Chronic obstructive pulmonary disease (COPD) is a major cause of morbidity and mortality worldwide. The international prevalence of Global Initiative for Chronic Obstructive Lung Disease (GOLD) stage 2 and higher COPD is estimated to be 10%, a figure that is steadily increasing.1,2 COPD is estimated by the World Health Organization to be the third leading cause of death in 2030.3 Although COPD is characterized by chronic airflow limitation, limb muscle dysfunction is a common consequence and a major systemic manifestation in COPD.4–6 Limb muscle dysfunction is associated with important clinical outcomes such as increased mortality,7,8 reduced quality of life,9 greater healthcare utilization,10 and exercise intolerance,11–13 independently of lung function impairment. Exercise intolerance is considered one of the key disabling factors in COPD with dyspnea and leg fatigue being the most frequently reported exercise limiting symptoms.4,14 Clinical manifestations of limb muscle dysfunction in COPD include muscle atrophy, weakness, reduced endurance, and/or greater muscle fatigability.4 Assessment of limb muscle mass and limb muscle function in COPD is therefore highly encouraged and improving this common feature of COPD is an important therapeutic goal.6,15

This article provides clinicians and health-care professionals with an overview and description of the various exercise modalities used within pulmonary rehabilitation (PR) to improve limb muscle function, especially highlighting effective modalities at the muscle level. Our objective is to provide guidance and recommendations to help clinicians’ design optimal limb muscle training during PR for patients with COPD.

Limb muscle dysfunction encompasses muscle weakness, reduced endurance or greater muscle fatigability.15 Prevalence rates of muscle weakness ranges from 20 to 40% depending on disease severity,16 while reduced limb muscle endurance and muscle fatigue occur in 30–80% of patients with COPD.6,17,18 The impairment in limb muscles function in COPD is heterogeneous with strength and endurance of upper limbs seemingly more preserved than those of lower limbs.6,19–21 Decreased limb muscle strength and endurance, especially when involving lower limbs, are associated with reduced walking capacity22 and physical activity,13,20,23 exercise intolerance,11,24 morbidity, mortality as well as increased health care service use, dyspnea and poor quality of life.8,10,9,25 Lower limb muscles of patients with COPD also exhibit a greater susceptibility to fatigue than that of age-matched healthy individuals.13,26 Limb muscle dysfunction is the end result of several muscle structural, molecular and cellular alterations which are summarized in Fig. 1 and include weakness, atrophy, fiber-type distribution shifts, reduced oxidative capacity, mitochondrial dysfunction, and reduced capillarisation that are mediated by numerous etiological factors.6,27,28 These include sedentarity, poor nutritional status, repeated COPD exacerbations and systemic use of corticosteroids.5 Other relevant etiological factors include cigarette smoke, hypoxia, hypercapnia and acidosis, metabolic alterations of several types including vitamin D and testosterone deficiencies, systemic inflammation and co-morbidities.5,6,29

Figure 1.

Morphological and structural alterations reported in limb muscles in patients with chronic obstructive pulmonary disease (COPD). CS, citrate synthase; HADH, 3-hydroxyacyl CoA dehydrogenase. Reprinted with permission of the American Thoracic Society. Copyright © 2016 American Thoracic Society.

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In patients with COPD, limb muscle strength is a determinant of the level of physical activity30 and of functional capacity4. Moreover, muscle strength is related to dyspnea as well as to quality of life.10,8 Quadriceps muscle strength significantly predicts mortality in COPD8, while weakness is associated with impaired balance and an increase risk of falls.31 Despite its clinical relevance, muscle strength mostly reflects the action of fast-twitch fibers32 and represents only one aspect of limb muscle function.13 Limb muscle endurance, defined as the muscle's ability to sustain or repeat a specific task over time,33 and muscle fatigability, the reversible reduction in force generated by the muscle during a given task, reflect other aspects of muscle function such as muscle oxidative capacity and oxygen supply34 that are relevant to the endurance tasks that are part of daily life physical activities of patients with COPD.35,36 Limb muscle endurance is also related to walking capacity and upper limb muscle function in COPD.22 An important concept is that strength and endurance cannot be predicted from each other as they reflect different muscle properties.37 Understanding that strength and endurance are both clinically important and that they reflect different muscle properties is important in the design of rehabilitative interventions aimed at improving limb muscle function in COPD.

