Clinical nutrition, enteral and parenteral nutrition

Quality of dietary intake in relation to body composition in patients with chronic obstructive pulmonary disease eligible for pulmonary rehabilitation

Abstract

Background/Objectives:

A poor dietary quality may accelerate disturbances in body composition in chronic obstructive pulmonary disease (COPD), but only limited studies have investigated dietary intake from this perspective. The objective of the current study was to investigate dietary intake in relation to low fat-free mass and abdominal obesity in COPD.

Subjects/methods:

Dietary intake was assessed by means of a cross-check dietary history method in 564 COPD patients referred for pulmonary rehabilitation. The Dutch Food Composition Database was used to calculate nutrient intake, which was compared with the 2006 recommendations from the Dutch Health Council. Body composition was assessed by DEXA scan.

Results:

In general, the reported intake of macronutrients represented a typical western diet. With regard to micronutrients, vitamin D and calcium intakes were below the recommended levels in the majority of patients (>75%), whereas vitamin A, C and E intakes were below the recommended levels in over one-third of patients. Patients with inadequate vitamin D intake more frequently reported a low intake of protein (P=0.02) and micronutrients (P<0.001). Patients with a low fat-free mass index (FFMI) more often had low intake of protein, while abdominally obese patients more often had low intake of protein and most micronutrients (P<0.05). Patients with both low FFMI and abdominal obesity appeared most often to be consuming a poor-quality diet.

Conclusions:

Our data indicate that dietary quality is low in COPD patients referred for pulmonary rehabilitation and differs between patients with different body composition profiles.

Introduction

Chronic obstructive pulmonary disease (COPD) is characterized by a usually progressive, persistent airflow limitation and an enhanced chronic inflammatory response in the airways.1 COPD is associated with progressive disability and declined health status, although this poorly correlates with the severity of pulmonary impairment.2 There is increasing evidence in the literature that COPD should not be considered as a localized pulmonary disorder but as a systemic disease. Well-characterized systemic features are muscle atrophy and weakness and osteoporosis.3 Recently, a high prevalence of abdominal obesity was found in COPD4 as well as an elevated abdominal visceral fat mass, independent of whole-body fat mass, contributing to the increased cardiovascular risk in COPD patients.5

Common symptoms of COPD that contribute to poor appetite and altered dietary intake are dyspnoea, fatigue, anxiety and depression.6 So far, dietary intake analysis primarily focused on energy and protein balance in relation to weight loss and muscle wasting.7, 8 Dietary intake has recently also been related to COPD risk and progression. Studies have focused on individual nutrients9, 10 or foods,11 as well as on overall dietary patterns.12 Weight loss in COPD can occur due to low dietary intake not balancing elevated energy requirements13 or due to anorexia.6 In contrast, higher intake of dietary (saturated) fat is an important factor for the development of abdominal obesity.14

Surprisingly, limited studies have investigated dietary quality in more advanced stages of disease. In a small group (n=17) of Swedish elderly underweight (body mass index (BMI)20 kg/m2) patients with established severe COPD, it was reported that energy and protein intakes were in line with recommendations for healthy people.15 Intake of saturated fatty acids was higher than recommended, whereas intake of poly-unsaturated fatty acids and vitamin D was below recommendations. Furthermore, a Spanish group of 275 moderate-to-severe COPD patients reported an adequate intake of macro- and micronutrients according to local recommendations, except for vitamin D.16 A recent study on 251 COPD patients in South Korea showed that patients with different states of disease severity differed in dietary intake, as total calorie intake was higher in patients with BODE stage 1 than in those with BODE stage 2, but this was not reflected in significant differences in nutrient intake.17

The question arises whether diet represents another lifestyle factor, next to physical inactivity and smoking, that is associated with or may accelerate existing abnormalities in body composition. Therefore, the aim of the current study was to investigate the quality of macro- and micronutrient intake in relation to body composition profiles in COPD patients referred for pulmonary rehabilitation.

Subjects and methods

Subjects

The study population was recruited from CIRO+, centre of expertise for organ failure in Horn, The Netherlands, between 2006 and 2009.18 Inclusion criteria encompassed patients with COPD according to the Global Initiative for Chronic Obstructive Lung Disease (GOLD) guidelines,1 who were referred for a pulmonary rehabilitation program by chest physicians from several hospitals in the Southeast of the Netherlands. Patients without DEXA measurements were excluded. In total, 564 patients fulfilled the criteria. Because of the use of de-identified and pre-existing data, our retrospective study is exempt from institutional review board approval.

