chronic obstructive pulmonary disease A.M.W.J. Schols, J. Brug Dept of Respiratory Medicine, University Hospital Maastricht, The Netherlands. Correspondence: A. Schols, Dept of Respiratory Medicine, University Hospital Maastricht, PO Box 5800, 6202 AZ Maastricht, The Netherlands. Weight loss and related muscle wasting are common complications among patients with chronic obstructive pulmonary disease (COPD) [1]. Clinical studies, as well as recent population studies, have clearly shown that involuntary weight loss and being underweight are related to increased mortality, regardless of disease severity [2]. In moderate-to-severe COPD, weight loss has also been related to decreased functional capacity and increased morbidity i.e. the outcome of acute exacerbations. It is therefore deemed important to encourage and help patients to avoid weight loss and/or to help them regain weight. Epidemiological studies have indicated a role of dietary habits in the aetiology of COPD [3, 4]. The present chapter aims to summarise the potential strategies for diet and nutrition in the prevention and management of COPD, and discusses evidence for the effectiveness of nutrition and dietary change interventions among COPD patients. Behaviour analysis: diet, nutrition and health among chronic obstructive pulmonary disease patients COPD has been associated with diet and nutrition in two ways. First of all, weight loss and muscle wasting is a common complication in COPD patients. Reported prevalence rates range from 20% in COPD outpatients [5] to 35% in patients participating in a pulmonary rehabilitation programme [6] and even to over 70% in patients with acute respiratory failure [7]. Regardless of disease severity, weight loss is related to increased morbidity in terms of the risk of acute exacerbations [8], hospital readmission [9] and the need for mechanical ventilation [10]. More specically, loss of lean body mass is related to decreased muscle function, which may also affect the respiratory muscles [11], exercise performance [12] and health status [13, 14]. Besides a role in disease progression, dietary habits have been implicated in the onset of the disease. Recent epidemiological studies indicate that diet may be related to COPD risk and, hence, that diet and nutrition could play a role in the primary prevention of COPD. Smit et al. [4] reviewed the literature on a possible relationship between diet and the indicators of COPD and asthma. Associations have been suggested between COPD risk and the intake of n-3 fatty acids, antioxidants, and fruit and vegetables. n-3 Fatty acids are polyunsaturated fatty acids (PUFAs) that are particularly common in fatty sh, and the metabolites of n-3 PUFAs can indirectly inhibit the production of pro-inammatory mediators. The evidence for a relationship between PUFA consumption and COPD risk is not straightforward. While a number of studies have indicated that a high intake of sh is associated with lower risk, other Eur Respir Mon, 2003, 24, 142152. Printed in UK - all rights reserved. Copyright ERS Journals Ltd 2003; European Respiratory Monograph; ISSN 1025-448x. ISBN 1-904097-27-8. 142 observational studies did not nd such an association, and no n-3 PUFA supplementa- tion intervention studies among symptom-free subjects have been published. Antioxidant nutrients, such as vitamins C and E, as well as antioxidant non-nutritive substances such as avonoids, may prevent air pollution-induced oxidative stress in the lungs. Experiments to study the value of antioxidant supplementation in protecting against oxidative air pollution have shown that this is indeed possible, but eld experi- ments have so far failed to show any effects of antioxidant intake or supplementation on COPD risk. The evidence for a protective effect of fruit and vegetables (one of the main sources of antioxidant nutrients) is somewhat stronger. For example, various cohort studies such as the Seven Countries Study [3] and the Morgen Study [15] have observed a negative association (indicating a protective effect) between fruit intake and 25-yr COPD incidence and mortality. In summary, although there is some evidence that consumption of sh and fruit may be benecial in COPD prevention, this evidence is not conclusive enough to warrant nutrition education promoting fruit and sh consumption strictly from a COPD prevention point of view. COPD is associated with loss of weight and related functional decline. Besides optimising the treatment of patients who are already underweight, it may be important to detect and reverse weight loss as soon as possible and to avoid further weight loss among COPD patients in order to avoid functional decline. This may be achieved by increasing dietary intake per se or by altering dietary habits to include different (energy-dense) foods and optimum timing of meals/snacks in relation to symptoms and activity patterns. The evidence that certain dietary habits may contribute to COPD prevention