Individualized and tailored exercise training is an essential part of disease management and rehabilitation in people with chronic obstructive pulmonary disease (COPD) (24). Regardless of the type of exercise performed, achieving optimal training stimulus at the muscle level could be challenging in this group of individuals because ventilatory limitation and dyspnea may occur before contracting muscles being sufficiently stressed (15,20,39). Partitioning the exercising muscle mass, for example, by exercising a single-limb (SL) at a time, is one strategy that could be used to reduce the extent to which ventilatory limitation hinders the ability to reach sufficient exercise stimulus and to optimize the effects of exercise training in people suffering from COPD (12). The concept of partitioning exercise in COPD was introduced by Richardson and colleagues (39) who found greater muscle specific work after a SL knee extension (KE) exercise compared with a conventional two-legged cycle exercise. Greater muscle-specific work have also been demonstrated comparing SL with whole-body exercises during continuous and interval aerobic cycling training in people with COPD (5,12). In addition to greater muscle specific work, Dolmage and Goldstein (12) showed that training one leg at a time produced further improvement in aerobic capacity compared to two-legged cycle training. In a similar way, Bjorgen et al. (5) demonstrated a higher increase in peak oxygen uptake after one-legged compared with two-legged interval training. Thus, partitioning exercise may play an important role during aerobic exercise training in people with COPD, allowing higher muscle specific exercise stimulus as well as larger physiological effects.
The potential effects of partitioning exercise during other exercise modalities, such as resistance training, have not been thoroughly documented. Resistance training is an important part of exercise training for people with COPD because impaired muscle strength and/or endurance is common in this population (13,22,46). In COPD, the vast majority of resistance training studies have focused on increasing limb muscle strength using high load/moderate number of repetitions (e.g., initial loads at 60%–70% of one repetition maximum [RM] with 8 to 12 repetitions per set) (32). Improving limb muscle strength is relevant because muscle weakness is common among people with COPD and because it is related to exercise intolerance, morbidity, mortality as well as dyspnea, and poor quality of life (11,16,26,47,49). However, decreased limb muscle endurance is also evident in COPD (13,45), often reported to a larger magnitude than muscle weakness and related to physical inactivity as well as altered lung function in this group of people (45,52). Limb muscle endurance also seems to be more closely related to walking capacity than limb muscle strength in people with COPD (30). Therefore, improving limb muscle endurance in people with COPD has been highlighted as an important therapeutic goal of COPD rehabilitation (13). If the goal is to improve limb muscle endurance, the American College of Sport Medicine (ACSM) recommends using low load/high repetition resistance training (3). The available literature on low load/high repetition resistance training in COPD is scarce, but we have previously found that this resistance training modality could improve walking capacity, arm function, limb muscle strength as well as limb muscle endurance while avoiding the occurrence of limiting exertional symptoms in people with moderate to severe COPD (28). In this previous study, all resistance exercises were performed using an SL at a time with the objective of minimizing the load on the ventilatory system (6). However, because the comparison group did not perform any exercise, it could not be determined if SL execution of low load/high repetition resistance training was more beneficial than if a larger amount of muscle mass had been involved, for example, when exercising both arms or both legs simultaneously. To our knowledge, no previous study has compared the physiological responses of SL versus two-limb (TL) resistance exercises in people with COPD, regardless of the goal of the resistance training performed (i.e., increasing limb muscle strength or endurance). Even though an SL-KE exercise was used in the study by Richardson and colleagues (39), the exercise involved cycle ergometry in accordance to aerobic and not resistance training principles (3,39).