Measurements

All measurements were taken at CIRO+ before patients entered pulmonary rehabilitation, as part of a 3-day baseline assessment.18

Lung function

For pulmonary function, post-bronchodilator forced expiratory volume in 1 s and forced vital capacity were determined in accordance with the latest GOLD guidelines1 with standardized equipment (Masterlab, Jaeger, Germany).

Body composition

Total body height was measured to the nearest 0.5 cm with a wall-mounted stadiometer. Total body weight was assessed to the nearest 0.1 kg using a weighing scale, and BMI was calculated as weight/height2 (kg/m2). Body composition was measured using dual-energy X-ray absorptiometry (Lunar Prodigy system, GE Healthcare, Madison, WI, USA). Fat-free mass index (FFMI) was calculated by dividing FFM by height2, and the ratio of the percentage fat mass in the android region (waist) to the percentage fat mass in the gynoid region (hip) was used as a measure for abdominal fat mass. Low FFMI was defined as an FFMI below 16 kg/m2 for men and 15 kg/m2 for women.19 Abdominal obesity was defined as android/gynoid %fat mass below 1.0 for men and 0.8 for women.20

Dietary intake

Habitual dietary intake of the last month, including intake of oral nutritional supplements, was assessed by three trained dieticians using a validated cross-check dietary history method and calculated using the Dutch Food Composition Database. In this database, intake of alcohol is separately described but is not taken into account in the current analyses as there were no recommended daily intake (RDI) values.

Dietary intake was individually compared with gender- and age group-specific Dutch governmental recommendations in energy percentages (E%) for macronutrients and in absolute terms for specific micronutrients (vitamins A, C, D and E and calcium). These exact RDI values were used as strict cutoff values to categorize dietary intake (e.g., above RDI, adequate, or below RDI) (Table 1). Protein intake was also expressed per kilogram body weight (g/kg body weight) as recommendations are adjusted for body weight.

Table 1 Reference daily intake (RDI)

Statistical analysis

Patients were studied as a group and stratified by abnormal body composition: low FFMI or abdominal obesity, or both.

All statistical analyses were performed using the Statistical Package for Social Sciences version 20.0 (SPSS, Inc., Chicago, IL, USA). Two-sided P values<0.05 were considered statistically significant. All data were first assessed for normal distribution. Forced expiratory volume in 1 s, forced expiratory volume in 1 s/VC, protein intake (expressed in g/kg body weight), calcium and vitamins A, C, D and E were not normally distributed and were thus log transformed for analyses. Continuous variables were presented as median±interquartile range and were compared using the Student t-test for independent samples and with one-way ANOVA. Discrete variables were presented as percentages and compared using the chi-squared test.

Not all data were available for the total study group. Data for abdominal obesity classification were missing in 130 patients; lung function data were missing in two patients; and in the vitamin C data one extreme outlier was deleted.

Results

Subject characteristics

In total, 564 patients (57% men) were included in the analyses. The group was characterized by moderate-to-severe airflow obstruction (Table 2). Male patients were older than female patients, had a comparable BMI, a higher FFMI and higher degree of airflow limitation. Despite a normal median BMI, almost a quarter of the patients had a low FFMI and more than three-quarters were abdominally obese.

Table 2 Characteristics and dietary intake of the patient group, stratified by gender

Quality of dietary intake

The current COPD sample had a median total energy intake of 2018 (1664–2498) kcal. Median macronutrient composition comprised 44.3 E% carbohydrates, 37.1 E% fat, of which 13.5 E% was saturated fat, and 15.0 E% protein, representing a typical western diet. Apart from a higher total energy and vitamin D intake and a lower vitamin C intake in men, dietary intake was not significantly different between men and women (Table 2). Therefore, further analyses were performed for men and women together.

Figure 1 categorizes the macro- and micronutrient intake according to age-dependent governmental recommendations for healthy subjects. Compared with the RDI (expressed in energy percentages), only 2% of the patients had a low dietary protein intake. Nevertheless, this proportion increased to 30% of all patients when protein intake was expressed per kg body weight. Carbohydrate intake was lower than recommended in 26% of patients, whereas dietary fat intake was too high in almost one-third of the patients. In particular, saturated fat was frequently consumed too much (89% of patients). Almost all patients showed an adequate consumption of poly-unsaturated fatty acids. On the level of micronutrients, intake of vitamin D often appeared to be lower than recommended (78% of patients), followed by too low calcium intake (72% of patients). In line, absolute intake was below RDI for vitamin A (34% of women vs 48% of men; P=0.001), vitamin C (35% of patients) and vitamin E (33% of patients).

