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(Chest. 2003;123:1460-1466.)
© 2003 American College of Chest Physicians

Prognostic Value of Nutritional Depletion in Patients With COPD Treated by Long-term Oxygen Therapy*

Data From the ANTADIR Observatory

Edmond Chailleux, MD; Jean-Pierre Laaban, MD, FCCP and Dan Veale, MD

* From the ANTADIR Observatory, Paris, France.

Correspondence to: Edmond Chailleux, MD, ANTADIR, 66 Bd St Michel, 75006 Paris, France; e-mail: Antadir{at}magic.fr


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Background: An association between weight depletion and mortality has been demonstrated in patients with COPD, but the prognostic influence of malnutrition has not been evaluated in patients with the most severe COPD treated with home long-term oxygen therapy (LTOT).

Study objective: To analyze the prognostic value of nutritional depletion in patients with COPD receiving LTOT with respect to survival and hospitalization rate.

Design: Analysis of a national database (Observatory of Association Nationale pour le Traitement a Domicile de l’Insuffisance Respiratoire Chronique [ANTADIR]).

Setting: The national nonprofit network for home treatment of patients with chronic respiratory insufficiency (ANTADIR) founded in France in the 1980s.

Patients: A total of 4,088 patients with a diagnosis of chronic bronchitis or emphysema, FEV1/vital capacity ratio < 60%, PaO2 < 8 kPa, and treatment with LTOT between 1984 and 1993.

Measurements and results: The prevalence of malnutrition, as defined by a body mass index (BMI) < 20, was 23% in men and 30% in women. BMI was significantly correlated with FEV1 and FEV1/VC. The mean follow-up duration was 7.5 years. The 5-year survival rates were 24%, 34%, 44%, and 59%, respectively, for patients with BMIs < 20, 20 to 24, 25 to 29, and >= 30. Multivariate analysis using the Cox model demonstrated that the effect of BMI on survival was independent of age, FEV1, PaO2, and sex. Lower BMI was the most powerful predictor of duration and rate of hospitalization, independently of blood gas levels and respiratory function. The mean (± SD) annual time spent in the hospital was 29.6 ± 40.4 days for patients with a BMI < 20 vs 17.5 ± 30.1 days for patients with a BMI > 30.

Conclusion: This study showed that nutritional depletion is an independent risk factor for mortality and hospitalization in patients with COPD receiving LTOT. The best prognosis was observed in overweight and obese patients.

Key Words: chronic respiratory insufficiency • COPD • hospitalization • nutrition • oxygen therapy • survival


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Malnutrition is a well-known complication of COPD.1 The prevalence of nutritional depletion in patients with COPD is quite variable, according to the method of nutritional assessment and the population studied. Malnutrition is frequent in patients with advanced disease, especially those with severe airflow obstruction, emphysema, or chronic hypoxemia.2 3 Several studies4 5 6 7 8 have shown that a low body weight, expressed as body mass index (BMI) or percentage of ideal weight is associated with an increased overall mortality, independently of the degree of airway obstruction. In one of these studies,7 low BMI was also demonstrated to have an independent effect on mortality from COPD. The relationship between body weight and mortality was most significant in the patients with moderate COPD in the study of Wilson and coworkers,4 whereas low BMI was an independent risk factor for mortality only in the patients with severe COPD in the study of Landbo and coworkers.7 A major limitation of the studies that evaluated the prognostic value of body weight in patients with COPD is that the most severely affected patients, ie, those with severe chronic hypoxemia needing home long-term oxygen therapy (LTOT), were excluded4 7 or represented a very low proportion of the studied population.5 6 The average follow-up was only 3 years in two studies4 8 and exceeded 5 years in only one study.7

Since the early 1980s, respiratory care in France has been provided mainly by a network of nonprofit associations in the Association Nationale pour le Traitement a Domicile de l’Insuffisance Respiratoire Chronique (ANTADIR) network. Since 1984, data concerning these patients have been registered in an observatory9 ; therefore, we have used this database to evaluate the long-term prognostic value of nutritional depletion in a large population of hypoxemic patients with COPD treated with home LTOT.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Organization of the ANTADIR Observatory
ANTADIR is a nonprofit associative network founded in the 1980s to ensure technical follow-up of patients requiring respiratory support, initially with oxygen therapy (LTOT) or home ventilation, and more recently with continuous positive airway pressure. At the beginning of 1997, ANTADIR had registered 17,000 patients receiving LTOT and > 8,000 patients receiving home ventilation in the whole of France. Since its foundation, ANTADIR has collected medical data on the patients and registered these data in an observatory.9 Twenty-five of the 33 associations in the network participate in the registry, and thus 79% of the patients are registered. The data are derived from a printed prescription and administration form that has to be filled in by the prescribing physician, and is necessary for payment for the treatment by the social security system. The data derived from the form are demographic—age, sex, height, and weight—plus clinical information, including diagnosis, arterial blood gas levels, lung function test results, and details of the prescription. Height and weight were usually measured in hospital lung function laboratories by a stadiometer with the patient barefooted in indoor clothing. These data plus data on hospitalizations, treatment withdrawal, and death are recorded in a common computer program in each participating association and are collected centrally by ANTADIR, where they are edited into an annual report and a national database.

