Exercise Training Modalities for People with Chronic Obstructive Pulmonary Disease

Abstract

Exercise training confers health benefits for people with chronic obstructive pulmonary disease (COPD). This article reviews the evidence for several exercise training modalities shown to be beneficial among individuals with COPD. These modalities include aerobic, resistance, nonlinear periodized, upper limb and balance training, as well as yoga, Tai Chi, inspiratory muscle training, whole body vibration training and neuromuscular electrical stimulation. The literature pertaining to each modality was critically reviewed, and information on the rationale, mechanism(s) of action (where known), benefits, and exercise prescription is described to facilitate easy implementation into clinical practice.

Key Words:

• Chronic obstructive pulmonary disease
• exercise
• aerobic training
• continuous endurance training
• resistance training
• interval training
• neuromuscular electrical stimulation
• balance
• yoga
• tai chi
• inspiratory muscle training
• exercise prescription

Introduction

Pulmonary rehabilitation (PR) is one of the cornerstones of the management of people with chronic obstructive pulmonary disease (COPD) (1) and individually tailored exercise training is an integral component of this treatment strategy (2). National and international guidelines recommend that the exercise component of PR includes both aerobic and resistance training (3–5). However, there is emerging evidence to also support new and alternative training modalities for people with COPD. This review article provides an overview of the traditional and less commonly used training modalities, including aerobic (continuous and interval), resistance, nonlinear periodized, upper limb and balance training, as well as yoga, Tai Chi, inspiratory muscle training, whole body vibration training and neuromuscular electrical stimulation (Table 1). The article outlines the rationale, mechanism(s) of action, benefits of and exercise prescription for each modality in order to facilitate easy implementation into clinical practice.

Table 1. Exercise training modalities for people with COPD.

Aerobic training

Continuous endurance training

Interval training

Single-leg cycling

Resistance training

Strength- or endurance- targeted

Non-linear periodized exercise

Balance training

Yoga and Tai Chi

Inspiratory muscle training

Whole body vibration training

Neuromuscular electrical stimulation

Aerobic training

The American College of Sports Medicine (ACSM) defines aerobic exercise as “purposeful exercise that involves major muscle groups and is continuous and rhythmic in nature” (6). It includes activities such as cycling, walking, swimming, dancing and can also be performed using equipment such as a treadmill or stationary bike.

Continuous endurance training

In studies that have established the efficacy of PR in the management of people with COPD, continuous endurance training of the lower limb muscles is the most commonly used aerobic training modality (7). It involves exercising for a sustained period of time at a specific intensity (8, 9).

The benefits of continuous endurance training for people with COPD are well documented and are based predominantly on studies involving cycling- and walking-based training strategies (7). Compared to walking, cycle training targets the quadriceps muscles (10) and is associated with less exercise-induced oxygen desaturation (11, 12). In contrast, walking is a functional activity that leads to greater improvements in functional exercise capacity than cycle training (13). The structural and functional changes (physiologic adaptations) associated with continuous endurance training of the lower limbs include increased cross-sectional area of all quadriceps muscle fiber types (14–16) with a reduction in the proportion of type IIx fibers (16, 17), increased oxidative capacity (17, 18), reduced exercise-induced lactic acid production (18, 19) and normalization of the decline in the ratio of inorganic phosphate to phosphocreatine during exercise (20). It is also associated with improvements in maximal exercise capacity, endurance time, dyspnea and fatigue symptoms during exercise as well as dyspnea in general (7). Continuous endurance training as part of a PR program for patients following hospital discharge after an acute exacerbation of COPD is also feasible and safe and is associated with improvements in exercise capacity and dyspnea (21).

The prescription of continuous endurance training is based on an exercise test, for example maximal cardiopulmonary exercise test (22), or an incremental shuttle walk test (ISWT) (23); a target exercise intensity is chosen based on measurement of the individual’s maximal exercise capacity. The six-minute walk test (6MWT), a measure of functional exercise capacity, is also widely used to formulate the exercise training prescription, based on target heart rate and/or metabolic equivalents (METS) (23, 24). Although the optimal prescription for continuous endurance training for individuals with COPD is not clear (25), international documents advise that the ACSM’s instructions on exercise prescription can be applied (5). Continuous endurance training should be prescribed three to five times per week at 60% to 80% of maximal work rate for 20 to 60 minutes per session (6) and can be progressed by increasing the work-rate and time as tolerated (9). A Borg CR10 (26) (dyspnea symptoms) score or Borg Rate of Perceived Exertion (27) (fatigue symptoms) score of 4 to 6 and 12 to 14, respectively, are considered appropriate target training intensities (28). If a patient is unable to exercise at the prescribed work rate intensity during the first training session, s/he should exercise at level 4 to 6 on Borg CR10 and be progressed to a higher level over time as able. Nonetheless, it is important to note that it is unclear whether high intensity continuous endurance training bestows any greater benefit in regard to peak exercise capacity or quality of life than lower intensity training (at <50% maximal work rate) in adults with COPD (29). Furthermore, the precise exercise intensity at which physiological adaptation with training occurs in patients with COPD is not known (29).