To investigate the potential benefits of partitioning exercise during low load/high repetition resistance training in people with COPD, we aimed at comparing SL to TL quadriceps resistance exercises with regard to 1) total work performed, 2) exertional symptoms, and 3) muscle fatigue in people with COPD and healthy controls. We also aimed at comparing total work and exertional symptoms between SL and TL in COPD and controls during low-load/high-repetition elastic resistance exercises involving the lower as well as the upper limbs (29). Comparison of SL and TL upper extremity exercises is of specific interest because the concept of partitioning exercise has mainly been examined on the lower limbs (5,12,39). The elastic resistance training protocol (29) used in the present study was designed in accordance to the (ACSMs recommendations for increasing limb muscle endurance (3). It is considered clinically applicable in people with COPD and has previously resulted in increased limb muscle strength as well as limb muscle endurance in these individuals (1,27,28,31). We hypothesized that, in ventilatory-limited people with severe to very severe COPD, SL execution of the load/high repetition resistance exercises would lead to larger localized total work, lower dyspnea ratings as well as larger amount of quadriceps muscle fatigue in comparison to TL. In contrast, in healthy controls, who are not ventilatory limited, partitioning exercise with SL exercises would not modify the amount of work performed, dyspnea ratings, nor muscle fatigue compared with TL.
The study was performed at the Institut Universitaire de cardiologie et de pneumologie de Québec, Université Laval, Canada. The research protocol was approved by the local ethics committee (CER:21111) and registered at www.clinicaltrials.gov (NCT02283580). Recruitment and data collection was performed from November 2014 to July 2015. All the participants signed a written informed consent before enrolment in the study.
Detailed description of the study procedure is provided in Table 1. In brief, eligible participants performed three visits. Each visit was separated by at least a 48-h rest period. Assessment of level of physical activity, anthropometric measurements, pulmonary function, isokinetic SL and TL KE, and multiple RM testing was performed on the first visit. The second and the third visits consisted of a high-repetitive SL or TL elastic band resistance training protocol that included six upper and lower limb exercises that were always administered in the following order for both the SL and TL: latissimus rowing (ROW), leg curl (LC), elbow flexion (EF), chest press (CP), shoulder flexion (SF), and KE (Table 1). SL or TL execution of exercises were randomized, i.e., if SL execution of resistance exercises were performed on the second visit, TL execution of exercises were then performed on the third visit, and vice versa. In addition, assessment of quadriceps muscle fatigue induced by SL or TL execution of KE was determined by measuring isometric quadriceps muscle force and potentiated twitch force before (baseline) and 15 min after the KE elastic band exercise.
Eligible people with COPD were 40 yr or older, had a cumulative (current or past) smoking history of > 10 pack years and a postbronchodilator forced expiratory volume in 1 s ≤ 50% predicted (37). They were excluded if they had a recent COPD exacerbation (<6 wk), neuromuscular, and/or orthopedic disorders that compromised participation to testing, recent cancer, unstable cardiac disease and cardiac stimulator, current asthma, low body weight, or obesity (body mass index [BMI] < 20 or > 30 kg·m2), resting O2-pulse saturation < 85% or a daily dose > 10 mg of systemic prednisone. Healthy controls were sedentary as defined by a Voorips score < 9 (36), were 40 yr or older, had normal pulmonary function, and did not suffer from neuromuscular and/or orthopedic disorders compromising participation to exercise.
Based on a study by Rossman et al. (40), a sample size of 11 people with COPD and 11 controls were considered sufficient to detect a relevant mean difference of 11% (±9) in quadriceps muscle contractile fatigue between SL and TL exercises, with α = 0.05, β = 0.20 (80% power), and a two-tailed test of significance. As we expected larger variations with COPD and considering that there was a planned comparison between COPD and healthy controls, we aimed to recruit at least 15 participants in each group.
Physical Activity, Pulmonary Function Anthropometric Measurements
Level of physical activity was assessed with the Voorips physical activity questionnaire which is validated for elderly individuals (37) and applied to people with COPD (10,14,38). Participants then completed pulmonary function assessment (plethysmography, spirometry) while being on their usual bronchodilator therapy, in accordance to testing guidelines (4) and related to predicted normative values (36). Anthropometric measurements included height and weight assessment and body composition by bioelectrical impedance (InBody520, Body Composition Analyzer; Biospace, Seoul, Korea).
