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American Thoracic Society/European Respiratory Society Statement on Pulmonary Rehabilitation

THIS JOINT STATEMENT OF THE AMERICAN THORACIC SOCIETY (ATS) AND THE EUROPEAN RESPIRATORY SOCIETY (ERS) WAS ADOPTED BY THE ATS BOARD OF DIRECTORS, DECEMBER 2005, AND BY THE ERS EXECUTIVE COMMITTEE, NOVEMBER 2005

• Section 1: Introduction and Definition
  
• Section 2: Exercise Performance: Limitations and Interventions

  Introduction
  

  Factors Contributing to Exercise Intolerance in Chronic Respiratory Disease
  

  Exercise Training to Improve Exercise Performance
  

  Special Considerations for Exercise Training in Patients without COPD
  

  Additional Strategies to Improve Exercise Performance
  

  
  
• Section 3: Body Composition: Abnormalities and Interventions

  The Scope of Body Composition Abnormalities in Chronic Lung Disease
  

  Interventions to Treat Body Composition Abnormalities
  

  Special Considerations in Obesity
  

  
  
• Section 4: Self-Management Education

  Introduction
  

  Curriculum Development
  

  Benefits of Self-Management Education
  

  Adherence to Therapeutic Interventions and Transference of Education and Exercise to the Home Setting
  

  
  
• Section 5: Psychologic and Social Considerations

  Introduction
  

  Assessment and Intervention
  

  
  
• Section 6: Patient-centered Outcomes Assessment

  Introduction
  

  Symptom Evaluation
  

  Performance Evaluation
  

  Exercise Capacity
  

  Quality-of-Life Measurements
  

  Outcomes in Chronic Respiratory Failure
  

  
  
• Section 7: Program Organization

  Introduction
  

  Patient Assessment and Selection
  

  Program Setting
  

  Program Structure and Staffing
  

  Program Audit and Quality Control
  

  Long-term Strategies
  

  
  
• Section 8: Health Care Utilization
  
• Section 9: Conclusions and Future Directions
  

	SECTION 1: INTRODUCTION AND DEFINITION

TOP SECTION 1: INTRODUCTION AND... SECTION 2: EXERCISE PERFORMANCE:... SECTION 3: BODY COMPOSITION:... SECTION 4: SELF-MANAGEMENT... SECTION 5: PSYCHOLOGIC AND... SECTION 6: OUTCOMES ASSESSMENT SECTION 7: PROGRAM ORGANIZATION SECTION 8: HEALTH CARE... SECTION 9: CONCLUSIONS AND... REFERENCES

 
Since the last statements on pulmonary rehabilitation by the American Thoracic Society (ATS; 1999) and the European Respiratory Society (ERS; 1997), there have been numerous scientific advances both in our understanding of the systemic effects of chronic respiratory disease as well as the changes induced by the process of pulmonary rehabilitation. Evidence-based support for pulmonary rehabilitation in the management of patients with chronic respiratory disease has grown tremendously, and this comprehensive intervention has been clearly demonstrated to reduce dyspnea, increase exercise performance, and improve health-related quality of life (HRQL). Furthermore, an emerging literature is beginning to reveal its effectiveness in reducing health care costs.

The impressive rise in interest in pulmonary rehabilitation is likely related to both a substantial increase in the number of patients being referred as well as the establishment of its scientific basis by the use of well-designed clinical trials that use valid, reproducible, and interpretable outcome measures. Advances in our understanding of the pathophysiology of chronic respiratory conditions are extending the scope and applicability of pulmonary rehabilitation.

Individuals with chronic obstructive pulmonary disease (COPD) still comprise the largest proportion of those referred for pulmonary rehabilitation. However, it has become clear that regardless of the type of chronic respiratory disease, patients experience a substantial morbidity from secondary impairments, such as peripheral muscle, cardiac, nutritional, and psychosocial dysfunction, as well as suboptimal self-management strategies. Therefore, pulmonary rehabilitation may be of value for all patients in whom respiratory symptoms are associated with diminished functional capacity or reduced HRQL.

The timing of pulmonary rehabilitation depends on the clinical status of the individual patient and should no longer be viewed as a "last ditch" effort for patients with severe respiratory impairment. Rather, it should be an integral part of the clinical management of all patients with chronic respiratory disease, addressing their functional and/or psychologic deficits. Patient education is more than simply providing didactic information. It involves a combination of teaching, counseling, and behavior modification techniques to promote self-management skills and self-efficacy. Patient education should also integrate end-of-life decision making into the overall treatment strategy.

In light of the recent advances in our understanding of the science and process of pulmonary rehabilitation, the ATS and the ERS have adopted the following definition: "Pulmonary rehabilitation is 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 individualized treatment of the patient, pulmonary rehabilitation is designed to reduce symptoms, optimize functional status, increase participation, and reduce health care costs through stabilizing or reversing systemic manifestations of the disease." Pulmonary rehabilitation programs involve patient assessment, exercise training, education, nutritional intervention, and psychosocial support. In a broader sense, pulmonary rehabilitation includes a spectrum of intervention strategies integrated into the lifelong management of patients with chronic respiratory disease and involves a dynamic, active collaboration among the patient, family, and health care providers. These strategies address both the primary and the secondary impairments associated with the respiratory disease.

This document has been developed by an international committee and has been endorsed by both the ATS and the ERS. It places pulmonary rehabilitation within the concept of integrated care. The World Health Organization has defined integrated care as "a concept bringing together inputs, delivery, management and organization of services related to diagnosis, treatment, care, rehabilitation and health promotion" (1). Integration of services improves access, quality, user satisfaction, and efficiency of medical care. As such, pulmonary rehabilitation provides an opportunity to coordinate care and focus on the entire clinical course of an individual's disease.

Building on previous statements (2, 3), this document presents recent scientific advances in our understanding of the multisystemic effects of chronic respiratory disease and how pulmonary rehabilitation addresses the resultant functional limitations. It was created as a comprehensive statement, using both a firm evidence-based approach and the clinical expertise of the writing committee. As such, it is complementary to two current documents on pulmonary rehabilitation: the American College of Chest Physicians and American Association of Cardiovascular and Pulmonary Rehabilitation (AACVPR) evidence-based guidelines (4), which formally grade the level of scientific evidence, and the AACVPR Guidelines for Pulmonary Rehabilitation Programs (5), which give practical recommendations.

	SECTION 2: EXERCISE PERFORMANCE: LIMITATIONS AND INTERVENTIONS

TOP SECTION 1: INTRODUCTION AND... SECTION 2: EXERCISE PERFORMANCE:... SECTION 3: BODY COMPOSITION:... SECTION 4: SELF-MANAGEMENT... SECTION 5: PSYCHOLOGIC AND... SECTION 6: OUTCOMES ASSESSMENT SECTION 7: PROGRAM ORGANIZATION SECTION 8: HEALTH CARE... SECTION 9: CONCLUSIONS AND... REFERENCES

 
Introduction
Exercise intolerance is one of the main factors limiting participation in activities of daily living among individuals with chronic respiratory disease. While there is a growing body of evidence defining the mechanisms of exercise limitation in all respiratory disease, the majority of the literature to date has focused on individuals with COPD (6). In addition, virtually all randomized controlled trials of exercise training have been in this population. Most of the evidence presented here concentrates on COPD, with discussion on exercise limitation and exercise training in other chronic respiratory diseases included, where available.