In the clinical setting, continuous endurance training can be performed using specialist gym equipment such as a treadmill, stationary bike or cross-trainer, and, in centers with minimal equipment, using a walking course. For the latter, the walking speed achieved in the 6MWT, ISWT or ESWT can be used to prescribe a specific distance to walk in a certain period of time. Even patients with severe dyspnea can benefit from walking aerobic exercise using mobility devices such as rollator walkers to reduce breathlesness (30, 31).

Interval training

Interval training provides an alternative aerobic training modality to continuous endurance exercise (32) for patients who are unable to perform or sustain high-intensity exercise due to dyspnea or fatigue (33, 34). Interval training involves repeated periods of high-intensity exercise alternated with short periods of low intensity exercise or rest (35) and is usually undertaken on a stationary bike (5).

A systematic review of eight randomized controlled trials compared the effects of interval and continuous endurance training in 388 patients with moderate to severe COPD (32). On completion of the training program, there were no significant differences between the modalities in terms of exercise capacity, peak power, change in oxygen uptake at lactate threshold, isotime dyspnea during exercise testing, dyspnea, skeletal muscle adaptation (fiber-type distribution and capillary-to-fiber ratio) and health-related quality of life (32). Despite these results, some features of interval training are not known, such as the duration of benefit and the capacity to achieve greater total work than continuous endurance training (which may lead to greater physiologic training adaptations) (5).

The decision to prescribe a continuous endurance or interval training protocol is a practical one, as both are equally effective in improving exercise capacity, dypsnea and health-related quality of life (25) although higher intensity exercise normalized for the volume of training may lead to greater physiological benefit (29). Nonetheless, interval training may be more appropriate for patients with severe airflow obstruction (forced expiratory volume in one second (FEV₁) ≤40% predicted; low exercise capacity; peak work rate ≤60% predicted; total time at a constant work rate ≤10 minutes; marked oxygen desaturation during exercise (SpO₂ ≤85%) and/or intolerable dyspnea during continuous endurance training (9).

The training prescription for interval training is usually based on a maximal cardiopulmonary exercise test performed on a stationary bike. Training should be undertaken three to four times per week at 80 to 100% of maximal work rate for 45 to 60 minutes (including rest time) per session (6). Intervals can be either 30 seconds exercise followed by 30 seconds rest or 20 seconds exercise and 40 seconds rest (9). Similar to continuous endurance training, a Borg CR10 (dyspnea symptoms) score of 4 to 6 is considered an appropriate training intensity target with training progressed by increasing the work-rate and time spent exercising (9). Similar to continuous training, if a patient is unable to exercise at the prescribed work rate intensity during the first training session, s/he should exercise at level 4 to 6 on Borg CR10 and be progressed over time accordingly.

Single-leg cycling

Ventilatory impairment, a key factor limiting exercise for many people with COPD (36), may preclude exercising at a sufficiently high intensity to induce physiological changes in limb muscle (37, 38). Single-leg cycling on a stationary bike may provide an alternative to conventional two-leg cycling by reducing the demand placed on the ventilatory system by training a small, rather than large, muscle group (i.e. one, not two, lower limbs) and thus permitting a longer duration of exercise at a high intensity (39, 40). During single-leg cycling, the “active” leg pedals whilst the “inactive” leg rests on the ergometer cross-bar (39) or box/platform away from the pedal (41). The patient alternates the “active” and “inactive” leg during the training program (42).

Three small studies have established proof-of-concept of this training modality for people with COPD and reported that it is associated with significantly greater improvements in peak oxygen uptake (V0₂) (40, 42) and endurance time (39) compared to two-leg cycling. Additionally, a pragmatic noncontrolled, nonrandomized study found that using single-leg cycling as the aerobic training modality in a PR program was found to be safe and acceptable by staff members and 75% of patients would recommend it to other patients (41). In this study, patients significantly improved peak oxygen uptake, functional exercise capacity and health-related quality of life following PR. Further investigation of this training modality is warranted to identify the optimal training protocol and to evaluate its impact on clinical, physiological and long-term outcomes.