Figure 1
figure1

Quality of macro- and micronutrient intake, stratified by gender. Quality of dietary intake was compared using the chi squared test between men (n=319) and women (n=245). Results of statistical analysis showed that men differed from women in the quality of dietary intake of vitamin A. Asterisks indicate a significant difference between groups: **P<0.01.

Inadequate vitamin D intake

As vitamin D was identified as a major dietary deficiency (78% of patients), sub-analyses were performed to further compare dietary intake between patients with adequate and those with inadequate vitamin D intake (Figure 2). The subgroup with inadequate vitamin D intake had a significantly higher prevalence of too low intake of protein per kg body weight (P=0.02), as well as of vitamins A, C and E and calcium (all at P<0.001). In contrast, the prevalence of a poly-unsaturated fatty acid intake above the recommended level was significantly lower (P=0.02).

Figure 2
figure2

Quality of macro- and micronutrient intake, stratified by adequacy of vitamin D intake. Quality of dietary intake was compared using the chi squared test between patients with (n=126) and those without (n=438) adequate vitamin D intake. Results of statistical analysis showed that patients with inadequate intake of vitamin D differed from patients with adequate of vitamin D with respect to the quality of dietary intake of protein (g/kg bodyweight), PUFA, vitamins A, C, D and E and calcium. Asterisks indicate a significant difference between groups: *P<0.05, **P<0.01.

Low FFMI

Almost a quarter of the total patient group had a low FFMI (FFMI<16 kg/m2 for men and <15 kg/m2 for women). This subgroup was characterized by younger age and higher degree of airflow limitation compared with the subgroup with normal FFMI (see Supplementary Information).

Table 3 shows dietary intake after stratification for FFMI. Patients with low FFMI reported higher energy intake. Although patients with a low FFMI had a lower protein intake expressed in E%, protein intake per kg bodyweight was higher. Patients with low FFMI also had a higher carbohydrate intake but comparable fat intake. Interestingly, micronutrient intake tended to be higher in patients with a low FFMI, although this was only significant for vitamin A and calcium.

Table 3 Dietary intake after stratification for low FFMI and after stratification for abdominal obesity

Nutritional supplements were used by one-third of patients with a low FFMI in an attempt to meet their dietary requirements. Nonetheless, the percentage of patients with intakes of protein, carbohydrate and micronutrients below recommendations was lower in those using nutritional supplements than in those not using nutritional supplements (data not shown).

Abdominal obesity

More than 75% of the patients were abdominally obese (android/gynoid %fat mass >1.0 for men and >0.8 for women). This subgroup was characterized by older age and lower degree of airflow limitation compared with the non-abdominally obese subgroup (see Supplementary Information).

Table 3 shows dietary intake after stratification for abdominal obesity. Abdominally obese patients reported lower energy intake. Apart from a comparable fat intake, abdominally obese patients received proportionally more energy from protein intake and less from carbohydrate intake compared with non-abdominally obese patients. On the level of micronutrients, dietary intake of vitamins A, D and E and calcium was significantly lower in abdominally obese patients.

Low FFMI and abdominal obesity

As stratification for body composition revealed a substantial overlap in patients with low FFMI and abdominal obesity, sub-analyses were performed to further compare characteristics (see Supplementary Information) and dietary intake in patients with different body composition profiles (Figure 3).

Figure 3
figure3

Quality of macro- and micronutrient intake, stratified for low FFMI and abdominal obesity. Quality of dietary intake was compared using the chi-squared test between (a) normal FFMI and non-abdominally obese patients (n=61); (b) normal FFMI and abdominally obese patients (n=275); (c) low FFMI and non-abdominally obese patients (n=36); and (d) low FFMI and abdominally obese patients (n=62). Results of statistical analysis showed that patients with different body composition profiles differed in quality of dietary intake of protein, vitamins A, D and E and calcium. Abbreviations: FFMI, fat-free mass index; PUFA, poly-unsaturated fatty acid. I, II, III or IV: represents a significant difference at P<0.05 with respective strata number I, II, III or IV.

