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Antioxidant status in a group of institutionalised elderly people with chronic obstructive pulmonary disease

Published online by Cambridge University Press:  22 March 2016

Elena Rodríguez-Rodríguez*
Affiliation:
Sección Departamental de Química Analítica, Facultad de Farmacia, Universidad Complutense de Madrid, 28040 Madrid, Spain UCM Research Group, VALORNUT-920030, Spain
Rosa M. Ortega
Affiliation:
UCM Research Group, VALORNUT-920030, Spain Departamento de Nutrición, Facultad de Farmacia, Universidad Complutense de Madrid, 28040 Madrid, Spain
Pedro Andrés
Affiliation:
Sección Departamental de Química Analítica, Facultad de Farmacia, Universidad Complutense de Madrid, 28040 Madrid, Spain UCM Research Group, VALORNUT-920030, Spain
Aránzazu Aparicio
Affiliation:
UCM Research Group, VALORNUT-920030, Spain Departamento de Nutrición, Facultad de Farmacia, Universidad Complutense de Madrid, 28040 Madrid, Spain
Liliana G. González-Rodríguez
Affiliation:
UCM Research Group, VALORNUT-920030, Spain Departamento de Nutrición Humana y Dietética, Facultad de Ciencias de la Salud, Universidad Alfonso X El Sabio, Villanueva de la Cañada, 28691 Madrid, Spain
Ana M. López-Sobaler
Affiliation:
UCM Research Group, VALORNUT-920030, Spain Departamento de Nutrición, Facultad de Farmacia, Universidad Complutense de Madrid, 28040 Madrid, Spain
Beatriz Navia
Affiliation:
UCM Research Group, VALORNUT-920030, Spain Departamento de Nutrición, Facultad de Farmacia, Universidad Complutense de Madrid, 28040 Madrid, Spain
José M. Perea
Affiliation:
UCM Research Group, VALORNUT-920030, Spain Departamento de Nutrición Humana y Dietética, Facultad de Ciencias de la Salud, Universidad Alfonso X El Sabio, Villanueva de la Cañada, 28691 Madrid, Spain
Paula Rodríguez-Rodríguez
Affiliation:
Servicio de Neumología, Hospital Fundación Jiménez Díaz, 28040 Madrid, Spain
*
*Corresponding author: E. Rodríguez-Rodríguez, fax +34 91 394 17 54, email elerodri@ucm.es; grupo920030@gmail.com
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Abstract

Chronic obstructive pulmonary disease (COPD) is one of the most important and prevalent diseases suffered by the elderly. Evidence exists that its onset and severity might be conditioned by antioxidant status. The aim of the present study was to investigate the relationship between antioxidant status and COPD in institutionalised elderly people. In all, 183 elderly people aged >65 years (twenty-one had COPD and 160 healthy controls) were studied. The subjects’ diets were investigated via the use of precise individual weighing for 7 d. Body weight, height, and biceps and triceps skinfold thickness were measured, and body fat (kg) and BMI (kg/m2) were calculated. Serum retinol, α-tocopherol, β-carotene and vitamin C levels were determined. Subjects with COPD ate less fruits than healthy controls (117 (sd 52) v. 192 (sd 161) g/d), their coverage of the recommended intake of vitamin C was smaller (150 (sd 45) v. 191 (sd 88) %; note that both exceeded 100 %) and their diets had a lower antioxidant capacity (6558 (sd 2381) v. 9328 (sd 5367) mmol trolox equivalent/d). Those with COPD had lower serum vitamin C and α-tocopherol concentrations than healthy controls (32·4 (sd 15·3) v. 41·5 (sd 14·8) µmol/l and 12·1 (sd 3·2) v. 13·9 (sd 2·8) µmol/l, respectively). In addition, subjects with α-tocopherol <14·1µmol/l (50th percentile) were at 6·43 times greater risk of having COPD than those subjects with ≥14·1µmol/l (OR 6·43; 95 % CI 1·17, 35·24; P<0·05), taking sex, age, use of tobacco, body fat and vitamin E intake as covariables. Subjects with COPD had diets of poorer antioxidant quality, especially with respect to vitamins C and E, compared with healthy controls.