Resistance training

Resistance training involves muscle contractions performed against a specific opposing force generated by a resistance such as body weight, free weights and weight machines (43). It is an umbrella term for training different aspects of muscle function such as strength and endurance (44).

Peripheral muscle dysfunction and its consequences (particularly of the quadriceps muscles) are well documented among people with COPD (8). In contrast to aerobic training, the clinical benefits as well as changes in muscle structure and function associated with resistance training are less well understood in patients with COPD (8). This is partly due to the lack of standardization in training protocols used in studies investigating resistance training (5). A systematic review of 18 controlled trials analyzed the effects of progressive resistance training in 543 patients with COPD (mean FEV₁ 46% predicted) (45). The training protocols included either strength or endurance resistance exercises of the arms, legs and trunk muscles, and on average patients attended two to three outpatient sessions for 12 weeks. Significant improvements were seen in muscle strength (particularly the quadriceps muscles), but the evidence for changes in skeletal muscle structure was inconclusive. Furthermore, several studies have reported that the addition of resistance training to an aerobic exercise program resulted in greater improvements in muscle strength and size compared to aerobic exercise alone (46–48). Lewis et al reported augmented expression of the components of the muscle insulin-like growth factor system and of myogenic regulatory factors following resistance training in patients with moderate to severe COPD (49) but further exploration of the alterations in muscle structure and function are required.

Despite the need for further research, resistance training, particularly of the lower limb muscles, is recommended two to three times per week for patients with COPD (5). The prescription for resistance exercise is usually based on a one repetition maximum (1RM) assessment (8), although it is important to note that due to inter-individual discrepancy this value may be under- or overestimated, and the intensity may need to be adjusted accordingly (50). For strength training, the ACSM recommends 1 to 3 sets of 8 to 12 repetitions at 60 to 80% 1RM [or 40% to 50% 1RM in older individuals (age not defined)] with 2 to 3 minutes rest between each set (44). For endurance training; 1 to 2 sets of 15 to 20 repetitions at <50% 1RM with 2 to 3 minutes rest between each set is advised (6). The subjective experience of strength and endurance training should be moderate to hard, and light to moderate respectively (6). Resistance exercise is progressed by increasing the weight once the maximum numbers of sets and repetitions have been achieved (44).

Nonlinear periodized exercise

Nonlinear periodized exercise (NLPE) is a training modality traditionally used by athletes. It involves a combination of high and low intensity aerobic and resistance training with the intensity, duration, and repetition volume altered according to the individual’s subjective and objective responses to exercise (51).

It is hypothesized that NLPE training may benefit patients with COPD as it provides an individualized training protocol which may cater to the multifactorial causes of exercise intolerance in this population (52). However, only one study has evaluated NLPE in COPD patients (52). Klijn et al undertook a randomized controlled trial that compared NLPE to conventional endurance and resistance training (control group) in 110 patients with severe and very severe COPD (52). The exercise intervention was delivered as part of a 10-week inpatient PR program with exercise training sessions delivered three times per week. For both training protocols, resistance exercise included leg press, leg extension, chest press and pull down, whereas the aerobic exercise was stationary cycling for NLPE and stationary cycling and walking for the control group. The NLPE protocol was sophisticated and variable: aerobic exercise training intensity ranged from intervals of 30 seconds to 10 minutes at 50% to 120% maximum workload and resistance training involved 1 to 5 sets of 1 to ≥20 repetitions at 30% to 95% of 1 repetition maximum. In contrast, the control group’s protocol was 10 to 24 minutes at 30% to 75% maximum workload for aerobic exercise and resistance training was prescribed at 50% of 1 repetition.

The control group attended significantly more training sessions and had a longer total time spent performing endurance exercise but had a lower cycle training intensity compared to the NLPE group. Despite this, the NLPE group achieved significantly greater improvements in cycle endurance time (primary outcome), dyspnea and health-related quality of life than the control group. However, there were no significant between-group differences in peripheral muscle strength or body composition. This is a novel training modality whose proof-of-concept has been demonstrated in patients with COPD; future work should replicate the results of this trial and explore the long-term benefits.

