General characteristics
The present study which included male COPD patients with moderate to severe airway obstruction showed that dietary intake and habitual food consumption differ in relation to fat-free mass index. The link between aging and the pathogenesis of COPD is strongly supported [
10] and longer duration of the disease since diagnose in severe COPD patients in our study can be explained by the progressive nature of the disease [
1]. Cigarette smoking is the most important environmental risk factor for the development of COPD [
13]. In our study the mean age for starting to smoke corresponded to adolescence, similar to the findings of a recent study by Kim et al. [
14], who found the mean initiation age of smoking of COPD patients as 16.4 ± 4.8 years.
In the current study 18.5% of patients were characterized by a low FFMI. Similarly, a study among 72 COPD outpatients suffering from a moderate degree of airflow obstruction showed that prevalance of fat-free mass depletion was 18% in male patients [
15]. In another study, among moderate to severe COPD patients the prevalance of fat free mass depletion was 20.3% in male patients [
16]. A recent study by Van de Bool et al. [
11] showed that almost 25% of moderate to severe COPD patients who were eligible for pulmonary rehabilitation were characterized by a low FFMI. These little discrepancies may be explained by different inclusion criteria of the studies. On the other hand, in a cross-sectional study among male COPD patients, depletion of fat-free mass based on fat-free mass index was about 42% [
17]. This discrepancy can be due to more severe COPD being present in the study as they mentioned that the prevalance of low FFMI was high among severe to very severe (stage IV) COPD patients.
Increased BMI does not protect against fat-free mass depletion in COPD, since there is a preferential loss of muscle tissue in this disease [
18]. In our study 8% of the patients had low FFMI despite a BMI ≥21 kg/m
2. A study by Pirabbasi et al. [
17] showed that among 271 male COPD patients 11.1% had a low FFMI (<16 kg/m
2) despite a normal BMI (≥21 kg/m
2). In the study by Vermeeren et al. [
16], the prevalence of being underweight was 17% whereas prevalence of FFM depletion was 42%. It should be noted however that in their study they used <18.5 kg/m
2 as the BMI cutoff for being underweight.
Nutritional intake and habitual food consumption
In the current study, mean daily energy intakes of COPD patients was 1906 kcal similarly to a group of 275 moderate to severe COPD patients (93% male) in Spain, whose mean daily energy intake was 2033 kcal [
19]. According to Turkey Health and Nutrition Survey-2010, mean energy intake of Turkish individuals was 1918 kcal in the 51–64 years age group and 1706 kcal in the 65–74 year age group [
20]. A study in Malaysia with 149 COPD patients showed that dietary energy intake of patients (assessed by one day or two days record) was below Malaysian RNI [
18]. Compared to the Malaysian sample, in our study prevalance of patients with energy intake below RNI is lower yet clinically significant (93% vs 75%, respectively). A recent study by Van de Bool et al., which is the only study to evaluate dietary intake of COPD patients in relation to body composition until now, showed that COPD patients with low FFMI reported higher energy intake than patients with normal FFMI [
11]. On the contrary, in the current study mean energy intake of patients in the low FFMI group was lower than normal FFMI group (1770 ± 338 and 1937 ± 606 kcal, respectively).
Selective wasting of fat-free mass is suggesting a disturbed protein balance in COPD patients [
21]; hence, protein intake of depleted COPD patients is recommended to exceed 1.5 g/kg/day [
22]. Increased protein intake and physical activity, in the form of resistance training, stimulate muscle protein synthesis in the elderly [
23]. In the study of Van de Bool et al. [
11], COPD pateints with low FFMI reported significantly higher protein intake per kg body weight. In the current study, protein intake of patients did not differ between low and normal FFMI groups. However, daily consumptions of dairy products and red meat were significantly low in the low FFMI group. This finding is considerable since high-quality protein sources such as whey protein, milk, and beef have been shown to improve protein synthetic response in the elderly [
24].
In the current study, majority of patients’ daily milk and yogurt consumption was below RNI and this finding was more marked in the patients with low FFMI. Milk proteins (casein and whey) are known for their high branched-chain amino acid (BCAA) content, which include leucine (LEU), isoleucine (ILE) and valine (VAL) [
25]. Since skeletal muscle is a major site of (BCAA) catabolism in disease state, they are used for maintenance of protein quality and repair process of tissues [
26]. Plasma levels of BCAAs, particularly leucine, are reduced in patients with COPD [
27] and a significant association was found between low levels of BCAAs and depletion of FFM [
17]. Engelen et al. showed an elevated anabolic response to sip feeding of a casein protein meal in patients with COPD [
28]. All of these findings make milk proteins an important preventive approach to conserve muscle mass in COPD.
In this study, a vast majority (92%) of the COPD patients could not meet RNI for fruits and vegetables with mean daily consumption of fruits being significantly lower in the low FFMI group compared to normal FFMI group. This finding is concerning since cross-sectional studies have showed a significant positive association between fruit and vegetable (FV) intake and forced expiratory volume in 1 s (FEV
1), with stronger evidence for fruit consumption [
29,
30]. Data from the MORGEN study showed that higher intakes of antioxidants such as vitamin C, beta-carotene and flavonoids are associated with higher FEV
1 values, compared with low intakes [
31,
32]. Moreover, Walda et al. [
33] demonstrated an inverse association between fruit intake and 20 yr COPD mortality.