Type
Full Papers
Copyright
© The Authors 2016 

Chronic obstructive pulmonary disease (COPD) is a chronic, inflammatory ailment of the lungs, in which there is a progressive and irreversible loss of airflow( Reference Martínez 1 , Reference Miravitllesa, Soler-Cataluñab and Callec 2 ). At present, there are 210 million people with COPD, and it has been estimated to be the third leading cause of death worldwide by 2030( 3 ). Many authors suggest COPD to be very prevalent among the elderly( Reference Martínez 1 , Reference Kobayashi, Yanai and Hanagama 4 ). In Spain, there are some 21·4 million people between 40 and 80 years of age, among whom 2 185 764 are affected by the disease( Reference Miravitlles, Soriano and Garcia-Rio 5 ). Although these figures come from one of the largest studies undertaken in this field, its age limit of 80 years should not go unnoticed.

Among the factors that might contribute towards the development of COPD are genetic background (especially those types leading to a deficiency in α-1-antitrypsin), exposure to oxidising agents (e.g. those in atmospheric pollution and tobacco smoke) and reduced antioxidant capacity( Reference MacNee 6 Reference Siedlinski, Postma and van Diemen 8 ). Certainly, people with COPD experience increased oxidative stress, which reduces airflow. This could lead to a greater demand for antioxidant nutrients such as vitamins C and E and carotenoids, which might leave COPD patients more vulnerable to deficiencies( Reference McKeever, Lewis and Smit 9 Reference McKeever, Scrivener and Broadfield 11 ). For example, in a group of 218 patients diagnosed with asthma and/or COPD, serum β-cryptoxanthin, lutein/zeaxanthin and retinol concentrations were found to be significantly and positively associated with the forced expiratory volume in 1 s (FEV1) – the most important measure of airflow. The antioxidant status of patients with COPD may therefore be important in terms of the progression of the disease( Reference Ochs-Balcom, Grant and Muti 10 ).

Although COPD is one of the most common diseases affecting the elderly, a few studies on antioxidant status in this population have been performed( Reference Ochs-Balcom, Grant and Muti 10 , Reference Lin, Wu and Chen 12 ). The aim of the present study was, therefore, to determine the antioxidant status of a group of institutionalised elderly people.

Methods

Study subjects

This case–control study included elderly people over 65 years of age, residing in four homes for the elderly in the Region of Madrid, Spain. The health personnel at the different homes selected the subjects after checking their medical records, their cognitive functional and affective capacity scores, and prescribed medication. This study was part of a larger study( Reference Bermejo, Aparicio and Rodríguez-Rodríguez 13 ), aimed at selecting groups of subjects with similar nutritional, cognitive and affective characteristics in order to include them in a nutritional intervention trial. The starting number for each group was about fifty subjects. Centres with less than sixty possible participants were excluded.

All subjects were informed of the characteristics of the study, and their signed consent to be included was requested. Those who did not provide signed consent were excluded, as well as those with any condition that might affect the digestion, absorption or utilisation of nutrients (neoplasms, cirrhosis, abnormal liver function, poor intestinal absorption, etc.) and those showing signs of manifest cognitive decline (i.e. with a Lobo & Ezquerra test score of <24( Reference Lobo and Ezquerra 14 )). Individuals for whom alcohol made up >10 % of their daily energy intake were also excluded. A total of 183 elderly people (sixty-three men and 120 women) completed the study.

The present study followed the principles of the Declaration of Helsinki and was approved by the Human Research Review Committee of the Pharmacy Faculty, Complutense University of Madrid. Signed informed consent was obtained from all participants.