Selection of Patients
We included in this study all of the patients who received LTOT between 1984 and 1993, with a clinical diagnosis of chronic bronchitis or emphysema, an FEV1/vital capacity (VC) ratio < 60%, PaO2 < 8 kPa (60 mm Hg) on room air, and in a stable state, defined as a pH value between 7.35 and 7.45.

Analysis
Nutritional status was estimated by BMI at the time LTOT was started. Malnutrition was defined as a BMI < 20. The distribution of BMI by sex and by age was compared graphically to general data for the French population.10 Spirometric data were expressed as a percentage of normal European values.11 The alveolar-arterial gradient in oxygen (P[A-a]O2) was estimated in kilopascals from the following formula:


The correlations between nutritional and functional data were studied by linear correlations and represented graphically by dividing BMI into classes of 5 kg/m2. Population survival was calculated from the onset of LTOT by the actuarial and Kaplan-Meier methods with the closing date of January 2, 1997. The study of prognostic factors was performed using the log-rank test and the Cox semiparametric model.12 13

Annual average of hospital admissions and number of days spent in the hospital were computed for patients with follow-ups of at least 1 year. The influence of BMI, age, sex, arterial blood gas levels, and respiratory function on hospitalization rates were studied by univariate and multivariate stepwise regression.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Patient Demographic and Functional Characteristics
Data were available on 4,088 patients (3,517 men and 571 women). The demographic and functional data by sex are shown in Table 1 .


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  		Table 1. Demographic and Functional Data by Sex*

 
Prevalence of Malnutrition
The prevalence of malnutrition, defined as a BMI < 20, was 23% and 30% for men and women, respectively. Obesity, defined as a BMI >= 30, was observed in 8% of men and 13% of women. Figure 1 shows the range of BMI by age and sex in comparison to the data for the general French population. The median BMI was lower than that of the general population in both sexes and especially in the younger patients.



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  		Figure 1. Distribution of BMI by sex and age in comparison with the French population. For each age group, the boxes with bars give the percentiles 10%, 25%, 50% (median), 75%, and 90% of BMI for the patients of the study and are superimposed on the same percentile repartition of BMI in the French population from the data of Rolland-Cachera et al.10

 
Nutrition Status and Respiratory Function
Figure 2 shows the variations of respiratory functional parameters in relation to BMI. The best correlations of BMI were with FEV1 (percentage of predicted) [r = 0.229, p < 0.001] and FEV1/VC (r = 0.231, p < 0.001), so that the most malnourished patients had the most severe airflow obstruction. The correlation of BMI with VC (percentage of predicted) was much lower (r = 0.080, p < 0.001). There was a positive and weak correlation between BMI and PaCO2 (r = 0.110, p < 0.001). A negative and weak correlation was observed between BMI and P(A-a)O2 (r = - 0.130, p < 0.001). The BMI was weakly correlated with PaO2 (r = 0.041, p = 0.008). The relationships between BMI and respiratory functional parameters were observed similarly in men and women.



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  		Figure 2. Links between BMI and respiratory function. The values shown are the mean spirometric and blood gas values for each interval of BMI with the SEM. D(A-a)O2 = alveolo-arterial gradient in oxygen (D for difference).

 
Nutrition Status and Survival
At the date of analysis, 2,750 patients had died and 732 patients were alive; 606 were unavailable for follow-up, with two thirds of them having stopped LTOT and one third having entered into a long-term care institution. Mean follow-up was 7.5 years, and overall median survival was 3.5 years. Figure 3 shows the prognostic influence of BMI divided into classes of 5 kg/m2. Survival rate improves with increasing BMI and was best for obese patients (p < 0.001 by the log-rank test). The 5-year survival rates were 24% (95% confidence interval [CI], 21 to 27) for patients with BMI < 20; 34% (95% CI, 32 to 36) for BMI between 20 and 24; 44% (95% CI, 41 to 48) for BMI between 25 and 29; and 59% (95% CI, 53 to 64) for BMI >= 30. The relative risk (RR) of death with reference to subjects with a BMI >= 30 was 1.4 for subjects with BMI between 25 and 29, 1.8 for BMI between 20 and 24, and 2.4 for BMI < 20.



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  		Figure 3. Prognostic influence of BMI. Survival is calculated by the actuarial method. The initial numbers in each group were 990 (BMI < 20), 1,731 (BMI, 20 to 24), 1,003 (BMI, 25 to 29), and 364 (BMI >= 30) [log-rank, 158; degrees of freedom, 3; p < 0.001].