is not yet substantial enough to warrant specic dietary advice aimed at avoiding COPD. Conversely, potentially preventive dietary habits, such as consumption of fatty sh and fruit, are in line with general recommendations for a healthy diet [16]. Determinants of energy balance among chronic obstructive pulmonary disease patients Clinically stable disease Although it is an established fact that severe COPD is often related to loss of body weight, it is not fully understood why COPD patients may lose weight, and especially why they may show muscle wasting. Weight loss is always the result of a negative energy balance, i.e. an energy expenditure (EE) exceeding energy intake (EI). Weight loss among COPD patients has been attributed to both sides of this balance. Patients with COPD often have increased energy requirements, probably caused by increased respiratory muscle activity [1, 17]. As a consequence of (dynamic) hyperination, breathing is less efcient for some COPD patients than for healthy subjects of the same age and sex. Further evidence points to the possibility that COPD patients have an increased anaerobic metabolism, related to intrinsic abnormalities in skeletal muscle morphology and metabolism, which is relatively inefcient in EE [1]. Thus, an obvious choice to improve their energy balance might be to decrease EE. However, according to the recent Global Initiative for Chronic Obstructive Lung Disease guidelines [18], pulmonary rehabilitation is an "evidence-based" key intervention to improve limited functional abilities and health status, and preliminary evidence points to the conclusion that high- intensity exercise may improve the oxidative capacity of the muscles. Since COPD patients may have an increased energy metabolism and should at the same time be advised to increase exercise, restricting energy output will be hard to realise and may not be desirable. This implies that COPD patients who suffer from weight loss should be NUTRITIONAL INTERVENTION 143 encouraged to increase their often apparently normal EI as well as their protein consumption. This could avoid weight loss, specic loss of lean body mass, and a related decrease in functional ability, or could help them regain weight. Acute exacerbations In the majority of patients, weight loss appears to develop gradually, indicating a chronic imbalance between dietary intake and EE. In a subgroup of patients, however, weight loss and muscle wasting follows a stepwise pattern related to acute exacerbations, suggestive for additional factors that aggravate the imbalance during stable periods. Two studies have investigated the effect of an acute exacerbation requiring hospitalisation on the nutritional and metabolic prole of patients with COPD [19, 20]. They have shown that the majority of patients have a decreased intake prior to hospitalisation. During the rst days of hospitalisation, a very low dietary intake is reported that may improve spontaneously during the remaining hospital period parallel to recovery from the exacerbation. In addition to the decreased dietary intake, resting energy expenditure (REE) is increased during the rst days of hospitalisation, decreasing thereafter. A subgroup of patients, however, seems to have another pattern of REE during exacerbation. In this group, REE does not decrease during hospitalisation. Moreover, these patients appeared to have an even higher REE at admission and a lower body mass index (BMI) than the patients who have the decreasing pattern of REE during admission. This group, which remained hypermetabolic at discharge, was characterised by a low BMI. Interestingly, it was shown in another study that a subgroup of patients, with a high risk of nonelective readmission to the hospital for an acute exacerbation, had a lower BMI and lost weight during admission, while patients with low risk for readmission were weight stable [9]. These two groups were not different with respect to common markers of disease severity. Besides a decreased caloric intake, a decreased daily protein intake has been reported prior to and during the rst fewdays of hospitalisation, gradually increasing thereafter [19]. In addition, a negative nitrogen balance has been reported, indicating loss of protein and thus muscle mass [21]. This negative nitrogen balance was strongly correlated with the dose of systemic glucocorticosteroids. The current studies indicate that during hospitalisation the focus of nutritional intervention should aim at maintenance of a net positive energy balance with particular attention to protein intake to limit protein catabolism. During recovery at home, the focus in underweight patients can shift from maintenance to net anabolism by a combined strategy of nutritional support and exercise. Potential determinants of dietary behaviour Derived from chronic obstructive pulmonary disease research Tailoring dietary change interventions to these COPD patients requires identication of the determinants of