Exercise Workloads and Quadriceps Muscle Fatigability
Total work (newton-meters, N·m) was assessed during isokinetic SL and TL KE using the Biodex Multi-Joint System 4 (Biodex Corp., Shirley, NY). A specialized attachment was created to allow bilateral KE. Five submaximal repetitions were performed as warm-up and to familiarize with equipment and exercise movements. The range of knee displacement was between 90° and −5° for all tests. Isokinetic testing consisted of 25 maximal KE performed at an angular velocity of 60°·s−1 once with the right leg, once with the left leg, and once with both legs simultaneously. Test order was randomized using a computer random number generator (www.randomization.com). A 15-min rest period was allowed between each test (29). SL workload was defined as the total workload achieved by the left and right legs together, whereas TL workload was defined as the total workload achieved when using both legs simultaneously. In addition to total work was peak torque from the highest contraction obtained for SL and TL.
Total work comparing SL with TL was also assessed during six low load/high-repetition elastic band resistance exercises (ROW, LC, EF, CP, SF, and KE). Five different elastic bands (Thera-Bands; The Hygenic Corporation, OH) with progressively increasing resistance from yellow (thin), red (medium), green (heavy), blue (extra heavy), and silver (super heavy) were used in this study to perform these exercises. Depending on the strength of the participant and the exercise performed, the elastic bands were used alone, or jointed together in different combinations to achieve the desirable load. Identical combinations of elastic bands were attached to each limb separately during SL and TL, respectively. A modified brace was used to fasten the elastic bands to the exercised limb(s), positioned just proximally of the medial/lateral malleolus for lower extremity exercises, whereas, for upper extremity exercises, the elastic bands were fastened using the modified brace just proximally of the wrist of the participant. The other end of the elastic bands were connected to a strain gauge (Biopac, CA) to measure the force of the contractions. The range of motion during all elastic exercises was standardized across SL and TL conditions, and participants were positioned so that the elastic resistance bands were stretched 100% at the end of movement for each exercise separately. Three sets of each exercise were performed with 1 min of rest between sets and 2 min of rest between exercises. Each set was performed until task failure at a rate of 30 contractions per minute (controlled by a metronome) with 1 s in the concentric and eccentric phase, respectively. Loadings used during both SL and TL execution of exercises were determined by a multiple RM test that was performed during the first visit and executed in accordance to recommended guidelines (50). Exercise loadings, targeted number of repetitions performed, repetition velocity, and rest periods were standardized in accordance to recommended guidelines for increasing limb muscle endurance (3) using a resistance training setup that has previously been found to be effective and feasible in people with COPD (27,28,48). Localized workloads for elastic exercises were expressed in kilograms and were calculated by multiplying elastic resistance (tension of the elastic band) by the total number of repetitions performed. SL workload was defined as the total workload achieved by the left and right legs together, whereas TL workload was defined as the total workload achieved when using both legs simultaneously.
Assessment of quadriceps fatigue
Evaluation of muscle fatigue during the elastic exercise protocol was chosen over the isokinetic protocol because it is of greater clinical relevance considering the limited availability of isokinetic equipment outside of research. Before and 15 min after the last elastic exercise (KE), isometric KE strength was assessed on the dominant leg by measuring the maximum voluntary isometric contraction (MVC) and the potentiated twitch force (Qtwpot) from a series of twitches induced by femoral nerve magnetic stimulation (Magstim 200 monopulse Bistim; Magstim Co. Ltd., Whitland, Dyfed, Wales, United Kingdom) (34,40). The occurrence of quadriceps fatigue was quantified by measuring the fall in both MVC and Qtwpot 15 min after elastic KE. A 15% or more drop in baseline Qtwpot measurements indicated the occurrence of fatigue of the quadriceps muscle (42). During the measurements, participants were seated in a recumbent chair (N-K 330 Exercise table; N-K Products, Elsinore, CA) with a knee joint angle of 90° and the ankle attached to a strain gauge (Biopac). A set of three MVC and three potentiated twitches were performed at 100% stimulator output. Qtwpot was obtained 5-s after MVC defined as the peak of the strongest contraction. Verbal encouragements were provided during these maneuvers.
