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EUR J PHYS REHABIL MED 2011;47:483-97

Exercise assessment and training in pulmonary rehabilitation for patients with COPD

IN C ER O V P A Y R M IG E H DI T C ® A

S. SINGH, S. HARRISON, L. HOUCHEN, K. WAGG

Chronic obstructive pulmonary disease (COPD) is a common condition with a growing impact on global health services. Patients with COPD frequently complain of dyspnoea and leg fatigue on exertion. Pulmonary rehabilitation (PR) is an established intervention for the management of patients with COPD. There is clear evidence for the benefit in this population. The purpose of this article is to describe the assessment process, exercise intervention and its anticipated benefits, in the context of a rehabilitation programme for individuals with COPD. This has been sub-divided into aerobic, skeletal muscle resistance and inspiratory muscle rationale, assessment and training. The evidence supporting the incorporation of aerobic and skeletal muscle resistance training in PR is well established. The benefit of including inspiratory muscle training (IMT) as an adjunct to PR is less clear. Key words: Pulmonary disease, chronic obstructive - Exercise - Rehabilitation.

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that may eventually result in repeated hospital admissions.4 Patients with COPD frequently complain of dyspnoea on exertion. Curiously, this is largely independent of the level of impairment as indicated by the patients’ spirometry.5 Patients become trapped in a vicious cycle of inactivity (Figure 1), initiated by breathlessness. Activities are avoided to reduce the impact of the sensation of breathlessness, inevitably, loss of fitness ensues. Patients become deconditioned and activities of daily living become disproportionately difficult. In the extreme, individuals become depressed and socially isolated.6

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hronic obstructive pulmonary disease (COPD) is a common condition with a growing impact on global health services. An estimated 210 million people have COPD worldwide.1 Although the prevalence of COPD may fall eventually in line with reduced smoking rates, the burden of the disease is in fact growing because of the rising incidence of COPD in women and the effect of the ageing population.2 The early stages of COPD often go unrecognized 3 but once established the later stages are characterised by acute exacerbations (AECOPD)

CLAHRC Rehabilitation Theme Office Glenfield Hospital University Hospitals of Leicester NHS Trust, Leicester, UK

Corresponding author: S. Singh, Professor of Pulmonary and Cardiac Rehabilitation, Glenfield Hospital, University Hospitals of Leicester NHS Trust, Leicester LE3 9QP, UK. E-mail: [email protected]

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Figure 1.—Vicious cycle of breathlessness.

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EXERCISE ASSESSMENT AND TRAINING IN PULMONARY REHABILITATION FOR PATIENTS WITH COPD

Pulmonary rehabilitation

There is not one preferred definition of self management, and the term is often used interchangeably with self care. Fundamental to the term however is a process of knowledge acquisition which provokes important lifestyle changes, which is key to the success of PR. The programme usually extends over 6-8 weeks, with two sessions per week of supervised exercise. In the majority of programmes this is standard practice, although in some parts of Europe the programme may extend over 6 months.14 There is some evidence exploring the value of a shortened 4 week course of rehabilitation, suggesting that it may be comparable (in the short term) to a 7 week programme.15 One of the challenges for rehabilitation services is to describe the optimal maintenance strategy. Various packages have been tested with no clear favourite. A number of approaches have been tested ranging from repeating courses of rehabilitation;16 regular maintenance exercise groups 17 to telephone follow-up.18 The effectiveness of rehabilitation is largely location independent, and high quality rehabilitation can be delivered in community and hospital-based programmes, although there may be some selection of patients for both locations. High risk patients may be diverted towards hospital-based programmes. In some parts of Europe in-patient rehabilitation has been reported, and although in the short term successful it is unlikely that this approach will be widely adopted. This is largely due to the expense of this type of PR delivery. An exception to this would be the possible treatment of patients during an exacerbation and this is an area of current research activity. We know that rehabilitation is feasible and effective immediately post exacerbation.19, 20 Postexacerbation rehabilitation has been shown to improve exercise capacity, reduce the risk of hospital readmission, reduce hospital days and emergency department visits in the 3 month period after hospital discharge.19, 20 The purpose of this article is to describe the assessment process, exercise intervention and its anticipated benefits, in the context of a rehabilitation programme for individuals with COPD.