Upper limb training

International statements recommend that upper limb training be included in the exercise component of PR (5), as patients with COPD report significant dyspnea when performing activities of daily living that involve their arms such as combing hair, showering, cooking or carrying groceries (53). Studies examining the effect of upper limb training have included aerobic (arm ergometry) (54), resistance (free weights, unsupported upper limb training) (54–56) and functional (ball throwing, ring moving) (54) exercise. A systematic review of five studies (n = 157) that evaluated upper limb training in patients with moderate to severe COPD reported that it significantly improved upper limb exercise capacity, but the impact on dyspnea and health-related quality of life was unclear (54). The authors were unable to comment on the specific type of exercise that should be prescribed and the appropriate outcome measure for upper limb training protocols because of the lack of standardization of exercise modality, prescription and progression, program duration and frequency as well as outcome measures. Two subsequent randomized controlled trials compared PR with upper limb training to PR alone (57) or PR with upper limb flexibility exercises (55). In both studies, significant improvements in upper limb function and exercise capacity were demonstrated in the intervention compared to the control group, with one study also reporting significant increases in upper limb muscle force (55). This is important because upper limb strength and endurance can impact peoples’ ability to perform daily activities. However, upper limb training did not provide any additional benefit on levels of exercise capacity (55, 57), dyspnea (55) or health-related quality of life (55). Future research should identify the optimal training protocol, target population, physiological effects on the upper limb muscles and outcome measures, and assess the impact of upper limb training on performance of upper limb-based daily living activities.

Balance training

In addition to maintenance of muscle strength and endurance, balance is important in maintenance of mobility and functional independence for older adults, including those with COPD (58) and is important in prevention of falls. Falls are common among people with COPD (59–61) and may lead to hip, vertebral and other fractures and pose risk of hospitalization, with its associated morbidity and mortality risk.

Maintenance of upright static (still) and dynamic (functional, with movement) postural balance requires integration of a complex array of central nervous system, peripheral neural, muscular and sensory signals (58). Notably, people with COPD have impairments of various aspects of static and dynamic balance (62–69). They have a harder time maintaining single leg stance (68), have reduced gait speed (58, 70), increased time between steps, narrow step width (71, 72), increased gait variability (71, 72) and greater degrees of postural sway (64, 65, 73, 74) compared to healthy age-matched controls. Alterations in proprioception contribute to this impaired balance control (73). Importantly, impairment of balance is associated with fall risk in COPD (63, 67, 69).

The American Geriatrics Society recommends exercise with balance training for prevention of falls in older adults (75). However, despite this, and the evidence for impaired balance among people with COPD, current international guidelines for PR consider, but do not yet formally recommend strategies to optimize balance in PR programs. Conventional comprehensive PR has only a small effect on measures of balance (76). Several recent trials have therefore assessed the potential role for balance training as a routine component of PR.

Beauchamp and colleagues conducted the first randomized controlled trial of balance training incorporated in a conventional six-week comprehensive multidisciplinary PR program versus PR without balance training among 39 subjects with moderate to severe COPD (77). In this study, balance training was conducted three times per week for 30 min per session for six weeks and included stance, transition, gait and functional strength exercises of incremental difficulty according to patient ability. As compared to comprehensive PR alone, addition of balance training led to significant improvements in measures of balance including the Berg Balance Scale (p < 0.01), Balance evaluations systems test (p < 0.01), and improvement in the physical function subscale of the SF-36 questionnaire; no significant differences were seen between groups in the Activities-Specific Balance Confidence Scale. Balance training was well tolerated by the participants and no adverse events were noted. Subsequent studies have confirmed benefits of balance training included in PR programs on balance measures (78, 79) and health-related quality of life (79). In one prospective cohort study, 84% of patients with COPD who had undergone balance training reported they enjoyed it and felt it helped with their daily activities, and 95% expressed a desire to continue it (80). Thus far, no studies have investigated the impact of balance training included alongside conventional exercise training in PR on falls among individuals with COPD. A large, multicenter, international randomized controlled trial to investigate the impact of balance training in PR on fall risk is underway (81). Although a detailed description is beyond the scope of this review, several methods to assess and measure balance among older adults and individuals with COPD are suitable for routine clinical use (58, 67, 76, 82–86).

Yoga and tai chi

Yoga

Yoga is an alternate method of exercise training that also focuses on mind-body interaction and incorporates stress reduction and breathing techniques. It affords several benefits including improvements in exercise capacity (87). The combination of exercise impairment, dyspnea, and prolonged time required for exhalation experienced by people with COPD has led to interest in the use of yoga, which incorporates Pranayama breathing (deep slow breathing with key focus on exhalation), as an exercise intervention in this population. Yoga is an attractive alternate method of exercise which can be undertaken in community gym and/or home-based settings. It is also potentially amenable to yoga tele-rehabilitation (88).