PR is an individualized, comprehensive and multidisciplinary approach that involves exercise training, education, psychosocial support, and nutritional interventions, in order to promote better self-management of the disease, minimize symptom burden, optimize functional status, and increase participation in activities of daily life.38–41 Body composition abnormalities (such as weight loss and muscle wasting) are prevalent in COPD.6,42 Sarcopenia has been reported in about 15% of patients with COPD and impairs function and health status of the individual patient. Patients with COPD and sarcopenia have reduced exercise capacity, functional performance, level of physical activity and health status compared with patients with COPD without sarcopenia.43 Nutritional interventions, dietary counseling, food fortification, and supplementation44,45 are recommended and may be efficient for increasing weight, fat-free mass, exercise tolerance as well as survival in compliant patients. Educational sessions should address smoking cessation, basic information about COPD and pathophysiology of the disease, general approach to therapy and specific aspects of medical treatment, strategies to help minimize dyspnea, advice about when to seek help, self-management and decision making during exacerbations, and advance directives and end-of-life issues.3,46 PR is perhaps the best example of evidence-based medicine in pulmonology as it improves, among other things, exercise capacity, health-related quality of life, as well as relieving dyspnea and fatigue.47 Risks of hospitalization, mortality,38,47 and healthcare utilization costs 48 are also reduced with PR. Although there is currently no consensus regarding the optimal duration of a PR program, the current recommendations suggest 8–12 weeks, while keeping in mind that extending this length might benefit patients who need more time to achieve clinical improvements.38,49 Even though the content of PR may vary depending on factors such as healthcare systems, resources, personnel or settings, individually tailored exercise training is considered the cornerstone of PR.47 Whole body aerobic training involving upper and lower extremities and strengthening exercises are recommended components of exercise training in patients with COPD.40 Exercise training within the context of PR is also considered one of the best available means to improve limb muscle function in COPD, demonstrating increase limb muscle strength, limb muscle endurance as well as reduced fatigability.40

It is recommended that an exercise assessment be carried out before commencing PR and exercise training in order to tailor the exercise prescription to the individual's specific requirements and goals.40,50 Such an assessment should include evaluation of exercise capacity and of muscle function. Design of exercise programs should always be based on the foremost principles of exercise training, including but not limited to, the principles of specificity, progressive overload and variation51 (Table 1). Firstly, the principle of specificity states that all training adaptations are specific to the stimulus applied.52 Second, the above discussion about muscle strength,53 endurance and fatigability implies that specific interventions are required to address these different aspects of muscle function. Lastly, specific aims of the training should be kept in mind in designing the program.

If the goal of exercise training is to improve specific aspects of limb muscle function such as strength and endurance, resistance training should be preferred over other available exercise modalities within PR. Resistance training protocols seem superior to aerobic training protocols with regard to increasing limb muscle function, especially limb muscle strength, in patients with COPD.37,40,52,55,60–62 Other exercise alternatives such as high-frequency NMES are feasible, especially in more severe patients,72 but more studies are needed to compare their effects with those of traditional exercise training protocols.

The requirements for improving limb muscle strength or endurance are different and this has serious implications for the exercise training approach to be used for optimal benefits. The exercise programs should be built on the founding principles of exercise training (progressive, overload, specificity and variation) (Table 1) and individualized and adapted to the specific goals of treatment. It would seem advisable to follow ACSM recommendations40,52 for increasing limb muscle strength or limb muscle endurance (Table 2).

The vast majority of resistance training regimens, aimed at improving limb muscle function in patients with COPD has used weight machines as a primary choice of exercise equipment.62,64 However, there is a growing evidence in COPD that exercise training using minimal equipment such as body weight and/or elastic resistance bands is also effective in improving both limb muscle strength and limb muscle endurance.70,83,84 The use of elastic resistance bands is also considered clinically applicable both for patients as well as care providers and could be considered a practicable and less costly alternative to weight machines,85 that could be more easily implemented outside specialized centers. The principle of progressive overload and, to some extent, the principle of specificity have been used in resistance training regimes for patients with COPD. However, variation or periodization which could be done by systemic variations of, for example, exercise volume and intensity, is rarely incorporated. Since the body adapts quickly to exercise regimens, variations in training parameters may help to ensure continual progression and optimization of the training intervention.52 Classic, reverse or undulation variation strategies could theoretically be used, however data on patients with COPDs are lacking.40 In one study, nonlinear exercise training was found to be superior to traditional non-varied exercise training with regard to improving aerobic work capacity on cycle ergometry.86 The potential use of nonlinear periodization in resistance training for improving limb muscle function among patients with COPD is interesting, but has yet to be investigated. Since improving limb muscle strength and endurance requires different exercise approaches, a periodized exercise approach including both high load, low-repetitive (muscle strength) and low load, high-repetitive (muscle endurance) components would appear to be a promising approach in this group of patients.

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).

François Maltais reports grants and lecture fees from Boehringer Ingelheim, GlaxoSmithKline and Novartis. François Maltais holds a CIHR/GSK research Chair on COPD at Université Laval.