 
The Table 2 shows the results of the prognostic study by the Cox model. Using a multivariate analysis, the prognostic factors remaining besides age were BMI, sex, FEV1 (percentage of predicted), and PaO2. The BMI was the next most important factor to age. The prognostic influence of BMI was significant both in men and women.


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  		Table 2. Multivariate Study of Prognostic Factors by Cox Model*

 
Nutritional Status and Hospitalization
For the 3,138 patients with follow-up of at least 1 year, the annual number of days spent in the hospital was 25.4 ± 35.8 (median, 13.6) [mean ± SD] and the annual rate of hospitalization was 1.18 ± 1.21 (median, 0.84). In a univariate study, BMI was the most powerful predictor of the duration of hospitalization (r = - 0.088, p < 0.001) and of the rate of hospitalization (r = - 0.058, p = 0.001). Patients with BMI < 20 were hospitalized a mean of 1.27 ± 1.28 times by year, with a mean annual time spent in hospital of 29.6 ± 40.4 days vs 1.02 ± 1.17 times and 17.5 ± 30.1 days for patients with BMI > 30 (Fig 4 ). The annual duration of hospitalization was also negatively correlated with FEV1 percentage of predicted (r = - 0.061, p = 0.001), VC percentage of predicted (r = - 0.041, p = 0.021), FEV1/VC (r = - 0.040, p = 0.023), and PaO2 (r = - 0.044, p = 0.013). Similarly annual number of hospitalizations were correlated with FEV1 percentage of predicted (r = - 0.045, p = 0.011), VC percentage of predicted (r = - 0.042, p = 0.017), and PaO2 (r = - 0.042, p = 0.018). By multivariate stepwise regression, predictive factors of annual duration of hospitalization were BMI (p < 0.001), FEV1 percentage of predicted (p = 0.018), and PaO2 (p = 0.024); for annual number of stays, BMI (p = 0,002), PaO2 (p = 0.033), and VC percentage of predicted (p = 0.036).



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  		Figure 4. Influence of BMI on hospitalizations. The values shown are the mean annual total of days spent in hospital and the mean annual rate of hospital admission for four intervals of BMI (with the SEM), calculated in 3,138 patients with a follow-up of at least 1 year.

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
This study shows that nutritional depletion defined by a low BMI was associated with increased mortality and hospitalization rates, independently of the severity of airway obstruction in a large population of hypoxemic patients with COPD treated with home LTOT. The highest survival and lowest hospitalization rates were observed in obese patients.

Other epidemiologic studies have demonstrated that malnutrition is a predictor of mortality in patients with COPD, but the patients with severe chronic hypoxemia needing home LTOT were excluded in these studies.4 7 In 2,132 patients with COPD from the Copenhagen City Heart Study cohort (with a mean FEV1 of 65% predicted in men and 66% predicted in women), Landbo and coworkers7 showed that BMI had an independent effect on all-cause mortality and respiratory mortality only in patients with FEV1 < 50% predicted. A retrospective analysis of the Intermittent Positive-Pressure Breathing trial,4 in 779 male patients with COPD with PaO2 >= 55 mm Hg, confirmed that mortality increased with decreasing body weight, but the relationship between mortality and body weight was surprisingly not significant in the patients with the most severe airflow obstruction (FEV1 <35% predicted). In the Intermittent Positive-Pressure Breathing study,4 the criterion of malnutrition was a body weight below 90% of ideal body weight taken from the Metropolitan Life Insurance Company tables. These norms are for a population of 25- to 59-year-old Americans, while most patients with COPD are > 60 years of age. Gray-Donald and coworkers5 showed, in 348 patients with COPD with FEV1 < 50% predicted recruited for a clinical trial of negative-pressure ventilation, that a low BMI was a predictor of all-cause mortality in multivariate analysis after controlling for age, gender, current smoking status, the use of home oxygen and FEV1. Although this study included very few patients treated with home oxygen (16% of the study population), the hazard ratio for a 5 kg/m2 increase in BMI was very close to the figure found in our study (0.73 vs 0.75, respectively). In the retrospective study of Schols and coworkers6 including 400 patients with COPD admitted to a pulmonary rehabilitation center, a low BMI was shown to have a negative effect on survival, independently of other prognostic factors. The percentage of patients treated with LTOT was not specified by the authors, but it was probably low since the mean PaO2 was 9 kPa in the study population. In 135 patients with COPD and moderate hypoxemia (PaO2 of 56 to 65 mm Hg), randomly allocated to LTOT and a control group, Gorecka and colleagues8 found that BMI was a significant predictor of survival, independently of FEV1, but the prevalence of malnutrition was not provided by the authors.