Pilot work showed the ability of patients with severe COPD to adopt and tolerate yoga breathing, with improvement in oxygen saturation, and without increase in dyspnea sensation (89). Two recent randomized controlled trials have shown benefits of Pranayama yoga breathing on 6MWD (90, 91); one also showed improved scores on the COPD Assessment Test (CAT) (91). Investigators from these two trials concluded that Pranayama breathing is a useful adjunct for people with COPD (91), and may be helpful for people who can’t or who are unwilling to participate in conventional PR or formal yoga programs (90).

Several randomized controlled trials and some non-randomized trials have also investigated the effects of formal yoga programs including yoga poses and exercises together with Pranayama breathing and meditation on outcomes among people with COPD. A small, non-randomized study of a formal yoga program undertaken for one hour three times per week for six weeks by 33 patients with COPD demonstrated significant gains in health-related quality of life [St Georges Respiratory Questionnaire (SGRQ)], as well as vital capacity, maximal inspiratory and expiratory pressures at the end of the study as compared to baseline values (92). However, only two thirds of the patients completed the study. In a trial comparing the effects of 24 one-hour sessions of yoga in 12 weeks to usual medical care, yoga led to significant improvements in 6MWD and self-reported functional performance and greater reductions in distress related to dyspnea (93). There were no significant differences in pulmonary function, depression, anxiety or health-related quality of life between the intervention and the control group. The yoga, which included exercises for stretching and improving flexibility in the spine, shoulders, hips and legs and relaxation techniques, and which was designed for people with COPD, was safe and well tolerated. Seventy-seven percent of the patients found the intervention beneficial (93). Subsequent trials have confirmed benefits of yoga on the 6MWD (94), and one recent trial showed significant improvements in CAT scores, as well as depression and anxiety measures among coal miners with COPD (95).

Three recent systematic reviews and meta-analyses have assessed the efficacy of yoga training in COPD (96–98). The most recently published analysis included 10 studies (eight randomized controlled trials and two nonrandomized trials) wherein the inclusion criteria were diagnosis of COPD, yoga training versus control without yoga training and wherein at least one of several primary outcomes was included (6MWT, Borg scores, pulmonary function or health-related quality of life measures) (98). Analysis of six studies (n = 312) demonstrated favorable treatment effects of yoga on 6MWD (weighted mean difference 22 m), three studies (n = 118) demonstrated a favorable effect on FEV₁ (weighted mean difference 190 ml). Benefits of yoga were also found for Borg dyspnea scores, SGRQ and CAT scores. There was, however, a high degree of inter-study heterogeneity, and the majority of studies were conducted in India, with a few from America and Australia, thus the findings of the analysis may be at risk of publication bias.

Further research is needed to confirm the benefits of yoga training for people with COPD with regard to various aspects of exercise capacity, lung function, symptoms, health-related quality of life and other important outcomes such as anxiety, depression, physical activity, exacerbations and hospitalizations. Further work is also needed to explore which patients may benefit the most, mechanisms by which FEV₁ may improve, determine the duration of training benefits, and the magnitude of benefits of participation in yoga compared to participation in other conventional forms of exercise training in PR.

Tai chi

Tai Chi is a form of martial arts that combines gentle low-impact exercise (focused on muscle strengthening, flexibility, posture and balance) with meditation, concentration and relaxation of the body and mind (99–101). It has been practiced in China for centuries, and has been demonstrated to improve balance, strength (especially of the lower extremities), and aerobic exercise capacity in sedentary persons. It may also improve sleep (102, 103) and overall sense of well-being (101). Extensive literature has also documented its health benefits for individuals with many chronic diseases, including osteoarthritis, Parkinson’s disease, cardiac disease, cancer and those undergoing stroke rehabilitation (100, 101, 104), and several recent trials show it can also afford benefits for people with COPD.

Several features of Tai Chi make it potentially desirable as an exercise/rehabilitative modality for people with COPD. It does not require any specialized equipment, hence can be practiced anywhere; it is suitable for community and/or home-based practice and is not staffing/resource intensive. It can be practiced alone or in groups (even large ones). Its focus on stress reduction has potential benefit for the many people with COPD affected by anxiety, and it may be a more culturally-acceptable form of exercise in some parts of the world as compared with conventional gym-based exercise. Several different forms of Tai Chi exist. One, known as short-form Sun-Style Tai Chi, which includes movements adapted for older people and those with arthritis may be particularly suitable for individuals with COPD (99).