The cardinal symptoms of chronic respiratory disease that limit exercise in most patients are dyspnea and/or fatigue, which may result from ventilatory constraints, pulmonary gas exchange abnormalities, peripheral muscle dysfunction, cardiac dysfunction, or any combination of the above. Anxiety and poor motivation are also associated with exercise intolerance. Although it is commonly accepted that anxiety and depression have an impact on symptom perception (7, 8) and hence may contribute to exercise intolerance, a direct association between emotional status and exercise tolerance has not been established (9). Further research is needed to unravel the potential interaction between mood disturbances and exercise limitation.

In the next section, the physiologic factors limiting exercise tolerance are discussed together with the most potent intervention to improve exercise tolerance: exercise training. Identifying one variable limiting exercise in patients with COPD is often difficult. Many factors may contribute directly or indirectly to exercise tolerance. Because of this, separating the various mechanisms contributing to exercise intolerance is often a largely academic exercise. For example, deconditioning and hypoxia contribute to excess ventilation, resulting in an earlier ventilatory limitation. By consequence, exercise training and oxygen therapy could delay ventilatory limitation during exercise without altering lung function or the maximum ventilatory capacity. Analyzing the limiting factors may uncover otherwise hidden exercise-related issues, such as hypoxemia, bronchospasm, dysrhythmias, musculoskeletal problems, or cardiac ischemia (10).

Factors Contributing to Exercise Intolerance in Chronic Respiratory Disease
Ventilatory limitation.
In COPD, ventilation during exercise is often higher than expected because of increased dead-space ventilation, impaired gas exchange, and increased ventilatory demands related to deconditioning and peripheral muscle dysfunction. Furthermore, maximal ventilation during exercise is often limited by the mechanical constraints imposed by the lung pathophysiology. Prominent among these constraints and typically seen in emphysematous patients is the delay of normal emptying of the lungs during expiration due to flow limitation (11, 12), which is aggravated during exercise (13). This leads to dynamic hyperinflation (14), resulting in increased work of breathing, increased load on the respiratory muscles (15, 16), and the intensified perception of respiratory discomfort.

Gas exchange limitations.
Hypoxia may directly or indirectly limit exercise tolerance. Hypoxia directly increases pulmonary ventilation through augmenting peripheral chemoreceptor output and indirectly through stimulation of lactic acid production. Lactic acidemia contributes to muscle task failure and increases pulmonary ventilation, as buffered lactic acid results in an increase in carbon dioxide production (17). Supplemental oxygen therapy during exercise in hypoxemic and even in nonhypoxemic patients with COPD allows for higher intensity training, probably through several mechanisms, including a dose-dependent decrease in dynamic hyperinflation by lowering respiratory rate, a decrease in pulmonary artery pressures, and a decrease in lactic acid production (14, 18–22).

Cardiac dysfunction.
The cardiovascular system is affected by chronic lung disease in a number of ways, the most important being an increase in right ventricular afterload imposed by an elevated pulmonary vascular resistance from direct vascular injury (23, 24), hypoxic vasoconstriction (25), and/or increases in effective pulmonary vascular resistance due to erythrocytosis (26). An overloaded right ventricle, in turn, leads to right ventricular hypertrophy, which, if severe or left untreated, may result in right ventricular failure (27). These right ventricular effects can also compromise left ventricular filling through septal shifts that further reduce the ability of the heart to meet exercise demands (28). Other complications include the detrimental effects of tachyarrythmias resulting from a dilated or hypertrophied myocardium. Air trapping and the consequent rise in right atrial pressure may further compromise cardiac function during exercise (29). Under these conditions, exercise-related left ventricular dysfunction, occult at rest, may be observed (30). Several studies have demonstrated substantial physiologic benefits after relatively high levels of exercise training (31–34), but it is difficult to determine the additional contribution of enhanced cardiovascular function to the improvements documented in peripheral muscle function. The role of exercise training in improving cardiovascular function in patients with chronic respiratory disease is largely undefined, and should be studied.

Finally, inactivity can lead to cardiovascular deconditioning, which further limits exercise tolerance. It is important to recognize that a substantial amount of the increase seen in exercise tolerance after exercise training probably reflects improvements in cardiovascular function.

Skeletal muscle dysfunction.
An outline of possible skeletal muscle abnormalities in chronic respiratory disease is given in Table 1. Weight loss and consequent peripheral muscle wasting occurs in approximately 30% of outpatients with COPD (35). Peripheral muscle dysfunction may also be attributable to inactivity-induced deconditioning, systemic inflammation, oxidative stress, blood gas disturbances, corticosteroid use, and reductions in muscle mass (36). The quadriceps muscle has frequently been studied in COPD because it is readily accessible and is a primary muscle of ambulation. However, the generalization of these findings to patients with less severe disease or to other skeletal muscles is unclear. Upper limb skeletal muscle strength and mechanical efficiency may be better preserved, although this is controversial (37–39). For example, unlike the situation in the quadriceps, citrate synthase (an enzyme of the citric acid cycle) activity of the deltoid muscle is relatively preserved in severe COPD (40). At present, there are no studies in which muscle biopsies from upper and lower limbs obtained from the same subjects with chronic respiratory disease have been compared.

Leg fatigue also contributes to poor exercise tolerance in chronic respiratory disease, and in some patients is the main limiting symptom (43, 41). This could be related to the fact that the peripheral muscle alterations described in Table 1 render these muscles susceptible to contractile fatigue (44). Recently, the impact of leg fatigue on the exercise response to acute bronchodilation in patients with COPD has been evaluated (45). In patients who developed leg fatigue during exercise, ipratropium failed to increase endurance time despite an 11% improvement in FEV₁. This study provides indirect evidence of the role of peripheral muscle dysfunction in exercise intolerance in some patients with COPD.

Respiratory muscle dysfunction.
The diaphragms of patients with COPD adapt to chronic overload and show a greater resistance to fatigue (46, 47). As a result, at identical absolute lung volumes, their inspiratory muscles are capable of generating more force than that in healthy control subjects (48, 49). This occurs early in the course of the disease, even before adaptations in the skeletal muscle are seen (50). However, these patients often have hyperinflation, which places their respiratory muscles at a mechanical disadvantage. Despite these adaptations in the diaphragm, both functional inspiratory muscle strength (52) and inspiratory muscle endurance (53) are compromised in COPD. As a consequence, respiratory muscle weakness, as assessed by measuring maximal respiratory pressures, is often present (51–54). This contributes to hypercapnia (55), dyspnea (56, 57), nocturnal oxygen desaturation (58), and reduced exercise performance (41). During exercise it has been shown that patients with COPD use a larger proportion of their maximal inspiratory pressure than healthy subjects, probably due, in large part, to increased respiratory muscle loading from dynamic hyperinflation (59). A last factor that may link the respiratory muscles to exercise limitation is the increase in systemic vascular resistance as the load on the diaphragm increases (60). This may lead to a "steal" effect of blood from the peripheral muscles to the diaphragm, although no convincing data are available to confirm this.