Pulmonary rehabilitation (PR) is an established intervention for the management of patients with COPD.7 There is clear evidence for the benefit in this population 8 and this group constitute the majority of patients benefiting from the programme, however there is accumulating evidence in other populations with chronic respiratory disease [such as interstitial lung disease.9 PR has most recently been defined in the American Thoracic and European Respiratory Society statement as: “… an evidence-based, multidisciplinary, and comprehensive intervention for patients with chronic respiratory diseases who are symptomatic and often have decreased daily life activities. Integrated into the individualised treatment of the patient, pulmonary rehabilitation is designed to reduce symptoms, optimise functional status, increase participation, and reduce health care costs through stabilising or reversing systemic manifestations of the disease”.10 PR should be made available to all individuals disabled by the COPD,7 in practice this is largely those rating themselves as Medical Research Council (MRC) grades 3-5. This is a grading system for breathlessness, which extends from grades 1-5. A higher grade indicates that patients are more disabled by their breathlessness.11 The aims of PR are to improve physical functioning, improve activities of daily living, reduce resting and exertional dyspnea, improve quality of life and reduce the burden of the disease upon the individual and the health care system. This is largely achieved with a combination of supervised exercise sessions and an educational programme delivered by a multi-disciplinary team.3 Of particular importance is advice about a home exercise programme, the ultimate aim is to achieve 30 minutes of exercise/brisk walking for 5 days per week, in line with many national guidelines.12 Many patients will never achieve this, but all participants should be encouraged to extend their walking times gradually. The educational programme covers a number of topics including chest clearance, exacerbation management, relaxation advice, breathing control, tests, travelling and managing physical activity. The agenda is to equip the individual with the knowledge and skills to self manage their disease. It has been reported that the process of rehabilitation does indeed improve the individuals’ knowledge.13

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Rationale for aerobic training Reduced exercise capacity is a well documented feature of COPD, although limiting factors may vary


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and change over time.21 Ventilatory limitation (including dynamic hyperinflation and reduced oxidative capacity), abnormal gaseous exchange, cardiovascular limitation, skeletal muscle dysfunction, inadequate energy supply to respiratory and peripheral muscles and psychosocial problems have all been identified as factors which can influence exercise capacity.21, 22 It has been debated which of these are the primary causes,23, 24 however it seems reasonable that as the disease progresses that more of these factors will play a role in exercise limitation.25 In the context of PR establishing the direct cause of exercise intolerance may not be as useful as measuring the degree of intolerance. Plankeel et al.26 found that despite the cause of reduced exercise capacity (i.e. ventilatory, cardiovascular or nonventilatory) the improvement in walking distance after PR was similar, in the order of 25-35% (P=0.12 between groups). The aim of aerobic training is to induce cardiovascular and peripheral muscle changes that improve oxygen transportation and increase respiratory capacity, thus increasing VO2max.27 Aerobic exercise assessment

Assessment of exercise capacity prior to PR not only helps to prescribe the training load of a programme but also provides a useful outcome measure following rehabilitation to evaluate the effectiveness of the course. Laboratory-based exercise tests

The gold standard measure of maximal exercise capacity testing is laboratory-based cardiopulmonary exercise testing (CPET, Figure 2).28 Cycle ergometry or treadmill tests are the most commonly employed. These tests are usually incremental in nature, meaning that a low work load is set at the start, which is gradually increased at regular intervals throughout the test.29 During cycle ergometry the individual is usually instructed to cycle at a constant speed (often around 50 revolutions per minute [rpm] is sustainable) and after 1 minute periods the work rate is increased by a specified number of Watts per minute (W/min). This is continued until the individual is no longer able to maintain the peak work rate. Treadmill tests are broadly similar in so far that the individual is required to walk at a designated

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Figure 2.—CPET. Cardiopulmonary Exercise Test (zAn-600 ErgoTest).