Recent randomized controlled trials have demonstrated that Tai Chi, compared with usual medical care (no exercise intervention) or with an alternate exercise activity, improves 6MWD (105, 106) and time walked in the ESWT (99). Improvements in measures of balance (body sway) (99), health-related quality of life (99, 107) and small improvements in lung function (FEV₁ and/or FEV₁% predicted) have also been reported. One trial demonstrated a reduction in exacerbation rates among those who participated in Tai Chi (106).

Several systematic reviews and meta-analyses of trials evaluating the effects of Tai Chi (and other meditative movements) for people with COPD (104, 108–113) have demonstrated favorable short-term effects on the 6MWD and quality of life (112, 113). A recent Cochrane Review evaluating the effects of Tai Chi either alone or with another treatment intervention (12 studies involving 984 patients analyzed) (111) demonstrated modest improvements in 6MWD (mean difference 29.64 m) and very small (mean 0.11mL) increases in FEV₁ after Tai Chi (111). The overall quality of evidence was considered very low to moderate. There were no conclusive effects of Tai Chi on dyspnea or health-related quality of life. Tai Chi was not found to be superior to or to add additional benefits to other treatment interventions such as breathing exercises or other forms of exercise. No adverse events were reported related to participation in Tai Chi.

Tai Chi and other forms of meditative exercise as training modalities appear to be safe and to have a role for some people with COPD. However, the optimal style of Tai Chi, program duration and context are not yet known, and substantive long-term benefits in exercise tolerance or other outcomes remain to be demonstrated. One small study did demonstrate comparable oxygen uptake between Tai Chi and conventional treadmill exercise (with lower respiratory rate and lesser increase in dynamic hyperinflation) with Tai Chi (114), but the impact of Tai Chi on lung function, breathing pattern and dyspnea requires further study. Further study is also needed to understand the effects of Tai Chi on maximal exercise capacity, muscle strength, balance measures, fall risk, anxiety, depression, physical activity and other health outcomes. Finally, a majority of clinical trials evaluating the effects of Tai Chi for people with COPD have been conducted among people from China or elsewhere in Asia. Thus, the generalizability of the trials’ findings, and the perceived desirability of Tai Chi as an exercise training modality for other cultural and geographic groups is not yet known.

Inspiratory muscle training

Dyspnea with exertion is a prominent feature of COPD; it has a multifactorial basis, but it relates, at least in part, to lung hyperinflation, with resultant mechanical constraint on the diaphragm and other respiratory muscles. Some individuals with COPD have outright respiratory muscle weakness. Others develop functional weakness of the respiratory muscles when the muscles have to work at faster respiratory rates (such as during exertion) and when forced into shorter fiber length by hyperinflation (115). As such, there has been longstanding interest in inspiratory muscle training (IMT) as a strategy to improve dyspnea for people with COPD (5, 116, 117).

There are a variety of hand-held devices available for inspiratory muscle training. Resistive training uses devices that have differing levels of inspiratory flow resistance (eg. achieved by patient breathing through holes of sequentially smaller diameter). The training load achieved from these devices can be difficult to standardize, as it may vary depending on fluctuations in the patient’s intrinsic airflow resistance. Threshold IMT, wherein the device has pre-set consistent training loads and the patient has to reach specific threshold of inspiratory effort to achieve air flow through the device, is used more commonly in the research setting, as the training load is easier to standardize. With threshold IMT, the inspiratory threshold (load) is also adjustable over time. More recently, other novel methods for IMT, including an electronic tapered flow resistive loading device (TFLR) (118) and a high-frequency airway oscillating respiratory muscle training device (119) have been reported. The TFLR device maintains relative intensity of resistance throughout the duration of the inspiration by adapting to changing configuration of the inspiratory muscles throughout each breath (118). It also has ability to store pressure and flow data from each training session, which can both track adherence to and intensity of training over time. The oscillating training device (119) incorporates a feature to promote muco-ciliary clearance in addition to strengthening the muscles of inspiration and expiration.

Protocols for inspiratory muscle training vary widely. In general, patients breathe quickly and forcefully through the hand-held training device either until a pre-set number of breaths (e.g. 30) or a time limit (e.g. 5 minutes) have been reached. Training sessions are usually conducted twice daily with several hours between sessions, and are undertaken two to six days per week for several weeks (118, 120). IMT can be provided as a stand-alone intervention, or in conjunction with other forms of exercise training. In general, a training stimulus of at least 30% of pre-measured maximal inspiratory muscle pressure (PIMax) is needed to achieve gains in inspiratory muscle function (121–123).