Exercise Training to Improve Exercise Performance
Introduction.
Exercise training, widely regarded as the cornerstone of pulmonary rehabilitation (73), is the best available means of improving muscle function in COPD (61–63) and (probably) other chronic respiratory diseases. It is indicated for those individuals with chronic respiratory disease who have decreased exercise tolerance, exertional dyspnea or fatigue, and/or impairment of activities of daily living. Patients with COPD after acute exacerbations are excellent candidates for exercise training (64). Exercise training programs must address the individual patient's limitation to exercise, which may include ventilatory limitations, gas exchange abnormalities, and skeletal or respiratory muscle dysfunction. Exercise training may also improve motivation for exercise, reduce mood disturbance (65, 66), decrease symptoms (67), and improve cardiovascular function. Patients with severe chronic respiratory disease can sustain the necessary training intensity and duration for skeletal muscle adaptation to occur (63, 68). Before exercise training and during a thorough patient assessment, clinicians must establish optimal medical treatment, including bronchodilator therapy, long-term oxygen therapy, and treatment of comorbidities. A thorough patient assessment may also include a maximal cardiopulmonary exercise test to assess the safety of exercise, the factors contributing to exercise limitation, and the exercise prescription (69). Table 1 summarizes the effects of exercise training on different aspects of skeletal muscle dysfunction.

Improvements in skeletal muscle function after exercise training result in gains in exercise capacity despite the absence of changes in lung function. Moreover, the improved oxidative capacity and efficiency of the skeletal muscles lead to less alveolar ventilation for a given work rate. This may reduce dynamic hyperinflation, thereby reducing exertional dyspnea.

Exercise programs in COPD.
PROGRAM DURATION AND FREQUENCY.
The minimum duration of exercise training in pulmonary rehabilitation has not been extensively investigated. Outpatient exercise training with two or three weekly sessions for 4 weeks showed less benefit than similar training for 7 weeks (70, 71). Furthermore, 20 sessions of comprehensive pulmonary rehabilitation has been demonstrated to show considerably more improvement in multiple outcomes than 10 sessions (72). Short-term, intensive programs (20 sessions condensed in 3–4 weeks) have also been shown to be effective (73). It is generally believed that longer programs yield larger, more endurable training effects (74–76).

Patients should perform exercise at least three times per week, and regular supervision of exercise sessions is necessary to achieve optimal physiologic benefits (77, 78). Because of program constraints, twice-weekly supervised exercise training and one or more unsupervised session at home may be an acceptable alternative (79), although it is unclear whether this is as effective. Once-weekly supervised sessions appear to be insufficient (80).

INTENSITY OF EXERCISE.
Although low-intensity training results in improvements in symptoms, HRQL, and some aspects of performance in activities of daily living (81, 82), greater physiologic training effects occur at higher intensity (31). Training programs, in general, should attempt to achieve maximal physiologic training effects (83), but this approach may have to be modified because of disease severity, symptom limitation, comorbidities, and level of motivation. Furthermore, even though high-intensity targets are advantageous for inducing physiologic changes in patients who can reach these levels, low-intensity targets may be more important for long-term adherence and health benefits for a wider population.

In normal subjects, high-intensity training can be defined as that intensity which leads to increased blood lactate levels (31). However, in the pulmonary rehabilitation patient population, there is no generally accepted definition of high intensity, since many are limited by respiratory impairment before achieving this physiologic change. A training intensity that exceeds 60% of the peak exercise capacity is empirically considered sufficient to elicit some physiologic training effects (84), although higher percentages are likely to be more beneficial and are often well tolerated. In clinical practice, symptom scores can be used to adjust training load (85, 86); these scores are anchored to a stable relative load and can be used throughout the training program (87). A Borg score of 4 to 6 for dyspnea or fatigue is usually a reasonable target. Alternatively, heart rate at the gas exchange threshold or power output has also been used to target training intensity (83).

SPECIFICITY OF EXERCISE TRAINING.
Pulmonary rehabilitation exercise programs have traditionally focused on lower extremity training, often using a treadmill or stationary cycle ergometer. However, many activities of daily living involve upper extremities. Because improvement is specific to those muscles trained, upper limb exercises should also be incorporated into the training program (88). Examples of upper extremity exercises include an arm cycle ergometer, free weights, and elastic bands. Upper limb exercise training reduces dyspnea during upper limb activities and reduces ventilatory requirements for arm elevation (89, 90).

ENDURANCE AND STRENGTH TRAINING.
Endurance training in the form of cycling or walking exercises is the most commonly applied exercise training modality in pulmonary rehabilitation (33, 34, 91, 92). Optimally, the approach consists of relatively long exercise sessions at high levels of intensity (> 60% maximal work rate). The total effective training time should ideally exceed 30 minutes (93). However, for some patients, it may be difficult to achieve this target training time or intensity, even with close supervision (34). In this situation, interval training may be a reasonable alternative.

Interval training is a modification of endurance training where the longer exercise session is replaced by several smaller sessions separated by periods of rest or lower intensity exercise. Interval training results in significantly lower symptom scores (79) despite high absolute training loads, thus maintaining the training effects (79, 94, 95).

Strength (or resistance) training also appears to be worthwhile in patients with chronic respiratory disease (96). This type of training has greater potential to improve muscle mass and strength than endurance training (96–100), two aspects of muscle function that are only modestly improved by endurance exercises. Training sessions generally include two to four sets of 6 to 12 repetitions at intensities ranging from 50 to 85% of one repetition maximum (101). Strength training may also result in less dyspnea during the exercise period, thereby making this strategy easier to tolerate than aerobic training (96).

The combination of endurance and strength training is probably the best strategy to treat peripheral muscle dysfunction in chronic respiratory disease, because it results in combined improvements in muscle strength and whole body endurance (62), without unduly increasing training time (99).

Practice guidelines:

1. A minimum of 20 sessions should be given at least three times per week to achieve physiologic benefits; twice-weekly supervised plus one unsupervised home session may also be acceptable.
   
2. High-intensity exercise produces greater physiologic benefit and should be encouraged; however, low-intensity training is also effective for those patients who cannot achieve this level of intensity.
   
3. Interval training may be useful in promoting higher levels of exercise training in the more symptomatic patients.
   
4. Both upper and lower extremity training should be utilized.
   
5. The combination of endurance and strength training generally has multiple beneficial effects and is well tolerated; strength training would be particularly indicated for patients with significant muscle atrophy.
   

Special Considerations for Exercise Training in Patients without COPD
To date, there are no formal evidence-based guidelines regarding the exercise prescription or response to exercise training for patients with respiratory disorders other than COPD. Therefore, recommendations for pulmonary rehabilitation of these diseases must rely on expert opinion based on knowledge of the underlying pathophysiology and clinical experience. Safety considerations as well as individual patient needs and goals of rehabilitation must guide the exercise prescription and implementation of the training program. Careful consideration of the multiple factors contributing to exercise limitation is essential for each patient. To follow are some unique features for rehabilitation among patients without COPD.