Dyspnea and leg fatigue were measured during both isokinetic and elastic exercises using the modified Borg scale (0–10) of perceived exertion as commonly and reliably used in people with COPD (19,23,28). Ratings were performed after completion of each isokinetic or elastic exercise. For elastic exercises, mean ratings of the three sets performed for each limb are reported.
Descriptive statistics are reported for subject characteristics, isokinetic and elastic total work, dyspnea, and leg fatigue ratings and quadriceps muscle fatigue. Data are expressed as mean ± standard deviation if otherwise not stated. Percentage differences are presented as the mean of individual differences between SL and TL. Within-group and between-group comparisons were performed using Wilcoxon signed-rank test and Mann–Whitney U test, respectively. Spearman correlations were performed to examine the association between differences in work and differences in postexercise Qtwpot between SL and TL exercises. Quadriceps fatigue was not assessed for two people with COPD and two controls because of participant’s refusal or technical problem with magnetic stimulation. A level of 0.05 was considered valid for statistical significance. For data management and statistical analysis, the IBM Statistical package for Social Science (SPSS) version 23.0 was used.
Baseline characteristics of the two groups are outlined in Table 2. People with COPD and healthy controls were similar with regard to age, sex, BMI, amount of fat-free mass, and level of physical activity, with both groups considered sedentary, i.e., Voorips score < 9 (P > 0.05). People with COPD had, on average, severe airflow obstruction (forced expiratory volume in 1 s 38% predicted).
Quadriceps muscle function—localized exercise workloads and exertional symptoms
SL and TL isokinetic peak forces were higher among healthy controls than in people with COPD (P < 0.05, Fig. 1A). In COPD, individual mean difference in total work during SL isokinetic and elastic KE was 17% ± 31% and 24% ± 18% higher than during TL, respectively (P < 0.05) (Fig. 1B, Table 3). Despite higher localized workloads during isokinetic and elastic SL than TL KE, dyspnea and muscle fatigue ratings were similar between the two exercises (P > 0.05) (Figs 1C and D, Table 3). In contrast, no difference was found between SL and TL with regard to total work (Fig. 1B), muscle fatigue perception, or dyspnea perception in healthy controls (Fig. 1C and D, Table 3) (P > 0.05).
Neuromuscular function and quadriceps fatigue
Fifteen minutes postexercise, MVC and Qtwpot of the dominant leg were significantly reduced from preexercise values in both groups after both SL and TL (P < 0.05) (Fig. 2A and B). The fall in Qtwpot was significantly greater after SL compared with TL in COPD, suggesting greater quadriceps muscle fatigue after SL-KE. The differences Qtwpot fall between SL and TL was higher in COPD compared with controls (−7.7 ± 5.2 vs −2.0 ± 7.3, P = 0.012). The reduction in MVC was numerically larger after SL-KE than after TL-KE among people with COPD, but this did not reach statistical significance (P = 0.061) (Fig. 2A and B). The proportion of people with COPD who were considered as fatiguers was larger after SL-KE than after TL-KE (83% ± 38% vs 50% ± 51%, respectively, P = 0.010). No difference was seen among healthy controls when comparing exercise conditions with regard to the fall in MVC or Qtwpot occurring during exercise (P > 0.05) (Fig. 2A and B). Differences in work performed during SL-KE and TL-KE correlated with the between-conditions differences in Qtwpot 15 min postexercise (r = 0.438, P = 0.018; Fig. 3).
Elastic exercises—localized exercise workloads and exertional symptoms
In people with COPD, exercise workloads were also higher during SL than during TL for ROW (mean of individual differences between SL and TL expressed in % of TL total work (17% ± 23%), LC (23% ± 21%), EF (19% ± 26%), CP (14% ± 15%), and SF (33% ± 24%) (all P < 0.05) (Table 3). Even though higher localized workloads were reached during SL, muscle fatigue ratings were similar as those reached during TL during all exercises, whereas dyspnea ratings were similar for LC but lower during ROW, EF, CP, and SF (P < 0.05). In contrast, in healthy controls, partitioning exercise with SL elastic exercises did not modify workload nor dyspnea or muscle fatigue perception compared with TL (Table 3).