the risk behaviour (e.g. why do some COPD patients have an insufcient EI, either in absolute or in relative terms?). Some research has been conducted into possible determinants of reduced and inadequate EI in COPD patients. Insufcient food intake has been found to be associated with various COPD-related factors. Chewing and swallowing may be impaired in COPD patients since both activities change the breathing pattern and may, therefore, decrease oxygen uptake [1]. Gastric lling in COPD patients may reduce the functional residual capacity of the lungs and lead to dyspnoea. Since dyspnoea results in fatigue, less time may be spent eating, leading to a lower EI [22]. There is also evidence that chronic mouth A.M.W.J. SCHOLS, J.BRUG 144 breathing may change taste perceptions in COPD patients [22, 23], which may decrease the attractiveness of foods they are used to. Further, certain medications and disease- related depression and anxiety may also cause changes in taste perceptions and decreased appetite. Finally, recent studies point towards altered regulation of the appetite- stimulating hormone leptin in patients with COPD, possibly caused by the presence of a systemic inammatory response [20]. According to behavioural theory The Health Belief Model, the Theory of Planned Behaviour and its predecessor the Theory of Reasoned Action, the Social Cognitive Theory, the Protection Motivation Theory and the Transtheoretical Model [24] have all been used to study correlates or determinants of dietary behaviour [25]. Based on these models, at least three categories of important as well as changeable proximal determinants of dietary behaviour have been identied that can be addressed with health education techniques [25, 26]: weighing (expected or perceived) pros and cons (attitudes), social inuences and perceived control. These factors are assumed to inuence dietary behaviours mostly via behavioural intentions. In these models, factors such as sex, age or socioeconomic status are regarded as more distal correlates of dietary habits [27]. Such models have also been used, although only sparsely, to study health behaviours among COPD patients [2830] and have been used to develop nutritional interventions for COPD patients [31]. Each of these three central theoretical determinants are described below. Attitudes Rational human behaviour is supposed to be inuenced by an evaluation of so-called outcome beliefs, i.e. the most salient expected consequences of that behaviour. The result of this evaluation is a behavioural attitude. Two of the above-mentioned models specically emphasise health-related beliefs and risk perceptions as important determinants of health (risk) behaviour: the Health Belief Model and the Protection Motivation Theory. There is evidence that risk perceptions may only be strong determinants of food choice when a health threat is perceived to be the direct result of a specic food or a specic dietary practice [25]. For most COPD patients, however, a low-calorie diet is not followed by immediate sickness; in fact, consuming more calories may lead to greater discomfort. In general, two categories of patients can be distinguished in terms of diet and COPD. First, there are patients with an apparently adequate EI who nevertheless lose weight over a longer period of time. The unhealthy consequences of their inadequate EI only become apparent after several months or even years. Such long-term negative effects are usually not very effective in shaping behaviours, especially when the immediate effects present a different message. Feedback strategies, for example providing feedback about weight and caloric intake, may be useful in making longer term consequences more salient [32]. Another aspect is that such patients may experience negative reactions from their social environment to an increased intake of foods to elevate energy, since "over-eating" is not regarded as socially desirable, especially if no obvious weight loss is visible. A second group of patients consists of those with an obviously inadequate EI, who lose signicant amounts of weight within a relatively short time span, e.g. within weeks. For these patients, the negative health consequences are much more obvious and health beliefs may therefore play a more important role. For patients who expect (or have experienced) discomfort from higher EI, because of dyspnoea from increased food intake and related gastric lling, this outcome should be avoided as much as possible. Patients NUTRITIONAL INTERVENTION 145 should be encouraged to exchange energy-poor foods for energy-dense foods, and to increase the frequency of food intake instead of the amount of food eaten per meal. Beliefs about the taste and hedonic consequences of foods or meals have been identied as probably the most important determinant of food choice [33, 34]. Most taste preferences are learned and can therefore be unlearned [35], but people will not willingly eat what they dislike (or