When treated appropriately, patients with asthma are often not ventilatory-limited and therefore can usually achieve substantial physiologic training benefit from high-intensity training. To minimize exercise-induced bronchospasm during exercise training, preexercise use of bronchodilators and an adequate period of gradual warm-up exercise are indicated. Cardiopulmonary exercise testing may be used to evaluate for exercise-induced bronchoconstriction (102). Patients with cystic fibrosis should exercise at stations a few feet apart from other participants to avoid cross-contamination with bacterial pathogens that may be antibiotic resistant (103, 104). In addition, patients and staff members must also pay close attention to hygiene techniques. Patients should maintain the protein and caloric intake necessary to meet the metabolic demand posed by exercise training (105), and precautions should be taken to maintain adequate fluid and salt intake (102, 106–108). Pulmonary rehabilitation has been shown to improve exercise capacity in patients with bronchiectasis (109). For patients with advanced interstitial lung disease, particular emphasis should be placed on pacing and energy conservation, because dyspnea may be severe and oxygen desaturation during exercise may be difficult to correct with supplemental O₂. Walking and low-impact and water-based exercise may be ideal for severely obese patients. Persons with neuromuscular disease–related respiratory disorders may require adaptive assistive equipment to optimize functional status. Exercise should be undertaken in a manner that maintains muscle conditioning while avoiding excess muscular fatigue (110).

Until recently, severe pulmonary hypertension was considered a contraindication to exercise training. However, a closely supervised program with attention to the nature and intensity of exercise may be useful before transplantation or for the treatment of functional limitation. High-intensity exercise is generally not recommended for this population. Low-intensity aerobic exercise, pacing, and energy conservation techniques are recommended. Telemetry monitoring may be indicated for those patients with known arrhythmias. Cessation of exercise is especially important if the patient develops chest pain, lightheadedness, or palpitations. Activities such as weight lifting, which lead to increased intrathoracic pressure, should be avoided because of the risk of syncope and circulatory collapse. Blood pressure and pulse should be monitored closely during exercise, and care should be taken to avoid falls for patients receiving anticoagulation medication. Extreme caution must be used to avoid interruption of continuous intravenous vasodilator therapy and to ensure adequate oxygenation.

Additional Strategies to Improve Exercise Performance
Maximizing pulmonary function before starting exercise training.
In patients with airflow limitation, bronchodilators may reduce dyspnea and improve exercise tolerance (111). These beneficial effects may be mediated not only through reducing airway resistance but also through the reduction of resting and dynamic hyperinflation (112–115). Thus, the effectiveness of bronchodilators should not be judged only by the improvement in FEV₁, as improvements in markers of hyperinflation, such as the inspiratory capacity, may be more relevant to the observed clinical benefit during exercise.

Bronchodilator therapy may be especially effective in enhancing exercise performance in those patients less limited by contractile muscle fatigue (45, 116). With optimal bronchodilation, the primary cause of exercise limitation may change from dyspnea to leg fatigue, thereby allowing patients to exercise their peripheral muscles to a greater degree (115). This nicely illustrates the potential synergy between pharmacologic and nonpharmacologic treatments. Optimizing bronchodilation within the context of a pulmonary rehabilitation program for COPD results in greater improvement in exercise performance, probably by allowing patients to exercise at higher intensities (117).

Practice guideline: In individuals with airflow limitation, optimal bronchodilator therapy should be given prior to exercise training to enhance performance.

Oxygen.
Patients who are receiving long-term oxygen therapy should have this continued during exercise training, but may need increased flow rates. Oxygen supplementation as an adjunct to exercise training has been tested in two distinct populations: those with and those without exercise-induced hypoxemia. In hypoxemic patients, randomized controlled trials compared exercise training with supplemental oxygen to training with room air. In one study, oxygen supplementation led to significant improvement in exercise tolerance and dyspnea (18). In three others, there were no significant between-group differences in exercise tolerance, dyspnea, or HRQL (118–120).

In nonhypoxemic patients, oxygen supplementation also allowed higher training intensities and enhanced exercise performance in the laboratory setting, even without desaturation, probably mediated through a reduced ventilatory response (19). There was a trend for a greater improvement in some aspects of quality of life in oxygen-trained patients, although the study was probably underpowered for this outcome. In another study, the prescription of supplemental oxygen for mild hypoxemia outside of the pulmonary rehabilitation setting did not show any increase in exercise tolerance or HRQL (121). These studies provide important information but do not enable the clinician to predict individual responses to oxygen therapy based on exercise-induced desaturation (122).

Practice guideline: Oxygen supplementation during pulmonary rehabilitation, regardless of whether or not oxygen desaturation during exercise occurs, often allows for higher training intensity and/or reduced symptoms in the research setting. However, at the present time, it is still unclear whether this translates into improved clinical outcomes.

Noninvasive mechanical ventilation.
Noninvasive positive-pressure ventilation (NPPV) reduces breathlessness and increases exercise tolerance in certain patients with chronic respiratory disease, probably through reducing the acute load on the respiratory muscles (123–129). In patients with COPD with chronic respiratory failure, a novel form of noninvasive ventilatory support, proportional assist ventilation, enabled a higher training intensity, leading to a greater maximal exercise capacity and evidence of true physiologic adaptation (130–132). In one study, the addition of nocturnal domiciliary NPPV in combination with pulmonary rehabilitation in severe COPD resulted in improved exercise tolerance and quality of life, presumably through resting the respiratory muscles at night (133).

Practice guideline: In selected patients with severe chronic respiratory disease and suboptimal response to exercise, NPPV may be considered as adjunctive therapy since it may allow for greater training intensity through unloading respiratory muscles. Because NPPV is a very difficult and labor-intensive intervention, it should be used only in those with demonstrated benefit from this therapy. Further studies are needed to further define its role in pulmonary rehabilitation.

Respiratory muscle training.
Adding inspiratory muscle training to standard exercise training in patients with poor initial inspiratory muscle strength has been shown in some studies to improve exercise capacity more than exercise training alone (134–138). In patients with less respiratory muscle weakness, evidence for the addition of inspiratory muscle training to regular exercise training is lacking. Three types of inspiratory muscle training have been reported: inspiratory resistive training (139), threshold loading (140, 141), and normocapnic hyperpnea (142–144). At present, there are no data to support one method over the other.

Practice guideline: Although the data are inconclusive, inspiratory muscle training could be considered as adjunctive therapy in pulmonary rehabilitation, primarily in patients with suspected or proven respiratory muscle weakness.

Neuromuscular electrical stimulation.
Neuromuscular electrical stimulation (NMES) involves passive stimulation of contraction of the peripheral muscles to elicit beneficial training effects. It has been used in patients with severe peripheral muscle weakness, such bed-bound patients receiving mechanical ventilation who have marked peripheral muscle dysfunction (145, 146). The application of NMES combined with active limb mobilization significantly improved muscle strength and exercise capacity and reduced days needed for patients to transfer from the bed to the chair (147). In one study, patients who were deemed by the investigators to be poor candidates for standard pulmonary rehabilitation were able to participate in regular rehabilitation after 6 weeks of NMES (145). One of the potential advantages of NMES is that it can be applied in the home setting. Larger studies are needed to further define its indications and applications.

Practice guideline: NMES may be an adjunctive therapy for patients with severe chronic respiratory disease who are bed-bound or suffering from extreme skeletal muscle weakness.