Only 15% of the patients had a normal body composition (normal FFMI+non-abdominally obese), whereas the majority (63%) had a normal FFMI but were abdominally obese. Merely 8.3% of the patients had a low FFMI only, whereas almost 15% showed both a low FFMI and abdominal obesity.

There were significant differences in dietary intake between the different body compositional profiles. Patients with normal body composition had the lowest prevalence of protein intake below recommendations (g/kg body weight), as opposed to patients with both low FFMI and abdominal obesity, who had the highest prevalence. In addition, abdominally obese patients with a low FFMI more often had a lower intake of vitamins A, D and E and calcium than recommended compared with non-abdominally obese patients with a low FFMI.

Discussion

The present study highlights poor dietary quality in a substantial number of COPD patients referred for pulmonary rehabilitation. Moreover, disturbances in body composition were associated with striking differences in macro- and micronutrient intake.

The results of a too low intake of protein (per kg body weight), carbohydrate, vitamins (especially vitamin D) and calcium, next to a too high intake of (saturated) fat, typically reflects the western diet, which not only increases cardiovascular risk but has also been associated with the risk and progression of respiratory disease.12

Unfortunately, no data are yet available on dietary intake in the Dutch elderly (>70 years). However, according to the Dutch National Food Consumption survey 2007–2010, 17–21% of older Dutch adults (51–69 years) had a low intake of vitamin A, a small percentage had a low intake of vitamins C and E and calcium, and the median total vitamin D intake was below RDI.21 In the COPD patients in this study, the reported percentages of patients with micronutrient intake below recommendations were remarkably higher and vitamin D was identified as the major deficiency.

The current finding of a high prevalence of inadequate intake of vitamin D in COPD patients (78%) was in accordance with earlier findings in a small group (n=17) of Swedish underweight (BMI20 kg/m2) elderly with established severe COPD. They found that intake of vitamin D was below recommendations, which may contribute to osteoporosis.15 Also, in a Spanish group of 275 moderate-to-severe COPD patients, merely 11% accomplished the daily recommendations of 10 mg/d vitamin D intake, comparable to the Dutch RDI.16 Nonetheless, it was suggested in that study that the elevated sunlight exposure in Mediterranean countries may complete the low dietary intake by a high vitamin D dermic synthesis. However, the included subjects in the present study all lived in the Netherlands, with less sun exposure than in Spain. Together with the fact that the elderly already have a poorer ability to synthesize vitamin D through the skin,22 our population might be at risk of inadequate vitamin D intake and production. Indeed, recent data from patients entering our pulmonary rehabilitation centre have shown that vitamin D deficiency, measured as plasma 25(OH)D concentration below 50 nmol/l, was present in 58%,23 which is higher than the reported 40% in healthy Dutch adults.24 Unfortunately, we did not have data on vitamin D status in the present study; thus, no correlation between vitamin D intake and plasma levels could be made. Nonetheless, previous research could not detect a correlation.23

Our finding of a low vitamin D intake deserved further investigation as vitamin D deficiency appears to be involved not only in the development of osteoporosis23 but also in several other COPD-related disease features, including impaired lung function,25 compromised immune function and impaired muscle strength and function.26 Patients with inadequate vitamin D intake had a less balanced dietary intake, as reflected by protein and micronutrients. Dietary sources for vitamin D are fatty fish, butter, dairy products and cheese, as is for calcium. Vitamin A is particularly present in animal products and liver, vitamin C in fruit and vegetables and vitamin E in vegetable oils, nuts, seeds, fruit and vegetables. Consequently, low vitamin D intake appears to reflect a poor dietary quality in general and simply recommending a vitamin D supplement would likely not cover all dietary needs in these patients. As it is also suggested that a dietary shift to higher antioxidant food intake may be associated with improvement in lung function,27 more attention to dietary quality is warranted in COPD management.

According to the recent Cochrane review, there is moderate-quality evidence for nutritional supplementation in the management of malnourished patients with COPD.28 In the current study, almost 25% of patients were characterized by a low FFMI. There was specific interest in protein intake in this subgroup as a potential limiting factor for muscle protein synthesis29 and in view of the reported elevated whole-body protein turnover.30 More than 60% of patients with low FFMI had inadequate protein intake (nutrition+supplements) per kg body weight, considering a recommended lower limit of 1.5 g/kg body weight. This level of protein intake, if possible in combination with physical exercise, is necessary to achieve a positive protein balance. Nonetheless, the prevalence of an inadequate dietary intake was lower in patients using nutritional supplements, confirming that nutrition supplementation is able to enhance dietary intake from a qualitative perspective.