have learned to dislike). Healthy people seem to be especially prone to learning to like foods that are high in calories. Undernourished COPD patients should be encouraged to eat calorie-dense foods and to eat such foods frequently. However, nutrition education in "Western" countries has for decades been aimed at discouraging people from eating high-calorie foods, and from frequent snacking, in order to contribute to the prevention of cardiovascular disease, obesity and certain cancers [25]. Frequently eating high-calorie foods is therefore generally regarded as an unhealthy choice. Underweight COPD patients have to be persuaded to think and act differently. Social inuences Although meals are increasingly no longer consumed in a traditional family setting, having a meal is still a more or less social behaviour. Normative beliefs ("what we believe that people who are important to us want us to eat") and modelling ("what we believe that these others eat themselves") are potentially important determinants of eating behaviour [3638]. Trying to eat less, and avoiding calorie-dense foods is and should be the social norm for most people. Further, the dietary advice for weight-stable COPD patients is to eat a "healthy diet", which is usually interpreted as a diet according to the general dietary recommendations, i.e. low in (saturated) fat, high in bre, containing complex carbohydrates and including large quantities of fruit and vegetables. Finally, initial weight loss may be met with positive feedback from the social environment, since leanness is generally regarded as socially desirable. Weight-losing and underweight COPD patients will therefore have to adopt an eating pattern that contrasts with the social norm, as well as with what they were advised to do themselves before weight loss became manifest. High-protein, high-carbohydrate diets are recommended for severe COPD cases [39]. Behaviour changes away from a habitual pattern and also in a direction opposite to the social norm are often extremely difcult. In such cases it may be important to establish patient peer groups that strive for similar dietary change goals [40]. Within such groups, group norms can be established that differ from the population norms, group members can be each others role models and can provide mutual social support. Today, virtual support and self-help groups are possible and effective, for example, via the internet. In addition, it should be standard procedure for health professionals to increase social support and establish norms, pay attention to the patients nutritional status and, if weight loss is observed, provide adequate dietary advice. As in most countries, a number of health professionals in the Netherlands could play a role in health education for COPD patients, including general practitioners, pulmonologists, physiotherapists, dietitians and (specialist COPD) nurses. It is important that these caregivers and other health professionals provide a consistent message on diet and nutrition and that this message is communicated repeatedly. Research has shown that this is often not the case [41]. COPD patients are often also, to a certain extent, dependent on others for their dietary intake. A spouse or other close relative may buy, prepare and serve the food [42]. This means that in order for these patients to change their diet, their social environment should also make changes. Dietary change interventions aimed at COPD patients should, therefore, at least include those people from the patients direct social environment who A.M.W.J. SCHOLS, J.BRUG 146 are important in the patients food choice. Since the dietary recommendations for patients may differ substantially from those for their healthy family members, special meals may have to be prepared for the patients. This is necessary to avoid the whole family adopting a high-calorie diet with frequent small meals that may be better for the patients but is not regarded as healthy for other people. This may be an important barrier toward lasting dietary changes. Self-efcacy and perceived behaviour control Self-efcacy is dened as the perceived abilities and opportunities to enact a given behaviour [43]. If people are not condent that they are able to maintain a certain diet, they will be less motivated to try and less persistent in their attempts. In terms of the topic of the present chapter, COPD patients self-efcacy with regard to EI would be their condence in their abilities and opportunities to consume food with an adequate amount of calories, and lack of condence would be a negative determinant of caloric intake. Self-efcacy has been found to be a signicant predictor of self-management behaviour among COPD patients [28, 29]. At least four situations have been identied that are perceived as potentially problematic for self-management behaviour: when medical supervision is lacking, when instructions are not clear or inconsistent, when no social support is present, and when