	SECTION 3: BODY COMPOSITION: ABNORMALITIES AND INTERVENTIONS

TOP SECTION 1: INTRODUCTION AND... SECTION 2: EXERCISE PERFORMANCE:... SECTION 3: BODY COMPOSITION:... SECTION 4: SELF-MANAGEMENT... SECTION 5: PSYCHOLOGIC AND... SECTION 6: OUTCOMES ASSESSMENT SECTION 7: PROGRAM ORGANIZATION SECTION 8: HEALTH CARE... SECTION 9: CONCLUSIONS AND... REFERENCES

 
The Scope of Body Composition Abnormalities in Chronic Lung Disease
Body composition abnormalities are probably prevalent in all advanced respiratory disease. However, most literature, to date, has focused on individuals with COPD. Therefore, most of the information given below relates to this disease. Individuals with moderate to severe COPD are frequently underweight, including up to one-third of outpatients (148, 149) and 32 to 63% of those referred for pulmonary rehabilitation or those participating in clinical trials (150–154). Muscle wasting associated with COPD is more common in, but by no means limited to, underweight patients. At a minimum, simple screening should be a component of comprehensive pulmonary rehabilitation. This can be most easily accomplished by calculating body mass index (BMI), which is defined as the weight in kilograms divided by the height in meters squared. On the basis of the BMI, patients can be categorized as underweight (< 21 kg/m2), normal weight (21– 25 kg/m2), overweight (25–30 kg/m2), and obese (> 30 kg/m2). Recent weight loss (> 10% in the past 6 months or > 5% in the past month) is also an important independent predictor of morbidity and mortality in chronic lung disease.

Measurement of body weight or BMI, however, does not accurately reflect changes in body composition in these patients. Body weight can be divided into fat mass and fat-free mass (FFM). FFM consists of body cell mass (organs, muscle, bone) and water. Under clinically stable conditions, measurement of FFM can be used to estimate body cell mass. The loss of FFM, which is characteristic of the cachexia associated with chronic lung diseases, such as COPD, can be estimated using skinfold anthropometry, bioimpedance analysis (which determines FFM) (155), or dual-energy X-ray absorptiometry (DEXA; which determines lean nonfat, nonbone mass) (156). Although reductions in FFM are usually associated with weight loss, the former may even occur in weight-stable patients. Loss of FFM is significantly related to selective atrophy of muscle fibers, particularly type II fibers (68, 157, 158).

In the last two decades, several studies have defined and quantified depletion of FFM. Patients can be considered to be depleted based on the FFM index (FFM/height2), with values below 16 kg/m2 for men and 15 kg/m2 for women (159). In European studies, using these criteria, 35% of patients with COPD admitted for pulmonary rehabilitation and 15% of outpatients with COPD were characterized as depleted (160–162), underscoring its high prevalence in chronic lung disease.

Patients with COPD and reduced FFM have lower exercise tolerance as measured using either 12-minute walk distance (163, 160) or O₂max (164, 165) than those with preserved FFM. In addition, peripheral muscle strength is decreased in patients with COPD (38, 166–168, 163), although it is seen in some muscle groups more than others (169). Because muscle power is directly proportional to its cross-sectional area, loss of muscle mass would be expected to impair muscle strength. Indeed, the finding that strength per kilogram of limb FFM is similar in patients with COPD and control subjects supports the concept that loss of muscle mass is a major determinant of limb weakness (166). Reduced FFM in COPD is also associated with impaired respiratory muscle strength (167, 168), although a proportion of the apparent weakness of these muscles is undoubtedly due to mechanical disadvantage due to changes in chest wall shape and hyperinflation (170).

Underweight patients with COPD have significantly greater impairment in HRQL than those with normal weight (171). Moreover, those with depletion in lean body mass have greater impairment in this outcome area than those without depletion (171). Because normal-weight patients with COPD and low FFM have more impairment in HRQL than underweight patients with normal FFM, this body composition abnormality appears to be an important predictor of HRQL, independent of weight loss (163).

In COPD, there is an association between underweight status and increased mortality (172–174), independent of the degree of airflow obstruction (172). Perhaps more importantly, weight gain in those with a BMI below 25 kg/m2 was associated with decreased mortality (172, 175). Because the midthigh muscle cross-sectional area (using computed tomography scanning) in severe COPD was demonstrated to be a better indicator of prognosis than BMI (176), the loss of muscle mass rather than body weight may be a better predictor of mortality. Normal-weight patients with COPD and depleted FFM may have a comparable mortality risk to underweight patients with depleted FFM.

Weight loss may be caused by increased energy and substrate metabolism or reduced dietary intake, and muscle wasting is the consequence of an imbalance between protein synthesis and protein breakdown. Impairment in total energy balance and protein metabolism may occur simultaneously, but these processes can also be dissociated because of altered regulation of substrate metabolism. Hypermetabolism may be the consequence of low-grade systemic inflammation in COPD (177, 178). Total energy expenditure, which reflects the metabolic state of the individual, includes resting energy expenditure and activity-related energy expenditure. In sedentary individuals, resting energy expenditure is the major component of total energy expenditure, and this has been found to be elevated in 25% of patients with COPD (179). Activity-related energy expenditure is also elevated in COPD, but there may be different mechanisms that underlie these metabolic alterations in subgroups of patients (154). Table 1 summarizes the effects of body composition on different aspects of skeletal muscle dysfunction.

Interventions to Treat Body Composition Abnormalities
Introduction.
The rationale for addressing and treating body composition abnormalities in patients with chronic lung disease is based on the following: (1) the high prevalence and association with morbidity and mortality; (2) the higher caloric requirements from exercise training in pulmonary rehabilitation, which may further aggravate these abnormalities (without supplementation); and (3) the enhanced benefits, which will result from structured exercise training.

Although the etiology of the weight loss and muscle wasting in chronic respiratory disease is complex and not yet fully understood, different physiologic and pharmacologic intervention strategies have been used to reverse wasting of fat mass and FFM. The duration of most of these interventions has been 2 to 3 months; limited information is available regarding longer term therapy. Assessment of body composition is indicated in the assessment and diagnostic workup of the individual patient to target the therapeutic intervention to the pattern of tissue wasting.

Caloric supplementation.
Caloric support is indicated to match elevated energy requirements to maintain or restore body weight and fat mass. This is especially important for chronic respiratory patients, since some may suffer from involuntary weight loss and/or exhibit a decreased mechanical efficiency during exercise. Adequate protein intake is crucial for stimulation of protein synthesis to maintain or restore FFM not only in underweight but also in normal-weight patients. The increased activity-related energy requirements during pulmonary rehabilitation must also be met, even in normal-weight individuals (180).

Caloric supplementation intervention should be considered for the following conditions: a BMI less than 21 kg/m2, involuntary weight loss of more than 10% during the last 6 months or more than 5% in the past month, or depletion in FFM or lean body mass. Nutritional supplementation should initially consist of adaptation in the patient's dietary habits and the administration of energy-dense supplements.