The major deficiencies were assessed in magnesium and calcium intakes in the current study. Mean magnesium intake of COPD patients was 239.3 ± 89.3 mg in our study. According to National Turkish Health and Nutrition Survey (NTHNS) 2010, mean magnesium intake was 290.8 mg in the 51–64 year old group, 271.3 mg in the 65–74 year old group and 241.7 mg in 75 years and older [
20]. Mean magnesium intake of COPD patients in our study was lower than all of the age groups in the national survey. Low consumption of dark leafy vegetables, nuts and seeds due to chewing problems [
34], or legumes due to gastrointestinal disturbances [
35] might be the reason of low magnesium intake in our group of COPD patients.
Mean calcium intake in the current study was 740.2 ± 310.2 mg and 92% of the patients’ intake could not meet RNI. Calcium intake in the NTHNS-2010 was 712.7 mg in the 51–64 year olds, 677.2 mg in the 65–74 year olds and 592.6 mg in 75 years and older [
20]. In the study by Van de Bool et al. which evaluated the dietary intake of COPD patients assessed by using a cross-check dietary history in in Netherlands, calcium intake was reported as “too low” since 72% of the patients’ dietary intake could not meet the RNI [
11]. In the COPD patients in this study, the reported percentage of patients with calcium intake below recommendations was remarkably higher. In a Spanish group of 275 moderate to severe COPD patients, prevalence of complience with recommendations was 31% for magnesium and 49% for calcium and similar to our study magnesium was the major mineral deficieny [
19].
We did not find any significant differences in daily macro- and micronutrient intakes between patients with low FFMI and normal FFMI. Unlikely to our study, Van de Bool et al. recently showed that intakes of calcium and vitamin A in COPD patients with low FFMI were significantly higher [
11]. The consumption of legumes, dairy products, fruits and vegetables were lowest as majority of the patients’ intakes did not comply with the recommendations in our sample. In a Spanish group of 275 moderate to severe COPD patients daily legume consumption was 31 ± 21 g while in our study it is 8.9 ± 5.6 g. This difference may be attributed to cultural differences between the countries.
Anthropometric measurements, body composition and physical activity level
In the present study mean weight, height, waist circumference (WC), mid-upper arm circumference (MUAC), fat mass and fat-free mass were significantly lower in patients with low FFMI. Mid-upper arm circumference correlate with total muscle mass and is therefore used to predict changes in the protein nutritional status [
36]. Accordingly, in the present study mean MUAC of patients with low FFMI was significantly low.
Patients with COPD have a significantly reduced duration, intensity, and counts of daily physical activity when compared to healthy control subjects [
37]. Low fat-free mass has been shown to impair exercise performance in COPD patients [
38]. A recent study by Andersson et al. [
39] showed that COPD patients who were more physically active were characterized not only by better pulmonary function but also higher BMI and FFMI. In the current study, mean total daily energy expenditure of patients with low FFMI was significantly low. Additionally, mean physical activity levels was lower in the low FFMI group, but the difference was not statistically significant.
Serum albumin is synthesized in the liver and is a marker of nutritional status. Data suggest that low serum albumin is associated with low appendicular skeletal muscle mass in elderly women and men. Reduced protein metabolism with aging may occur concurrently in the liver and muscle causing similar decrements in both serum albumin and muscle mass [
40]. Although in our study mean serum albumin levels were not markedly different between low and normal FFMI groups, there was a positive weak correlation between FFMI and serum albumin.
Cesari et al. showed in their study that hemoglobin levels were associated with muscle and fat mass changes, and that decreased muscular strength occured in the presence of anemia in individuals who were 65 years and older [
41]. Similarly to these findings, in our study patients with low FFMI had significantly low hemoglobin and hematocrit levels.
Limitations
Some shortcomings of the current study need to be considered. First, no healthy control group could be included in the present analyses in order to compare the nutritional intake between COPD patients and healthy subjects. Nevertheless, results were compared with general findings in general older Turkish adults from the Natonal Turkish Nutrition and Health Survey-2010 [
20]. Second, loss of FFM seems to be more frequent in patients with emphysema-type COPD than in patients with chronic bronchitis. Unfortunately, we were unable to differentiate COPD subtypes in our study. Third, the assessment of dietary intake of fat might be underestimated in food frequency questionnaire. The food frequency method is generally applied in order to assess the quality of dietary intake because it is able to provide data about particular food groups. While there is concern that food frequency questionnaires can be prone to measurement error [
42], they have been shown to identify similar patterns of diet as other dietary methods [
43].
Fourth, in the current study physical activity was assessed by a 24-h recall questionnaire. It has been reported that COPD patients overestimate the time spent walking and underestimate time spent standing. Therefore, using a multisensor armband or an accelerometer to assess physical activity would be more reliable [
37].