological training effects in traditional rehabilitation using CON cycling (17). However, it was not the intention of this study to limit in any way the ECC intensity reached; in fact, in some patients, intensities reached during the final exercise sessions were as high as 88% CONpeak. Based on the response of our subgroup of severe COPD patients to the ECC protocol, 60% CONpeak can be recommended as an intensity for subsequent ECC training studies aimed at inducing physiological adaptation.

In our assessment of ventilation, a similar was observed between CON and ECC cycling at similar , which has previously been reported in healthy subjects (18). In terms of breathing frequency however, disproportionate increases have been reported during ECC compared to CON cycling in healthy subjects (19). This raises the question that ECC exercise might have deleterious consequences for patients with respiratory conditions (4, 19), as it could augment dynamic hyperinflation and breathlessness. Our findings do not support this suggestion, as our patients were able to cycle eccentrically at work rates 5 times higher than CON submaximal work rates while achieving similar breathing frequencies. Additionally, the ECC power achieved by the end of 15 sessions did not induce ventilatory limitation, as most patients showed breathing reserve greater than 15 L.min⁻¹ with minimal breathlessness reported.

CONCLUSION

Our study showed that an ECC cycling protocol based on progressive increases in power aimed to achieve an intensity known to produce physiological muscle adaptation, can be performed by patients with severe COPD with no side effects and high compliance. Our results warrant study of a larger group of patients over a longer duration to establish whether such high workloads can be sustained and translated into improved biological, physiological and functional outcomes. This preliminary report suggests that ECC cycling may be a feasible approach for exercise rehabilitation in patients with severe COPD.

DECLARATION OF INTEREST

The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.

ACKNOWLEDGMENTS

We would like to thank Carmen Darauay for technical assistance and the COPD patients for their time and participation.