In early controlled clinical trials, oral liquid dietary supplementation (without exercise) was able to restore energy balance and increase body weight in underweight patients with COPD (181–183). These early intervention studies did not assess the ratio of fat mass to FFM. In most outpatient settings, however, nutritional supplementation alone has not been successful in inducing significant weight gain (184). Several factors may contribute to this, including a reduction in spontaneous food intake (180, 185, 186), suboptimal implementation of nutritional supplements in daily meal and activity pattern (185), portion size and macronutrient composition of nutritional supplements (187), and the presence of systemic inflammation (186). Addressing these factors by integrating nutritional intervention into a comprehensive rehabilitation program should improve outcome. For example, two controlled studies have demonstrated that nutritional supplementation combined with supervised exercise training increased body weight and FFM in underweight patients with COPD (168, 188). From these studies, it can be anticipated that the combined intervention can result in a 2:1 ratio of gain in FFM to gain in fat mass.

Physiologic interventions.
Strength training may selectively increase FFM by stimulation of protein synthesis via insulin-like growth factor 1 (IGF-1) or targets downstream of IGF-1 signaling. In patients with COPD and a normal body composition, 8 weeks of whole body exercise training increased body weight as a result of modest increases in FFM, whereas body fat tended to decrease (189). Enhanced bilateral midthigh muscle cross-sectional area, assessed by computed tomography, was seen after 12 weeks of aerobic training combined with strength training in normal-weight patients with COPD (190). However, BMI did not change. This different response in BMI could be related to differences in dietary intake between study groups (191).

Pharmacologic interventions.
Several pharmacologic strategies have been used in an attempt to induce weight gain and, specifically, increase FFM in COPD. Anabolic steroids have been investigated most extensively, either as single therapy (192) or combined with pulmonary rehabilitation (184, 168). In general, treatment duration ranged from 2 to 6 months. Anabolic steroids may improve outcome of pulmonary rehabilitation through various mechanisms: (1) stimulation of protein synthesis either directly or indirectly by interaction with the IGF-1 system, (2) regulation of the myostatin gene, (3) antiglucocorticoid action, and (4) erythropoietic action. Low-dose anabolic steroids, given either by intramuscular injection or orally administered, increase FFM, but not fat mass, generally without harmful effects (193). In male patients with low testosterone levels, testosterone administration resulted in an increase in muscle mass. This effect was augmented by concomitant resistance training, and resulted in increased strength (194). It is not clear whether anabolic therapy will lead to improvements in exercise capacity or health status. Specific indications for this treatment are not yet defined.

Growth hormone, which is a potent stimulator of systemic IGF-1 levels, has been shown to increase lean body mass in a small number of underweight patients with COPD participating in a pulmonary rehabilitation program (195). The modest improvement in body composition was associated with increases in exercise performance. However, this therapy is expensive and has been associated with a number of undesirable side effects, such as salt and water retention, and impairment in glucose metabolism. Currently, studies are ongoing to investigate the efficacy and safety of growth hormone–releasing factors to improve body composition and functional capacity in COPD.

The progestational agent megesterol acetate has been shown to increase appetite and body weight, and stimulate ventilation in chronic wasting conditions such as AIDS and cancer. In underweight patients with COPD, 8 weeks of this drug resulted in a treatment–placebo difference of 2.5 kg weight. However, this favorable change in weight was mainly fat mass (196).

On the basis of the current studies, it appears that several physiologic and pharmacologic interventions are able to modulate either fat mass or FFM in patients with COPD. Although these interventions appear to be safe in the short term, further studies are needed to evaluate long-term effects. Further studies are also necessary to develop optimal strategies for pharmacologic interventions for muscle wasting in chronic lung disease. These will include combining exercise training with pharmacologic therapy, targeting specific subpopulations (disease severity and tissue depletion pattern), and determining whether improvement in body composition translates into functional benefits and prolonged survival.

Special Considerations in Obesity
The respiratory disturbances associated with obesity cause an increased work and oxygen cost of breathing (197), with impaired exercise tolerance, disability, and impaired quality of life (198–200). Significant abnormalities of respiratory function can result from obesity alone, even in the absence of underlying parenchymal lung or restrictive chest wall disease. Respiratory disturbances associated with obesity include impaired respiratory mechanics with low lung volumes and decreased respiratory system compliance, increased small airway resistance, and alterations in both breathing pattern and respiratory drive (197, 201). Patients with "obesity hypoventilation syndrome" have resting daytime hypoxemia and hypercarbia, impaired central respiratory drive with decreased ventilatory responsiveness to CO₂, and nocturnal alveolar hypoventilation (197, 201). Persons with "simple obesity" may also have hypoxemia greater than expected for age, due to poor expansion of the lung bases, but maintain normal daytime PCO₂. Obstructive sleep apnea and nocturnal alveolar hypoventilation are also extremely common in obese persons, and can result in pulmonary hypertension and cor pulmonale (197, 202). Obesity is also associated with an increased risk of thromboembolic disease, aspiration, and complications from mechanical ventilation (197). Many morbidly obese individuals eventually develop overt respiratory and/or cardiac failure.

Pulmonary rehabilitation is an ideal setting in which to address the needs of people with obesity-related respiratory disorders and individuals with lung disease in whom obesity is also contributing to functional limitation. Specific interventions may include nutritional education, restricted calorie meal planning, encouragement for weight loss, and psychologic support. Although there is no established target for the amount of weight loss to be achieved after pulmonary rehabilitation, comprehensive rehabilitation of obese persons can lead to weight loss, and improved functional status and quality of life (203–205).

Practice guideline: Pulmonary rehabilitation programs should address body composition abnormalities, which are frequently present and underrecognized in chronic lung disease. Intervention may be in the form of caloric, physiologic, pharmacologic, or combination therapy.

	SECTION 4: SELF-MANAGEMENT EDUCATION

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Introduction
Patient education remains a core component of comprehensive pulmonary rehabilitation, despite the difficulties in measuring its direct contribution to overall outcomes (5, 206, 207). Education permeates all aspects of pulmonary rehabilitation, beginning at the time of diagnosis and continuing through end-of-life care. It is a shared responsibility among the patient, family, primary care physician, specialist, and nonphysician health care providers.

The style of teaching used in pulmonary rehabilitation is changing from traditional didactic lectures to self-management education (208). Although the former provides information related to the patient's condition and his or her therapy, the latter teaches self-management skills that emphasize illness control through health behavior modification, thus increasing self-efficacy, with the goal of improving clinical outcomes including adherence (Figure 1) (209, 210). Self-efficacy refers to the belief that one can successfully execute particular behaviors to produce certain outcomes (211). Strategies to enhance self-efficacy are listed in Table 2.

View larger version (7K): [in this window] [in a new window]   Figure 1. Causal chain of behavior modification. Reprinted by permission from Reference 210.

Prevention and early treatment of respiratory exacerbations, informed end-of-life decision making, breathing strategies, and bronchial hygiene techniques are important educational issues to be included in pulmonary rehabilitation. Health professionals should always be aware of those patients who still require smoking cessation interventions.

End-of-life decision making.
Prognostic uncertainty as well as health care provider reluctance form barriers that hinder the discussion of end-of-life decision making. Pulmonary rehabilitation has been identified as an appropriate setting for the discussion of advance care planning and palliative care (221, 222).