Cardiovascular disease is the major cause of death in mild-to-moderate COPD patients, and abdominal obesity is a well-established risk factor.5 A very high proportion of 77% of the study population met the criteria for abdominal obesity. Although the general population reported a high fat intake, abdominally obese patients did not have a higher fat intake compared with non-abdominally obese patients. In general, abdominally obese patients had a higher prevalence of inadequate micronutrient intake. We had no data on specific food product intake, but from these results it can be suggested that the patients with abdominal obesity consume less nutrient-rich products compared with patients without abdominal obesity. Until now, no studies have reported nutrient intake in a specific subgroup of abdominally obese COPD patients. Only in the Spanish cohort were lower levels of energy and calcium intake reported in patients with a BMI30 kg/m2 compared with the remaining patients.16 However, a study on healthy Mexican elderly confirmed our findings that micronutrient intake was inadequate in obese subjects.31

Additionally, stratification for body composition revealed a subgroup of abdominal patients with low FFMI, characterized by less adequate protein and micronutrient intake. Patients with this body composition profile deserve specific attention, as the combination of low FFMI and abdominal obesity can lead to adverse metabolic health.32

Some shortcomings of the current study need to be considered. Unfortunately, no healthy control group could be included in the present analyses in order to directly compare the classification of macro- and micronutrient intake between COPD patients and healthy subjects. Nonetheless, results were compared with findings in general older Dutch adults from the Dutch National Food Consumption Survey.21 In addition, no data were available on vitamin D status to compare with vitamin D uptake, although previous research could not detect a correlation.23 Furthermore, the assessment of dietary intake could have led to some information bias, as dietary (fat) intake might be underestimated in obese subjects33 and overestimated in underweight subjects. However, based on previous research by Goris et al,7 comparing dietary intake with energy requirements assessed by doubly labelled water and accelerometry, we are inclined to rule out the possibility of overestimation of dietary intake in patients with low FFMI. Furthermore, a higher energy intake can be expected in patients with a low FFMI because of their risk for increased energy expenditure.34 In the present study, the cross-check dietary history technique was applied by trained dieticians and has the advantage that it provides a profile of habitual dietary intake, contrary to food records and 24 h-recalls. The food frequency method is generally applied in order to assess the quality of dietary intake because it is able to provide clear insight into particular food product groups. Nonetheless, food consumption might be missed by the focus on food product groups rather than on specific food products. Overall, the reliability and validity of the dietary history with cross-checks are generally accepted.35

In conclusion, we demonstrated that daily intake of macro- and micronutrients was often below recommendations in COPD patients. The greatest deficiency identified was that of vitamin D, which reflected poorer dietary quality in general. Furthermore, disturbances in body composition were associated with differences in micro- and macronutrient intake. The lowest quality of dietary intake was found in patients with abdominal obesity in addition to a low FFMI. Our findings implicate that dieticians should be aware not only of patients with low FFMI needing nutritional energy or protein-rich supplementation but also of inadequate micronutrient intake such as vitamins D, A and E and calcium in all patients.

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Correspondence to C van de Bool.

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The authors declare no conflict of interest.

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Author Contributions

Each author has participated sufficiently, intellectually or practically, in the work to take public responsibility for the content of the article, including the conception, design and conduct of the experiment and for data interpretation. The contribution of the authors to the manuscript is as follows: CvdB: study design, analysing data, drafting the manuscript, primary responsibility of the final content; CV: study design, first analyses, conducting research; FF, MS, AS and EW: study design, reviewing the manuscript; PvM: conducting research, reviewing the manuscript; ER: study design, drafting the manuscript and primary responsibility of the final content, reviewing the manuscript.

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van de Bool, C., Mattijssen-Verdonschot, C., van Melick, P. et al. Quality of dietary intake in relation to body composition in patients with chronic obstructive pulmonary disease eligible for pulmonary rehabilitation. Eur J Clin Nutr 68, 159–165 (2014). https://doi.org/10.1038/ejcn.2013.257

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Keywords

  • COPD
  • nutrition
  • dietary intake
  • body composition
  • abdominal obesity

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