no regular check-ups are available [29]. Improving self- efcacy can be accomplished via so-called enactive mastery experiences, observational learning and specic educational activities [44]. Enactive mastery experiences are successful prior experiences. On the basis of such experiences, patients learn to evaluate whether they possess the abilities necessary to succeed in a particular behaviour or in new but similar behaviours. Observational learning can be accomplished by watching and learning from (the skills, strategies etc.) other patients who have successfully increased their calorie intake. An additional important emotional barrier that may impede patients adopting a diet higher in calories is dyspnoea-related fear. Increasing self-efcacy to manage this fear is a major challenge for COPD self-management [28]. Specic instructions to eat calorie- dense foods and snacks frequently, instead of increasing meal sizes, may help to avoid or to decrease mealtime dyspnoea. Interventions aimed at improving the nutritional status of chronic obstructive pulmonary disease patients Nutrition education is the tool most commonly applied to encourage people to adopt healthier diets. Other approaches are so-called environmental changes, i.e. expanding the availability of preferred foods, or direct prescription of dietary supplements. Diet and nutritional interventions for COPD patients have focused mainly on direct dietary supplementation by way of therapeutic nutritional support to help COPD patients stop or reverse their weight loss. However, this focus is relatively recent, since weight loss was long regarded as inevitable for severe COPD patients. Therefore, to date, few well- controlled studies (i.e. randomised controlled trials; RCTs) have been conducted to investigate nutritional interventions in COPD management. Such studies may provide information about the feasibility of dietary change, or at least changes in EI, among COPD patients. Further, such studies may provide indications of whether the association between weight loss and health status among COPD patients is a causal relationship, i.e. whether avoidance of weight loss or regaining weight results in better health. Ferreira et al. [45] recently reviewed the available studies on therapeutic dietary NUTRITIONAL INTERVENTION 147 supplementation in a meta-analysis. They managed to select only six RCTs that were considered to be of sufcient quality, of which two were double-blinded. The pooled effects, based on the analysis of a total of 277 subjects, as well as the results of the individual studies, showed that the effect of nutritional support on anthropometry was minor at best and generally did not achieve clinical importance nor statistical signicance. Five of these studies used oral supplementation and four were conducted among outpatients. These results contradict to some extent the results reported by Baldwin et al. [46], who reviewed the literature on dietary advice and supplementation interventions for patients with disease-related malnutrition in general. Their conclusion was that dietary supplementation resulted in better effects on body weight than dietary advice. The review by Ferreira et al. [45] made no distinction between what may be called "failure to intervene" on the one hand and "failure of the intervention" on the other. In some of the papers on which the meta-analysis was based, patients took the prescribed dietary supplements to replace regular meals rather than as an additional calorie input. In such cases the intervention failed to achieve a relevant increase in EI and therefore no weight gain could be expected. In the studies that did accomplish increased EI, functional improvements were also observed [4749]. Further, studies investigating the effect of dietary supplementation are often conducted among severe COPD cases, in whom a specic negative protein balance is often observed, caused by inammation, decreased blood levels of anabolic hormones, and hypoxia. Such a negative protein balance cannot be treated by dietary supplementation alone. However, the meta-analysis and related studies do show that increasing EI among severe COPD cases is difcult to accomplish, and if EI is not increased, weight and functionality will certainly not improve. The authors argue that because dietary supplementation interventions among severe COPD patients are intensive and in some patients insufcient, interventions should also be extended to prevention and early treatment of weight loss, that is, before patients are extremely wasted. Few studies have been published on the possibilities and effects of voluntary dietary change among outpatients [29, 31]. Diet is often part of the focus in self-help or self- management programmes for COPD patients and some of these programmes have been evaluated. However, there have not been any well-controlled studies of the prevention of weight loss among COPD collecting specic data on diet and nutrition. Conclusion