Dietary study

The subjects’ consumption of food and intake of nutrients were determined by the ‘precise individual weighing’ method over a period of 7 consecutive days (including a weekend to take into account any change in the normal daily diet)( Reference Maisey, Loughridge and Southon 15 ). The individual portions consumed at each of the main meals (breakfast, lunch, early evening snack, evening meal) were weighed, as were the amounts left on the plate after eating. The subjects could choose their meals as the homes offered a range of menus. Thus, the foods recorded over this 7-d period likely reflect the normal food choices made by the subjects. All foods consumed outside established mealtimes, as well as outside of the homes, were reported by the subjects themselves.

The dietary data collected were treated using DIAL software( Reference Ortega, López-Sobaler and Andrés 16 ) in order to determine the amounts of the different food groups consumed, the nutrient and energy intakes, the total antioxidant capacity (TAC) of the diet and the adequacy of the intake of different dietary components, especially vitamins A, C and E, with respect to recommended intakes (RI).

TAC can be determined in different ways including the ferric-reducing antioxidant power (FRAP) method, which determines the capacity to reduce a ferric complex( Reference Benzie and Strain 17 ), the radical trapping antioxidant parameter (TRAP) method, based on the thermal decomposition of azo-hydrosoluble compounds that produce peroxyl radicals( Reference Ghiselli, Serafini and Maiani 18 ), the trolox equivalent antioxidant capacity (TEAC) method, which measures the capacity to reduce the ABTS+(2,2’-azinobis(3-ethylbenzothiazoline-6-suslfonic acid) radical under lipophilic and hydrophilic conditions( Reference Rice-Evans and Miller 19 ), and the oxygen radical absorbance capacity (ORAC) method, which measures the oxidative degradation of a fluorescent molecule subjected to a flow of peroxyl radicals( Reference Prior, Hoang and Gu 20 ). In the present study, the TAC of the diets was determined using values recorded in the Spanish Food Composition Tables ( Reference Ortega, López-Sobaler and Requejo 21 ), drawn up by collecting values published by different authors. The database used contained 483 measurements made by the FRAP method (mmol/100 g), 140 by the TRAP method (trolox equivalent (TE) mmol/100 g), 158 by the TEAC method (TE mmol/100 g) and 225 by the ORAC method (TE mmol/100 g).

Presence of chronic obstructive pulmonary disease

The medical histories of the subjects were examined in search of information on/diagnoses of COPD. When this information was insufficient to identify a subject as having this problem, the doctor who attended to the subjects at each home was asked for assistance. COPD was deemed present when, following the inhalation of bronchodilators, the FEV1/forced vital capacity multiplied by 100 was <70 %( Reference Pauwels, Buist and Calverley 22 , Reference Rabe, Hurd and Anzueto 23 ).

Of the 183 subjects who took part in the present study, twenty-one were deemed to have COPD.

Other covariables

Information was also collected on risk factors for COPD, such as age (years), smoking habits (non-smoker, ex-smoker, smoker), alcohol consumption and use of multivitamin supplements.

Anthropometric study

Body weight was determined using a Seca Alpha digital balance (range 0·1–150 kg; accuracy 100 g; Seca Alpha, GmbH & Co.), with the subjects wearing only underwear and standing on the centre of the horizontal plate. Body weight of subjects who found it difficult to stand was determined using an Alpha 6868 medical balance equipped with a seat (range 1–360 kg).

Height was determined using a Harpenden digital stadiometer (range 70–205 cm; accuracy 1 mm; Pfifter). Subjects were measured while standing, holding the back as straight as possible and with the arms parallel to the body, heals together and the head in the Frankfort horizontal plane. This measurement was taken only for those subjects who could maintain a standing position. For subjects with problems of balance or conditions affecting the vertebral column (kyphosis, sclerosis), height was estimated from the knee–heel distance using the formula of Chumlea( Reference Chumlea 24 ):

$$\eqalignno{ &#x0026; {\rm Men\,\colon\,}\,{\rm 64}\!\cdot\!{\rm 2}\,{\minus}\,\left( {{\rm 0}\! \cdot \!{\rm 04}\,{\rm age}\,{\rm (years)}} \right)\cr {\plus}\left( {{\rm 2} \!\cdot \!{\rm 02}\,{\rm distance}\,{\rm knee}\,{\minus}\,{\rm heel}\,{\rm (cm)}} \right), \cr &#x0026; {\rm Women\,\colon\,}\,{\rm 89} \!\cdot \!{\rm 4}\,{\minus}\,\left( {{\rm 0}\! \cdot \!{\rm 24}\,{\rm age}\,{\rm (years)}} \right)\cr {\plus}\left( {{\rm 1\!} \cdot \!{\rm 83}\,{\rm distance}\,{\rm knee}\,{\minus}\,{\rm heel}\,{\rm (cm)}} \right). $$