speed with the treadmill at a zero gradient during the first interval, and the gradient is increased by a specified number of degrees on each of the following increments until the individual is no longer to maintain the work load.30 These tests can also allow the individual to be monitored more closely for vital signs and observations of exercise limitation, such as ventilatory, cardiac or leg fatigue. For individuals who have COPD, peak oxygen uptake (VO2peak) is a measurement which is frequently focused upon.28 This is an indication of maximal exercise capacity and is defined as the highest value of oxygen uptake that is attained during an incremental exercise test. Work rate is also recorded, commonly reported in Watts (W). In a meta-analysis of 13 trials of cycle ergometry (268 participants and 243 controls),8 the common effect size was 8.4 watts (95% confidence interval [CI] 3.4-13.4) following PR. This equated to an 18% improvement in peak work rate from baseline in a similar review.31 Field exercise testing

Whilst laboratory-based exercise tests may be the gold standard, there are limitations in their application. Cycle ergometers and treadmills are expensive, which although may be useful in a research environment, can make them unfavourable in routine clinical use. It can also be argued that cycle ergometry and treadmill walking do not necessarily reflect what an individual is able to achieve in functional capacity (30). Field tests are therefore often employed as


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an alternative. The most common field tests are the 6 minute walk test (6MWT 32) and the incremental shuttle walking test (ISWT).33 Adhering to ATS Guidelines,32 during the 6MWT the individual is instructed to walk as far as possible during 6 minutes around a 30 metre (m) course which is designated by 2 cones, and marked out at 3 metre intervals. The individual is permitted to slow down or stop and rest as necessary. The operator is required to track the distance covered by the individual during the test. A practice walk is not required, but should be considered, and in the event that it is undertaken, a 60 minute rest between tests should be allowed. Distance walked has shown to correlate with peak oxygen uptake on treadmill tests,34 however we cannot be sure whether it is a test of endurance or maximal exercise capacity. It has been shown that individuals are likely to reach their fastest speed during the first 3 minutes of the test, and then the work rate reaches a plateau,35 unlike an incremental test where the work load is constantly increased. It is important to standardise the test course and conduct because it is known that encouragement and course layout may influence the outcome. The ISWT 33 is an externally paced field test (Figure 3). The individual is provided with standardised instructions prior to commencing the test. They are then required to walk around a 10 metre course along a flat surface, which is demarked by 2 cones placed 9 metres apart, allowing 0.5 m at each end for turning. The speed of walking is dictated by an audio signal which begins slowly, and increases at 1 minute intervals. The test is continued until the individual is too breathless to continue or can no longer maintain the speed of walking. A practice walk is followed by a second walk, allowing for a 30 minute rest. Peak oxygen consumption during the ISWT correlates favourably with oxygen consumption during standard treadmill tests as described above 30 and during the test a linear response in lung gas exchange indices occurs.36 A linear response would indicate that as measures of oxygen uptake increase, work load also increases. This test is therefore useful for measuring the distance walked to predict maximal oxygen uptake. The response to the 6MWT and the ISWT has been compared.34 The physiological response to the ISWT is gradual and mirrors the response observed in an incremental cycle test. This is not seen in the 6MWT where a peak response is observed within the first 3 minutes.

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Figure 3.—Incremental Shuttle Walk Test.

By predicting maximal oxygen uptake from the ISWT, it can be used to calculate a walking speed set at a desired training threshold and assessed by the endurance shuttle walk test (ESWT).37 The ESWT is an externally paced constant speed walking field test of endurance capacity. Individuals are instructed to walk around a 10 metre course, similar to that described for the ISWT. The pace is dictated by audio signals, and following a 100 second warm up at a slower pace, the individual is required to walk at a faster pace for as long as they are able to do, although the test has a predefined limit of 20 minutes. There are 16 different levels of speed that can be selected for the ESWT. It is recommended that individuals train at an intensity which exceeds 60% of maximal exercise capacity, however it is generally considered that the higher the intensity the greater the training