A systematic review and meta-analysis of 32 randomized controlled trials (including 830 participants) of IMT undertaken as a stand-alone treatment intervention showed that IMT leads to significant and clinically important gains in inspiratory muscle strength and endurance as well as dyspnea, exercise capacity and health-related quality of life (123). One study evaluating impact of longer term (one year) of IMT also demonstrated a reduction in use of healthcare services and hospital length of stay following IMT (124). More recent randomized controlled trials including patients with moderate-to-severe COPD have further confirmed the benefits of IMT for increasing respiratory muscle strength and/or endurance (118–120, 125), reducing dyspnea (119, 125) and improving health-related quality of life (120), and also demonstrated improvement in cycle endurance time (125). These findings were corroborated in the recent systematic review and meta-analysis by Beaumont and colleagues (126). In a randomized controlled trial by Langer and colleagues, reduced diaphragm activation (relative to maximum) was found after IMT, despite no significant change in total ventilation, breathing pattern or degree of dynamic hyperinflation (125). No significant gains in ISWT (119, 120) or ESWT (119) were noted following IMT. Earlier studies suggested that individuals with weaker respiratory muscles achieve greater gains following IMT than those with preserved normal inspiratory muscle strength (123, 127); however, this is not a universal finding (128). Thus, the mechanism(s) by which IMT may confer its clinical benefits are not fully clear, and may vary among individuals. Given that inherent force-generating capacity of diaphragm myocytes is often preserved among individuals with COPD, further increases in strength and/or endurance of the diaphragm and other respiratory muscles may contribute to the benefits conferred by IMT.

IMT also leads to improvements in respiratory muscle strength and/or endurance when delivered in conjunction with other forms of exercise training (126, 128–130), including among individuals with severe COPD with resting hypercapnia who require noninvasive ventilation following a bout of acute respiratory failure requiring mechanical ventilation (131). Improvements in thoracoabdominal mobility have also been demonstrated following IMT (130) or respiratory muscle stretching exercise (132). However, IMT added to other forms of exercise training, such as in PR, does not consistently lead to greater overall gains in dyspnea, exercise tolerance or health-related quality of life than those conferred by rehabilitation without IMT (126, 128, 133, 134). As such, IMT is not presently included routinely in most PR programs. In one trial, participants in the IMT plus PR group had greater gains in cycle endurance time and reductions in Borg dyspnea measures at isotime during cycling exercise, but did not have any significant differences in gains in 6MWT, compared to those who had PR alone (129). Thus, it is possible that IMT provided in addition to PR confers benefits for some but not all forms of physical exertion; for example, the impact of IMT plus PR on participants’ ability to perform other daily life tasks such as those involving use of the upper extremities was not assessed in this trial.

Whole body vibration training

Whole body vibration training (WBVT) is a technique of exercise training wherein the individual stands and/or performs squat exercises on an up-down or side-alternating vibration platform. The platform/plate vibrates at variable frequency (typically 24–35 Hz) and peak-to peak amplitude (typically 2–6mm). Contractions of the leg (flexor and extensor) and trunk muscles are elicited via stretch reflexes (135), while the individual controls their body posture and movement.

WBVT has been used for training athletes and for people with other health conditions. Gloeckl and colleagues were the first to demonstrate benefits of WBVT among individuals with COPD (135) in a randomized controlled trial wherein patients performed 3 × 3 minute bouts of squat exercises with versus without use of a WBVT platform (24–26Hz) as part of a three-week inpatient PR program that also included conventional endurance and strength training. Patients in the WBVT group had greater improvements in 6MWT than the control group (mean between-group difference: 27 m; p = 0.046), as well as greater decrease in time performed in sit to stand test (135). Comparable gains between groups were noted in health-related quality of life.

Several subsequent trials have confirmed benefits of WBVT in regard to 6MWT (136–139), as well as maximal work achieved during incremental symptom-limited cycle ergometry (watts) (137), quadriceps force (137) and health-related quality of life (137). A recent systematic review and meta-analysis evaluated six studies investigating the effects of WBVT versus control (without exercise intervention), or versus sham WBVT, in addition to conventional endurance and/or strength training, or during acute COPD exacerbation (140). All of these randomized trials demonstrated benefits in favor of WBVT on exercise capacity (6MWT) (140). Notably, WBVT can improve measures of functional performance relevant to activities of daily living (such as the timed-up-and-go test and sit to stand testing) when delivered in the home setting (141). Randomized controlled trials have also shown benefits of WBVT for people hospitalized with acute COPD exacerbation (gains in exercise capacity (6MWT) and health-related quality of life (SGRQ) above those conferred by physical therapy alone) (142), and for patients recovering from lung transplantation (gains in exercise capacity (6MWT) and peak work rate above those conferred by conventional exercise training plus squat exercises on the floor) (143).