COPD is a prevalent and serious condition in which diet and nutrition may be an important factor, possibly in COPD prevention and most probably in COPD management. There are some indications from epidemiological studies that dietary factors may decrease COPD risk. The available evidence is, however, not (yet) substantial enough to warrant dietary recommendations for primary prevention of COPD [4]. Substantial evidence does point to the conclusion that weight loss is an important negative factor in COPD management or tertiary prevention. Nevertheless, nutritional support for severely underweight COPD patients may have only a very limited effect on the recovery of functional exercise abilities, because compliance (i.e. truly increased EI) appears to be difcult [45]. The potential effect of dietary and nutritional interventions in COPD management may be greatest if the interventions are extended to early detection and further prevention of weight loss in less severe cases of COPD. This means working with outpatients before they have become underweight, and greater focus placed on dietary change than on medically prescribed supplementation to improve nutrition. Prevention of weight loss among outpatients assumes (voluntary) adjustment of dietary behaviour. A.M.W.J. SCHOLS, J.BRUG 148 Health professionals may play an essential role in encouraging patients to make and maintain these changes [29] and it is important that the various health professionals who are involved in the treatment and counselling of COPD patients pay consistent attention to nutritional status and give consistent dietary advice. Cooperation between the various health professionals is therefore necessary. Attempts have been made and are still being made to develop dietary advice protocols to facilitate the necessary cooperation and consistency. Nevertheless, dietary changes among primary care and outpatients will have to be achieved by the patients themselves. Dietary change among COPD patients will, therefore, require a combination of diet counselling and self-management. In conclusion, diet and nutrition are important in COPD management. Health professionals should be aware of potential nutritional problems, i.e. weight loss, among COPD patients, preferably in the early disease stages. This will allow them to detect initial weight loss and to encourage patients to prevent wasting by changing their diets to include more calories and protein. A combination of diet counselling and self- management, based on achieving a considered decisional balance and attitude change, goal setting, building skills and self-efcacy, and feedback strategies to prevent relapse, may be a promising approach to achieve the required dietary change. Summary Chronic obstructive pulmonary disease (COPD) is a prevalent and serious condition. Nutrition might play a role in COPD prevention and is denitely important in COPD management. There are some indications from epidemiological studies that dietary factors such as ample consumption of fruit and sh may decrease COPD risk. The available evidence is, however, not substantial enough to warrant dietary recommendations for primary prevention of COPD. Substantial evidence does point to the conclusion that regardless of disease severity, weight loss is related to decreased exercise capacity, health status and mortality, as well as to increased morbidity among patients with moderate-to-severe COPD. Current nutritional support strategies have primarily focused on treatment of clinically stable but severely underweight and disabled patients. Limited data is available regarding the role of nutritional intervention during acute exacerbations. In an inpatient setting or when incorporated in a pulmonary rehabilitation programme, nutritional support has proven effective in inducing weight gain and related functional improvements. However, such interventions are only feasible for a selected group of patients and are very laborious. Therefore, opportunities for dietary and nutritional interventions in COPD management should be explored, aiming at early detection, prevention and early treatment of involuntary weight loss. This means expanding the target group to include COPD outpatients and primary care patients before they have become underweight, and putting more emphasis on dietary change than on medically prescribed supplementation. Successful intervention assumes (voluntary) adjustment of dietary behaviour, and health professionals may play an essential role in encouraging patients to make and maintain these changes. Achieving dietary change among COPD patients may require a combination of diet counselling and self-management. Keywords: Chronic obstructive pulmonary disease, diet, nutrition, prevention, self- management, therapy. NUTRITIONAL INTERVENTION 149 References 1. Schols AM. Nutrition in chronic obstructive pulmonary disease. Curr Opin Pulm Med 2000; 6: 110115. 2. 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