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1. a minimum of 20 sessions, 3 times a week, 2 supervised sessions; 2. high intensity training produces greater physiological benefits; 3. interval training may be useful; 4. upper and lower limb extremity training; 5. combination of endurance and strength. As previously mentioned, a threshold of 60% of maximal exercise capacity should be employed in setting an aerobic training programme, however exercising at higher intensity is likely to produce greater physiological effects.38 Training is often focused on lower extremity exercises, such as walking or cycling. Walking is the most accessible form of exercise, as it requires no specific or expensive equipment, and has also been found to be the most important activity to patients.44 In PR programmes which targeted aerobic training by walking, marked improvements in shuttle walking distance, exceeding the MCID of 48 m 15, 45, 46 have been shown. Due to the involvement of the upper limb in many activities of daily living, it is recommended that upper limb training should also be part of an exercise programme.38 This may be part of a resistance training programme, but aerobic training such as arm cycles can be employed. For individuals who are not able to tolerate long duration of continuous endurance training, interval training has been found to have similarly beneficial effects in terms of exercise capacity and health related quality of life for people with moderate to severe COPD.47 We can speculate that greater functional capacity and health related quality of life may be accumulated from a training programme in which exercises are tailored to meet the needs of an individual. However Sewell et al.44 found that this kind of programme yielded no benefits above and beyond those of a typical programme consisting of walking, cycling and resistance training. This means that a standardised approach can be used, regardless of an individual’s particular goal. The benefits of this kind of programme are achievable, regardless of disease severity as defined by the MRC Dyspnoea Grade.48 There is an assumption that improvements in exercise performance on a standardised exercise test inevitably leads to improvements in physical activity, this is not necessarily the case. Human nature is such that simply having the capacity to be more physically active does not guarantee translation into


effect.38 Revill et al.37 conducted the ESWT at three levels of intensity; 75%, 85% and 95% of the maximum. A work rate of 95% elicited a response highly similar to most individuals maximal exercise capacity, while 40% of individuals were able to complete the test at a 75% work rate, therefore a rate of 85% was found to be the optimum training load. The exercise tests described above are not only useful to prescribe a training programme but also to determine an individual’s improvement following completion of the programme. It is currently accepted that a change of around 48m for the ISWT 39 and 54 m 40 for the 6MWT are the minimum distances required for the benefits to be perceived by the individual, or the minimal clinically important difference (MCID). In a systematic review of 16 trials which used the 6MWT to evaluate change after PR (346 patients and 323 controls), the common effect was 48 m (95%CI 32-65).8 However the inferior CI in the review by Lacasse et al. was smaller (32 m) than the lower CI for the MCID (37 m), in this outcome measure. This raises some uncertainty about the clinical significance of the effect size found in this review.8 It is likely that improvements from PR should be judged on a case by case basis, however the MCID provides us with useful benchmarks to evaluate PR programmes. Despite efforts, no MCID could be established for the ESWT within the context of rehabilitation.41 For pharmaceutical interventions the MCID for the ESWT is 65 seconds.41 These walking tests can also be incorporated into measures which predict survival. The 6MWT is one of the components of the BODE Index 42 which is a multidimensional model of predicting survival in COPD. The BODE incorporates body mass (B: BMI), airflow obstruction (O: forced expiratory volume in 1 second [FEV1]), dyspnea score (D: MRC grade) and exercise performance (E: 6MWT). More recently an alternative index has been developed which substitutes the 6MWT for the ISWT. This has been called the i-BODE.43 The incorporation of exercise capacity as a factor for predicting survival suggests that reductions in exercise tolerance have a substantial impact on both the individual and the healthcare system.

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Aerobic exercise training The exercise component for PR has been suggested by the ATS/ERS guidelines,3 as follows:

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increased daily activity. We may need to be careful in how we measure physical activity. Some studies have reported the benefits of rehabilitation in terms of domestic physical activity using simple pedometers 49 or sophisticated motion sensors/accelerometers with varying degrees of success.44, 50, 51

ables to measure because they are better prognostic indicators than lung function.59 Quadriceps weakness is also associated with higher health care utilisation.60