The optimal training parameters of WBVT are as yet unknown, especially for individuals with osteoporosis, orthopedic limitations and/or history of falls. Squat exercises during WBVT elicit comparable physiologic responses (such as ventilatory efficiency and oxygen uptake), dyspnea severity and oxygen desaturation to squat exercises without WBVT among people with severe COPD (144). The spectrum of mechanisms by which WBVT may afford its benefits to people with COPD are also incompletely understood, but improvements in several domains of postural balance control and muscle power output (138) likely contribute to improvements in walking exercise capacity.

Whole body vibration training is not yet used routinely in PR programs, as it requires specialty equipment that is not readily available in many centers. However, it is generally well tolerated and can provide benefits of exercise training even for people with severe COPD (138), and may be a particularly beneficial option for training for those who have difficulty participating in conventional exercise training.

Neuromuscular electrical stimulation

For people who are unable to participate in conventional exercise training due to, for example, ventilatory limitation which precludes effective whole body exercise training, neuromuscular electrical stimulation (NMES) is another alternative method of improving limb muscle strength (145). NMES uses a small battery operated stimulator which, via conductive electrodes placed on the skin of the target muscle, produces a controlled, intermittent electrical current that triggers action potentials and consequently activates intramuscular nerve branches and muscle fibers to generate a contraction and relaxation of the underlying muscles (146, 147). It is most commonly used to target the quadriceps muscles (148) and other lower limb muscles and can be programed to deliver both strength and endurance training protocols (147, 149).^,Furthermore, NMES fulfills the ACSM’s broader definition of exercise as “a planned, structured and repetitive bodily movement done to improve or maintain one or more components of physical fitness” (150) as it can generate a muscle contraction equivalent to 20% to 40% of a maximum voluntary contraction (147).

Preliminary studies have established proof of principle for NMES as a promising rehabilitative tool in patients with COPD (148, 151–155). A Cochrane review of NMES for muscle weakness in patients with advanced disease (COPD, heart failure and cancer) reported statistically significant improvement in quadriceps force and muscle mass as well as exercise capacity (145). The authors concluded that NMES may be an effective treatment for muscle weakness in adults with advanced progressive disease, and could be considered an exercise treatment for those with muscle weakness who have difficulty engaging with traditional exercise modalities (145).

More recently, Hill et al conducted a meta-analysis of 16 studies involving 267 patients that was specific to the use of NMES in patients with COPD (155). NMES was delivered as a stand-alone intervention or an adjunct to exercise training in seven and nine studies respectively. The majority of studies compared NMES to placebo NMES or no treatment and the settings included patients’ homes, PR facilities, inpatient rehabilitation facilities, outpatient settings, hospital wards, the high dependency unit and the intensive care unit. Most studies applied NMES to the quadriceps muscles, although the gluteal muscles were also targeted and training programs involved NMES once or twice a day for 30 to 60 minutes, most days a week for one to two months. Despite study participants’ having severe to very severe COPD, NMES appeared to be safe and did not increase adverse outcomes. Compared to the placebo, NMES delivered as a stand-alone therapy led to a statistically significant improvement in quadriceps force and endurance as well as exercise capacity. The effect of NMES as an adjunct to exercise training is less clear due to the inclusion of both stable and hospitalized patients in the meta-analysis. Nonetheless, there was mixed evidence for improvements in peripheral muscle force and exercise capacity. However, when NMES was delivered as an adjunct to an exercise program in the ICU, the number of days patients were confined to bed decreased. The authors concluded that offering NMES to patients with advanced COPD in the home is likely to be the most feasible and inexpensive use of this training modality and further high-quality studies exploring NMES as an adjunct to exercise training are required.

Conclusion

Impaired exercise and activity tolerance, and exertional dyspnea are cardinal features of COPD, and several modalities of exercise training are safe, effective and beneficial for people with the disease. The content and structure of PR programs varies widely (156). Ultimately, the type of exercise training received depends on individuals’ limitations, co-morbidities, needs, preferences and goals. It also depends on available exercise program resources and equipment, staff expertise, and costs of the exercise training program.

Declaration of Interest

Carolyn L. Rochester has served on COPD-related advisory boards for GSK pharmaceuticals and Boehringer Ingelheim in the past (none in past year), and has participated in clinical trials in COPD funded by GSK, Boehringer Ingelheim and Astra Zeneca in the past (none in the past year). Claire M. Nolan reports no conflicts of interest.