The novel findings of this study are that performing low load/high-repetition resistance exercises using an SL at a time allowed higher localized exercise workloads during both upper and lower limb resistance exercises in people with severe to very severe COPD, with similar or lower level of exertional symptoms than during TL exercises. SL-KE also resulted in larger amount of quadriceps fatigue when compared with bilateral KE. In contrast, partitioning exercise did not modify workload for each exercised limb, exertional symptoms, nor quadriceps muscle fatigue in healthy controls who were similar to COPD participants in terms of age, sex, BMI, muscle mass, and physical activity.
Localized exercise workloads and exertional symptoms
Partitioning exercise allows higher muscle specific workloads compared with whole-body exercises during continuous and interval aerobic cycling training in COPD (5,12) (39). To our knowledge, the present study is the first to demonstrate that the principles of partitioning exercise also apply to low load/high-repetition resistance training of the lower and upper extremities in this group of individuals. Considering that people with COPD may experience shortness of breath when using upper extremity muscles (9,25), the possibility of optimizing training programs for these muscles should not be neglected. Further, as the physiological benefits of exercise training are directly related to the magnitude of the training stimulus, the markedly increased localized exercise workloads (range, 14%–33%) obtained during SL resistance exercises have the potential to enhance the effectiveness of exercise training in people with COPD (39). This may be clinically relevant considering that the benefit of exercise training may be suboptimal in up to a third of the COPD population (51). Even though larger localized workloads were obtained during both lower and upper limb SL exercises among people with COPD, exertional symptoms (dyspnea and muscle fatigue ratings) were similar between conditions for lower body exercises, whereas dyspnea ratings were lower for upper body exercises. The difference in dyspnea perception between SL and TL in COPD is likely to be clinically important because dyspnea is a major exercise-limiting symptom in this disease (8). Allowing people with COPD to exercise with less breathing discomfort may improve acceptance (35) and adherence to pulmonary rehabilitation (37).
Quadriceps muscle fatigue
People with COPD exhibit susceptibility to limb muscle fatigue that is multifactorial in origins, being mediated intrinsically, within the muscle, by factors, such as poor oxidative capacity and reduced capillarization (44) and, to a lesser extent, by reduced blood flow and oxygen delivery to the contracting muscle (2). When compared with healthy control subjects, the fall in quadriceps strength for a given workload is larger in people with COPD (21). However, when allowed to reach their own peak exercise capacity, people with COPD and healthy controls show similar fall in quadriceps strength (43). Consistent with this last notion, we found that the fall in quadriceps strength after isometric KE was of similar magnitude in COPD and controls, but at much lower workloads in the former group, again illustrating greater susceptibility to fatigue in COPD. Although investigating the sources of muscle fatigue in COPD was beyond the scope of the current study, the observed relationship between the greater decline in Qtwpot with SL with the variations in localized workloads between SL and TL KE support the view that the amount of work performed contributed to muscle fatigue. Further, the larger amount of muscle fatigue after SL could also be explained by a lower amount of inhibitory feedback on the central motor drive allowing to reach larger muscle activation during SL in comparison to TL KE (40). A larger fraction of people with COPD (83% vs 50%) were considered fatiguers after SL-KE than after TL-KE. This is of clinical interest because the development of quadriceps muscle fatigue in COPD has been linked to greater training benefits (7). Along those lines, greater degree of muscle fatigue is likely to be associated with more profound intramuscular metabolic disturbances which may favorably translate into greater limb muscle adaptability to exercise training (40).
To minimize any bias that may be associated with the absence of blinding, we used standardized instructions and testing procedures including standardization of position, range of motion, as well as of repetition velocity. We decided to use a low-load/high-repetition resistance training protocol, designed in accordance to exercise recommendations for increasing limb muscle endurance (3), and that was previously found effective and feasible in COPD (27,28,48). Whether similar effects would also be seen in other types of resistance training approaches (such as those focusing on gaining strength) remains to be determined. Our training modalities were evaluated in people with severe ventilatory limitation, and the results may not be generalizable to milder forms of COPD.