Rationale for resistance training

The aims of measuring muscle function in patients with COPD are: to identify and quantify impairment, to prescribe an appropriate exercise regime and to evaluate the response to treatment. Strength can be measured using volitional or non-volitional techniques (61). Volitional techniques require maximum effort by the subject and can be affected by operator encouragement. Non-volitional testing using nerve stimulation is not effort dependant. Volitional strength can be assessed using static (isometric) or dynamic (isotonic/isokinetic) contractions and measured manually using resistance machines, with portable devices (e.g. handheld dynamometers [HHD], cable tensiometers) and using computerised dynamometers. Manual testing (using the 0-5 Medical Research Council grades) is often used in clinical practice but is insensitive to changes in strength, particularly at grade 3 and above (against gravity).62 The one repetition maximum (1RM) measurement of strength can be used to measure isotonic strength and is a safe and reliable measure of strength in patients with COPD.63 The 1RM is defined as the maximum amount of weight that can be lifted with the proper technique for one repetition only.64 1RM testing is practical and may better reflect functional movements compared to other testing methods. To achieve the maximum, weight should be incrementally increased by 1-5 kilograms (kg) at intervals of 1-5 minutes.62 However this type of testing may not be suitable in very frail subjects or those with unstable cardiac disease. In these individuals, multiple repetition tests may be performed and the 1RM can be calculated using validated equations.65 Cable tensiometers are used to measure isometric strength and quadriceps strength can be measured by this method in patients with COPD.66 To measure quadriceps strength, a cable is strapped to the lower leg and connected to the tensiometer (Figure 4). The tensiometer can measure strength at a variety of joint angles and the equipment is portable. Dynamometers measure isometric strength via the

Measuring muscle strength


The clinical symptoms of COPD are not confined solely to the lungs and the extra- pulmonary consequences of the disease are now well documented.52 The selective loss of skeletal muscle mass and strength is a particular problem which is evident even in the presence of normal body weight.53 The mechanisms responsible for regulating skeletal muscle growth and atrophy in this population are not fully understood. However, deconditioning through inactivity (disuse atrophy) is undoubtedly involved. A progressive loss of fitness occurs as a result of avoiding exertional symptoms. Other proposed causes include systemic inflammation, hypoxaemia, oxidative stress, steroid-induced myopathy and nutritional depletion.52 The effects of ageing on the muscles of patients with COPD is unknown.52 It is unclear whether the decline in muscle function seen with normal ageing (sarcopenia) is more pronounced or accelerated in these patients. In addition to breathlessness, skeletal muscle dysfunction is now recognised as an important factor in the exercise limitations of this population 52 and contributes to whole-body exercise performance.54 We have known for a number of years that patients with COPD are weaker than healthy counterparts of the same age. The reduction in quadriceps strength is around 20-30%.55 A recent study has found that a significant proportion of patients with mild disease; GOLD stages I/II or an MRC dyspnoea score of 1/2, also display quadriceps weakness (28% and 26%, respectively).56 Both upper and lower limb muscle strength are reduced, although the muscles of ambulation are more significantly affected. This may be because the upper-limbs are used heavily during daily tasks (e.g. washing and dressing) or used as accessory muscles for breathing. These factors may contribute to their relative preservation in strength.57 Muscle strength is further reduced during acute exacerbations of the disease.58 Muscle weakness and atrophy are important vari-

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Figure 4.—Cable Tensiometer (custom built strain gauge: Kern CH 50 K 100).

Figure 5.—Hand-held dynamometer (MicroFET 2).

Figure 6.—Hand grip dynamometry (Takei Physical Fitness Test, GRIP D).

application of an external force which either compresses a steel spring (mechanical dynamometer) or moves an electronic force transducer (electronic dynamometer).62 Handheld dynamometer (HHD, Figure 5) can test varying muscle groups by an assessor placing the device over the lever being tested. Two methods of testing have been described: the “make”-test and the “break”-test. In the make-test, the maximal force of the subject is equal to the force

of the assessor. In the break-test, the force of the assessor exceeds that of the subject. Higher reproducibility has been found during break-tests.67 HHD is a cheaper alternative to other more expensive modes of isometric testing, reference values are available 68 and this device has been used to test strength in patients with COPD.69 Hand grip dynamometers (Figure 6) measure grip strength and have been used in several studies of COPD patients. Normative