Breathing strategies.
Breathing strategies refer to a range of techniques, including pursed-lip breathing, active expiration, diaphragmatic breathing, adapting specific body positions, and coordinating paced breathing with activities. These techniques aim to improve regional ventilation, gas exchange, respiratory muscle function, dyspnea, exercise tolerance, and quality of life (223).

Pursed-lip breathing attempts to prolong active expiration through half-opened lips, thus helping to prevent airway collapse. Compared with spontaneous breathing, pursed-lip breathing reduces respiratory rate, dyspnea, and Pa_CO2, while improving tidal volume and oxygen saturation in resting conditions (224). Though these have not been convincingly demonstrated to result in enhanced exercise performance, many patients with chronic lung disease use this technique instinctively and report decreased dyspnea with its use.

Active expiration and body positioning techniques attempt to decrease dyspnea, possibly by improving the length–tension relationships or geometry of the diaphragm. Diaphragmatic breathing techniques require the patient to move the abdominal wall out during inspiration and to reduce upper rib cage motion. The goal is to improve chest wall motion and the distribution of ventilation, thereby decreasing the energy cost of breathing. To date, evidence from controlled studies does not support the use of diaphragmatic breathing in patients with COPD (225, 226). Forward leaning has been noted clinically to be effective in COPD and is probably the most adopted body position (227). Use of a rollator/walker while ambulating allows forward leaning with arm support, decreases dyspnea, and increases exercise capacity (228, 229).

As with the development of all aspects of the patient's self-management education curriculum, the breathing strategies must be individualized. Patients will usually adopt the techniques most effective in reducing symptoms (230).

Bronchial hygiene techniques.
For some patients, mucus hypersecretion and impaired mucociliary transport are distinctive features of their lung disease. Instruction in the importance of bronchial hygiene and training in drainage techniques are appropriate for these patients. A recent review concluded that the combination of postural drainage, percussion, and forced expiration improved airway clearance, but not pulmonary function, in patients with COPD and bronchiectasis (231). Use of a positive expiratory pressure mask and assisted coughing were more effective than assisted coughing alone in patients with COPD during an exacerbation (232). Short-term crossover trials suggest that airway clearance regimens have beneficial effects in cystic fibrosis. However, based on a Cochrane review, there is currently no robust scientific evidence to support the hypothesis that chest physiotherapy for the purpose of clearing airway secretions has a beneficial effect in patients with cystic fibrosis (233).

Benefits of Self-Management Education
Self-management improves health status and lowers health service use in many chronic diseases. Recently, a multicenter randomized clinical trial (220) provided evidence that a multicomponent, skill-oriented self-management program that incorporated an exacerbation action plan and home exercise reduced hospitalizations, emergency visits, and unscheduled physician visits, and improved HRQL. However, the beneficial effects of comprehensive self-management were not replicated in another randomized trial (234). Self-management might be especially beneficial for patients with reduced health status and/or a high frequency of exacerbations. This is a fruitful area for research.

Adherence to Therapeutic Interventions and Transference of Education and Exercise to the Home Setting
Adherence is defined by the World Health Organization as the extent to which a person's behavior corresponds with agreed-on recommendations by the health care provider. Adherence to therapeutic interventions is a crucial health behavior in the management of chronic respiratory disease. The most effective adherence-enhancing interventions are designed to improve patient self-management capabilities (235). The degree of adherence is enhanced when the relationship between the patient and the health care provider is a partnership. Pulmonary rehabilitation is a venue that supports the strengthening of this partnership.

Although the short-term benefits of pulmonary rehabilitation with a supervised exercise training program are well established, challenges remain in understanding and promoting long-term self-management and adherence to exercise in the home setting. Most of our knowledge in exercise behavior comes from emerging research in chronic disease populations, not specifically in patients with chronic respiratory disease. In longitudinal studies of the elderly (236, 237), exercise self-efficacy and estimate of expected benefits from regular exercise were predictors of exercise adherence. Confusion and depression were predictors of poor adherence to a home-based strength-training program (238). In a review of 27 cross-sectional and 14 longitudinal studies of individuals 65 years or older, it was shown that educational level and past exercise behavior correlate positively with the performance of regular exercise (239). Conversely, perceived frailty and poor health were the greatest barriers to adopting an exercise and maintenance program. This is in agreement with a qualitative study conducted specifically in patients with COPD (240). This qualitative study demonstrated that barriers to lifestyle changes frequently reported by patients were progression of COPD and associated comorbid conditions.

A recent study compared enhanced to conventional follow-up strategies at completion of a comprehensive pulmonary rehabilitation program (241). Adherence with exercise was high shortly after completion of the rehabilitation program, but dropped off in both groups over the next 6 months. The most consistently reported reasons for nonadherence were chest infection and disease exacerbation. Although not the primary focus of the study, the description of adherence to home exercise and reasons for nonadherence provide important insight into the patterns and predictors of physical activity behavior modification after rehabilitation. Longer lasting programs seem to enhance long-term effects (76, 242).

Adherence to therapeutic interventions, including exercise programs, is a crucial health behavior in the management of chronic respiratory disease. Instruction in individualized self-management skills is a cornerstone in the promotion of long-term adherence.

Practice guidelines:

1. The educational component of pulmonary rehabilitation should emphasize self-management skills.
   
2. Self-management should include an action plan for early recognition and treatment of exacerbations and discussions regarding end-of-life decision making.
   
3. In selected patients, instruction in breathing strategies and bronchial hygiene techniques should be considered.
   
4. The transference of educational training and exercise adherence to the home setting should be emphasized.
   

	SECTION 5: PSYCHOLOGIC AND SOCIAL CONSIDERATIONS

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Introduction
Chronic respiratory disease is associated with increased risk for anxiety, depression, and other mental health disorders (243, 244). Psychologic and social support provided within the pulmonary rehabilitation setting can facilitate the adjustment process by encouraging adaptive thoughts and behaviors, helping patients to diminish negative emotions, and providing a socially supportive environment.

Patients often experience fear and anxiety in anticipation of, and in association with, episodes of dyspnea (245). This heightened physiologic arousal can precipitate or exacerbate dyspnea and contribute to overall disability. Frustration with poor health and the inability to participate in activities can present in the form of irritability, pessimism, and a hostile attitude toward others. In the later stages of respiratory disease, progressive feelings of hopelessness and inability to cope often occur. Patients with chronic respiratory disease who have positive social support have less depression and anxiety than those who do not (246). Those with a history of preexisting mental health disorders often have the greatest difficulty adjusting to chronic respiratory disease. Most at risk are those with a major depressive or anxiety disorder, previous adjustment or personality disorder, alcohol or drug abuse, or history of psychosis.

Depressive symptoms are common in patients with moderate to severe COPD, with an approximate prevalence rate of 45% (247). The tendency for depressed patients to withdraw from social interactions increases feelings of isolation and depression for both the patient and their loved ones. Sexual activity is also limited by depression and physical restrictions. Subthreshold depression (clinically relevant depression that does not fit operational criteria) is seen in 25% of elderly patients with COPD (248). Both depression and anxiety in the elderly are significantly undertreated (247, 249). Even when appropriate treatment is recommended, many patients refuse anxiolytics or antidepressant medication because of fear of side effects, embarrassment, denial of illness, worries about addiction, cost concerns, or a frustration with taking too many medications (250).