We did not investigate potential mechanisms of exercise limitation factors such as cardiopulmonary and muscle physiological limitations during SL and TL high-repetitive resistance training. Some evidence suggests that despite increased ventilatory requirements during high-repetitive resistance exercises, ventilatory limitation does not seem to be the main exercise limiting factor if it is performed using a SL approach (17). However, the magnitude of the ventilatory demand when performing high-repetitive exercises using a TL approach remains to be determined. The higher exercise workloads, as well as the larger amount of muscle fatigue, reached during SL compared with TL resistance exercises in people with COPD in the present study, suggest that the amount of muscle mass involved during TL exercises might play a role in limiting exercise during low load/high-repetition resistance training in this group of people. For example, it is conceivable that involving a smaller muscle mass during SL may result in a lower demand on the respiratory system, minimizing dynamic hyperinflation in comparison to TL exercises. Reducing ventilatory demand during SL, by delaying the exhaustion of ventilatory capacity, would allow people with COPD to reach higher exercise workloads during resistance training (8). In addition to involving a lower amount of muscle with the consequent reduced metabolic requirements, a lower ventilatory response during SL exercises could also be explained by a decreased stimulation of muscle metaboreceptors (decreased activation of group III/IV muscle afferents) when involving a smaller amount of muscle mass, reducing the impact of the metaboreflex on ventilation (18,33). Consistent with this interpretation, activation of group III and IV skeletal muscle afferent fibers has been shown to contribute to differences in exercise tolerance and quadriceps muscle fatigue between SL and TL exercise conditions by reducing the amount of inhibitory feedback to the central nervous system leading to reduced central fatigue (40,41). However, in the absence of ventilatory measurements, these hypotheses cannot be substantiated. In contrast to previous research, we found no difference in exercise workloads and quadriceps muscle fatigue between SL and TL among the healthy controls. We suggest that this could be explained by the fact that healthy controls were able to accommodate the additional metabolic and ventilatory requirements during TL and, as such, had the ability to exercise at the similar localized workload during TL than during SL. However, based on the work of Rossman et al. (40) who reported a significant difference in quadriceps muscle fatigue when measurements were performed 2 min after end of exercise, compared with 15 min in the present study, we acknowledge that we might have underestimated the fall in quadriceps strength after SL and TL by quantifying it 15 min postexercise. This timeline was selected because we have previously used this approach with success in the investigation of muscle fatigue in people with COPD (7,42). Also, given the complexity of the measurements and the reduced mobility of this older population, performing the measurements 2 min postexercise would have been challenging. Even though Rossman et al. (40) used a KE exercise in their study, it was performed using a cycle ergometry in accordance to aerobic and not resistance training principles (3,39). Because exercise adaptations are specific to the stimuli applied, similar responses should not necessarily be expected when comparing SL with TL using either aerobic or resistance training modalities, even though the targeted muscles are the same. Thus, to fully understand the impact of potential exercise limiting factors during low load/high repetition resistance training in people with COPD, further investigation providing thorough cardiopulmonary and muscle physiological measurements would be required.
Partitioning exercise during low-load/high-repetition resistance training enabled larger localized exercise workloads as well as larger amount of quadriceps muscle fatigue with similar or lower level of exertional symptoms in people with severe COPD. This is at variance to what was found in healthy controls in whom SL resistance exercises did not allow reaching greater localized workload in comparison to TL exercise. These findings may have implications for the design of resistance training programs in COPD.
The work was funded with grants from the CIHR/GSK Research Chair on COPD, Université Laval, The Swedish Heart and Lung Foundation and The Fonds de recherche du Québec-Santé (FRQS). The authors would like to thank Dominique Auger for recruitment of patients.
F. M. reports grants and lecture fees from Boehringer Ingelheim, GlaxoSmithKline and Novartis. F. M. holds a CIHR/GSK research Chair on COPD at Université Laval. The results of the present study do not constitute endorsement by ACSM.
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Keywords:© 2016 American College of Sports Medicine
DYSPNEA; MUSCLE ENDURANCE; EXERCISE TRAINING; ISOKINETIC; MUSCLE FATIGUE