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(e.g. arthritis). Peripheral muscle function can also be measured via non-volitional twitch force; the quadriceps muscle has been investigated in this way. This involves applying supramaximal magnetic stimulation to the intramuscular branches the femoral nerve to produce a force which is not effort dependant or subject to learning effect.74 However this technique may be uncomfortable and technically more difficult to perform than some volitional methods. For these reasons, the technique is generally reserved for research use rather than clinical practice. Using this technique, quadriceps strength has been found to be lower in COPD patients compared to healthy controls and a drop in twitch force after exercise is a useful indicator of muscle fatigue.75

Figure 7.—Isokinetic dynamometry (Cybex II Norm).

data is available for hand grip strength in several age groups.70 Hand grip force is a useful indicator of nutritional status, particularly in differentiating individuals with chronic malnutrition from those who are underweight but not undernourished and have a similar Body Mass Index.71 Isokinetic dynamometry uses a computer-assisted dynamometer (e.g. Cybex, Figure 7, or Kin-com) to measure isokinetic and isometric strength of various muscle groups at a variety of joint angles and contraction velocities.62 This device represents the gold standard method of measuring strength. Isokinetics describes a process in which a body segment accelerates to achieve a pre-selected speed. As a patient applies a force or “torque”, the dynamometer varies the resistance to match this force throughout the full range of movement and so maintains the fixed speed. The presence of an accommodating resistance allows for the safe measuring of torque (Newton metres: Nm), work ( Joules: J) and power at constant speed throughout the full range of movement and therefore gives a comprehensive picture of muscle function. In healthy subjects, a good correlation exists between isometric and isokinetic measurements 72 and normal values are available.73. Whilst highly accurate; isokinetic dynamometry may not be widely available in clinical practice due to its cost, size and practicality of use. All of these testing methods may be limited by patient effort, learning effect and other extrinsic factors

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Resistance exercise training

The skeletal muscle alterations displayed in patients with COPD indicate that muscle training should play an important role in the treatment of this patient population. Furthermore, resistance training (RT) may allow for effective conditioning of specific muscle groups in patients who are ventilatory limited.52 Given the consequences of skeletal muscle dysfunction in patients with COPD, guidelines recommend that resistance training should be included in a pulmonary rehabilitation programme.76 Despite these recommendations, relatively few published studies have explored the role of RT in subjects with COPD. In a systematic review on strength training in patients with COPD,63 only 9 experimental studies were located. Training sessions generally included 2 to 4 sets of 6 to 12 repetitions of each strength exercise at 50% to 85% of an individual’s 1RM. Training programmes were, on average, 8 to 12-weeks in duration at a frequency of 2 or 3 times per week, with individual sessions lasting between 40 and 90 minutes. These training regimes were generally in line with guidelines for healthy adults,77 and reflect what was subsequently published in the American Thoracic Society/ European Respiratory Society Statement on Pulmonary Rehabilitation.38 Many of the programmes included combined endurance and RT; therefore it is difficult to establish the relative contribution of RT in isolation. The authors of this review 63 concluded that peripheral muscle strength training was feasible and safe for patients with COPD, even at intensities of 80% or


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nitude of strength changes will depend upon the frequency, intensity and duration of training (principle of overload) and will only take place in the mode of performance by which the training occurs (principle of specificity).84 Most resistance training programmes in research studies use a percentage of the 1RM to establish a training load; ≥70% would be typical for RT in all populations. Alternatively loads can be assigned by a given number of repetitions.64 For example, if an individual can lift 20 kilograms (kg) for 10 repetitions, their 10RM is 20kg. Using RM training loads is appropriate for machine weights (Figure 8) or free weights (Figure 9) and 3 sets of 8 repetitions is sufficient to elicit a training response in patients with COPD.85 However other modes of resistance are available including isokinetic dynamometry, elastic resistance bands and using body weight (callisthenics). The choice of equipment is dependant upon what is locally available and the risk assessment of the patient.78 RT is generally progressed by increasing the resistance/ weight, whilst keeping the number of sets and repetitions the same (i.e. low).


more of the pretraining 1RM. No adverse events were reported, although the teaching of the correct lifting technique is important to avoid breath holding in these individuals.78 Furthermore, meta-analysis suggested that RT had a positive effect on both upper limb and knee extensor strength (P