It has been demonstrated that malnutrition is also associated with a poor outcome following an acute exacerbation of COPD. A decrease in active cell mass estimated from bioelectrical impedance analysis has been reported to be associated with a high ICU mortality rate in patients with COPD with acute respiratory failure.14 In a prospective cohort of 1,016 patients with COPD who were hospitalized with an acute exacerbation and hypercapnia, Connors and coworkers15 showed that the 6-month survival rate was independently related to BMI. Among the eight variables that were significantly related to survival in multivariate analysis, BMI had the best prognostic value next to an acute physiologic score.

In addition to the consequences of low body weight on mortality, malnutrition has been shown to be related to morbidity in acutely ill patients with COPD: increased need for mechanical ventilation in acute exacerbation,16 increased risk of early nonelective readmission in patients previously admitted for an exacerbation,17 increased duration of ventilatory support following lung transplantation18 or lung volume reduction surgery.19 A relationship between malnutrition and morbidity has also been reported in patients with COPD in clinically stable condition: increase in the severity of dyspnea,20 decreased exercise capacity,21 and greater impairment in health-related quality of life.22 These consequences of low BMI on morbidity could not be addressed in our study. We have now shown that low BMI was correlated with frequency and duration of hospitalization in a severely affected COPD population.

The prevalence of malnutrition, defined as a BMI < 20, was high (23% in men and 30% in women) in our study including patients with COPD and severe chronic hypoxemia treated with home LTOT. In patients with COPD with severe airflow obstruction in whom home LTOT was not required in 84% of cases, the prevalence of low BMI was reported to be 18%.5 The prevalence of low BMI was found to be much lower in patients with less severe COPD recruited from the general population, reaching 5% in men and 15% in women.7 The prevalence of nutritional depletion was reported to be very high in patients with acute respiratory failure and in patients accepted for lung transplantation, with values up to 60% and 72%.18 23 The use of body weight as the sole criterion of malnutrition may have led to an underestimation of nutritional depletion in our study population. Indeed, body composition measurements using bioelectrical impedance analysis have shown that depletion of fat-free mass occurred in 36% of 255 patients with COPD in stable clinical conditions admitted to a pulmonary rehabilitation center, while depletion of fat-free mass occurred in the absence of low body weight in 10% of the patients.2

A relationship between nutritional status and respiratory function in COPD has long been noted. Several studies3 4 8 have reported a positive correlation between body weight expressed as percentage of ideal weight or BMI and FEV1. It is noteworthy that such a correlation between BMI and indexes of airflow obstruction (FEV1 and FEV1/VC) was also found in our study, although only patients with severe airflow obstruction were included. We observed a drop of VC in the patients with low BMI, and this may reflect the effect of nutritional depletion on respiratory muscle function.24 A positive correlation between BMI and carbon monoxide diffusing capacity has been reported, suggesting that malnutrition is more prevalent in patients with emphysema than in those with chronic bronchitis.3 25

Overweight and even obesity were associated with an improved survival in our study. This surprising finding has been found by other authors,4 5 6 7 although obesity is usually associated with an increased mortality that mainly results from an increased cardiovascular risk. There is no clear pathogenic mechanism that could explain why obesity should improve the survival of patients with severe COPD. It has been suggested that obese patients with COPD are better protected from a decrease in body cell mass during periods of acute illness because of higher energy reserves.5 Another hypothesis is that obesity in itself contributes to low FEV1, so that obese patients with COPD classified as having severe COPD may in fact have a less severe airflow obstruction and therefore a better survival.7

In conclusion, this study showed that nutritional depletion is an independent risk factor for mortality and hospitalization in patients with COPD patients treated with home oxygen. The best prognosis was observed in overweight and obese patients.


   Acknowledgements
 
The authors thank all the Regional associations who provide data to the Observatory: AIR Angers, AVD Angoulême, DDS Besançon, AVAD Bordeaux, AIR Caen, AIRRA Clermont-Ferrand, ALIZE Dijon, ADAIR Fouquières, AGIR Grenoble, GHAHR Le Havre, ARARR La Réunion, SANTELYS Respiration LILLE, ALAIR Limoges, ARARD Marseille, APARD Montpellier, AIR Mulhouse, ARAIRLOR Nancy, ARIRPLO Nantes, CARDIF Paris, ARAIRCHAR Reims, AADAIRC Rochefort, ADIR Rouen, ADIRAL Strasbourg, SADIR Toulouse, and ARAIR Tours.


   Footnotes
 
Abbreviations: ANTADIR = Association Nationale pour le Traitement a Domicile de l’Insuffisance Respiratoire Chronique; BMI = body mass index; CI = confidence interval; LTOT = long-term oxygen therapy; P(A-a)O2 = alveolar-arterial gradient in oxygen; RR = relative risk; VC = vital capacity

Received for publication May 28, 2002. Accepted for publication November 25, 2002.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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