Mild to moderate neuropsychologic impairments may exist as a result of depression as well as disordered gas exchange. These deficits contribute to difficulties in concentration, memory disturbances, and cognitive dysfunction (251), and may lead to difficulty solving common problems in daily living, missed office or clinic appointments, or failure to adhere to the medical and self-management plans (252). Oxygen supplementation should be considered in those patients with documented hypoxemia.

Assessment and Intervention
The initial patient assessment should include a psychosocial evaluation. The interview should allow adequate time for patients to openly express concerns about the psychosocial adjustment to their disease. Questions should cover perception of quality of life, ability to adjust to the disease, self-efficacy, motivation, adherence, and neuropsychologic impairment (e.g., memory, attention/concentration, problem-solving abilities). Common feelings and concerns that are expressed in this component of the evaluation include the following: guilt, anger, resentment, abandonment, fears, anxieties, helplessness, isolation, grief, pity, sadness, stress, poor sleep, poor marital relations, and failing health of the spouse caretaker (253). If possible, interviewing the significant caregiver (with the patient's consent) may help to explore issues related to dependency, interpersonal conflict, and intimacy. Screening questionnaires, such as the Hospital Anxiety and Depression Questionnaire or the Beck Depression Inventory, may aid in the recognition of significant anxiety and depression (254, 255). When a patient seems to be depressed, psychologic counseling should be considered.

Developing an adequate support system is a most important component of pulmonary rehabilitation (256). Patients with chronic respiratory disease will benefit from supportive counseling to address their concerns, either individually or in a group format. Treating depression may make a significant difference in the patient's quality of life (257). However, although moderate levels of anxiety or depression may be addressed in the pulmonary rehabilitation program, patients identified as having significant psychosocial disturbances should be referred to an appropriate mental health practitioner before the start of the program.

Patients should be taught to recognize symptoms of stress and be capable of stress-management techniques. Relaxation training can be accomplished through techniques such as muscle relaxation, imagery, or yoga. Relaxation tapes, supplemented through biofeedback, may be provided for home use. Relaxation training should be integrated into the patient's daily routine, for tackling dyspnea and controlling panic. Useful crisis management skills include active listening, calming exercises, anticipatory guidance regarding upcoming stressors, problem solving, and identifying resources and support systems.

The sensitive topic of sexuality is often of central importance to quality of life (258). A number of factors may determine how sexual functioning is affected by chronic illness: the patient/spouse relationship, degree of affection, communication, and the level of satisfaction with a partner. Although general information may be provided during patient education in a small-group format, specific questions and concerns are generally best addressed in a one-on-one or couples format. For those having significant interpersonal or family conflicts, referral to a clinical social worker, psychologist, or other counselor for family/relationship counseling is recommended.

Practice guidelines:

1. Screening for anxiety and depression should be part of the initial assessment.
   
2. Although mild or moderate levels of anxiety or depression related to the disease process may improve with pulmonary rehabilitation, patients with significant psychiatric disease should be referred for appropriate professional care.
   
3. Promotion of an adequate patient support system is encouraged.
   

	SECTION 6: OUTCOMES ASSESSMENT

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Introduction
Outcomes assessment in pulmonary rehabilitation may be evaluated from three different perspectives: those of the patient, the program, and society. This section will discuss patient-centered outcomes. Program audit and societal outcomes (health care utilization) are covered later in this document.

Patient-centered outcome assessment can range from unstructured clinical assessments to the use of specific, validated tests and instruments, such as a field test of exercise performance or an HRQL questionnaire. These are useful in assessing change among a group of individuals enrolled in a rehabilitation program. Although the utility of these structured assessments in the evaluation of the specific patient has not received much critical study, clinical experience seems to suggest they may also be useful in this setting. In addition, some of the measures used for outcome analysis may also be useful in the initial assessment of the patient. For example, a cardiopulmonary exercise test is useful to determine the mechanism of exercise intolerance, to generate an exercise prescription, to determine the need for oxygen supplementation, and to detect contraindications to a training program.

Patients are referred to pulmonary rehabilitation for several reasons: they do not feel their symptoms (dyspnea or fatigue) have sufficiently improved from medications alone, they are dissatisfied with their ability to perform activities of daily life, and/or they are dissatisfied with their quality of life. Thus, for pulmonary rehabilitation, the important patient-centered outcomes should reflect the following: (1) control of symptoms, (2) the ability to perform daily activities, (3) exercise performance, and (4) quality of life. The effect of pulmonary rehabilitation on these outcomes has been studied with numerous instruments, many of which are described on the website of the ATS: http://www.atsqol.org/qinst.asp. In addition, the AACVPR Guidelines for Pulmonary Rehabilitation Programs provides practical recommendations for using outcome measures (5).

Family members are affected by the patient's condition through role changes, impact on social activities, emotional stress, and financial burden. Little is known about the specific impact of pulmonary rehabilitation on family dynamics.

Like many treatment modalities, pulmonary rehabilitation has made significant progress in evaluating patient outcomes; however, understanding outcomes evaluations continues to require scrutiny. For example, programs should not only determine how much individual patients benefit from rehabilitation but should also identify what component(s) of the process led to these benefits. Meaningful conclusions regarding the benefits of the program require robust evaluative instruments. It is generally recommended that outcomes such as dyspnea, activity, and exercise capabilities should be evaluated, because these areas should improve with pulmonary rehabilitation.

Although an emerging body of literature suggests that pulmonary rehabilitation is beneficial in patients with disorders other than COPD (102, 103, 110, 259–268), this level of evidence has not reached the magnitude of that for COPD. Many of the outcome tools used in pulmonary rehabilitation have only been tested in COPD and require validation studies to establish their effectiveness. Generic questionnaires such as the Medical Outcomes Study Short Form 36 (SF-36) may be appropriate in these patients (269).

Patients with interstitial lung disease may achieve substantial gains in functional status by virtue of improving knowledge and skills for coping with symptoms, using energy conservation and pacing techniques, or using assistive equipment for activities of daily living. Persons with respiratory impairment related to advanced degenerative neuromuscular disease may have limited tolerance for traditional exercise training, but may achieve improved functional status through education, secretion clearance techniques, pacing and energy conservation techniques, use of adaptive assistive equipment, and NPPV. Thus, health care providers must think broadly regarding ways in which pulmonary rehabilitation may benefit patients with non-COPD diagnoses. Age- and disease-appropriate outcomes assessment tools must be considered (270).

The outcome measures described in this section are most commonly used in pulmonary rehabilitation and many have been designed primarily for patients with COPD. Further research is needed to develop outcome assessment tools that are specific for respiratory diseases other than COPD. In the absence of disease-specific outcome tools, the assessment should focus on the symptoms and functional limitations of that population.

Symptom Evaluation
The two major symptoms in patients referred to pulmonary rehabilitation are dyspnea and fatigue (271–274). These symptoms are complex, with multiple mechanisms of action (275, 276), and comprehensive reviews are available elsewhere (76, 275, 277). By nature, symptoms are subjective and require self-reporting. In the pulmonary rehabilitation setting, dyspnea or fatigue can be assessed in two ways: (1) in "real time" or (2) through recall (