BMI was then calculated from the height and body weight measurements( Reference Durnin and Fidanza 25 ):

$${\rm BMI}\,({\rm kg\,/\,m}^{{\rm 2}} )\,{\equals}\,{{{\rm weight}\,({\rm kg})} \over {{\rm height}^{{\rm 2}} \,({\rm m}^{{\rm 2}} )}}.$$

Skinfolds (biceps and triceps) were measured using a Holtain skinfold caliper (range 0–40 mm; accuracy 0·1 mm Holtain Ltd), applying a constant pressure of 10 g/mm2 over the contact surface. Measurements were taken on the non-dominant side of the body. All readings were taken after some 4 s with the caliper in place to reduce the variation associated with skin compressibility( Reference Becque, Katch and Moffatt 26 ). The biceps skinfold thickness was measured over the cubital fossa with the arm relaxed, at the mid-point between the acromion and the olecranon. The triceps skinfold thickness was measured with the arm relaxed, also at the mid-point between the acromion and the olecranon.

The percentage of body fat (BF%) was calculated using the equation of Siri( Reference Siri 27 ):

$${\rm BF\,\&#x0025;\,}{\equals}\left( {{{{\rm 495}} \over D}} \right)\,{\minus}\,{\rm 450,}$$

where D is the density term calculated using the equation of Durnin & Womersley( Reference Durnin and Womersley 28 ):

$$\eqalignno{ D \,{\equals}\,c\cr {\minus}\left( {m{\times}{\rm log}\,\left( {{\rm sum}\,{\rm of}\,{\rm the}\,{\rm biceps}\,{\rm and}\,{\rm triceps}\,{\rm skinfold}\,{\rm thicknesses}} \right)} \right),$$

in which c=1·1185 for men and 1·1226 for women, and m=0·0683 for men and 0·0710 for women.

Once BF% was known, BF mass (kg) was determined using the equation of Méndez & Lukaski( Reference Méndez and Lukaski 29 ):

$${\rm BF}\,{\rm (kg)}{\equals}{{\left( {{\rm BF\,\&#x0025;\,}{\times}{\rm weight}\,({\rm kg})} \right)} \over {100}}.$$

Blood sample collection

Blood samples were collected by venepuncture between 08.00 and 09.00 hours in the morning after 12 h of fasting. Adherence to the fasting period was checked by nurses before blood was collected. All sample collections were performed at the respective centres.

Biochemical study

Retinol and α-tocopherol levels were determined together by reversed-phase HPLC following the method of Driskel et al.( Reference Driskel, Neese and Bryant 30 ). The mobile phase was a 95:5 mixture of methanol–water, the flow rate was 1·0 ml/min and the column was a Supelcosil LC-18 model (4·2×150 mm; 5 μm particle size; Sigma-Aldrich Co. LLC). All determinations were made using a Varian 5000 apparatus equipped with a Varian variable wavelength UV detector (Varian BV). Vitamin A detection was performed at 325 nm and vitamin E detection at 294 mm 3 min later. Retinyl acetate and tocopheryl acetate were used as internal standards (CV=2·4 % for retinol and 2·8 % for tocopherol).

β-Carotene was also determined by reversed-phase HPLC. The target molecule was extracted from 100 μl serum samples via the addition of 120 μl n-hexane plus 100 μl of echinenone as an internal standard. The mixture was then centrifuged (500 g , 5 min) and 100 μl of the supernatant was extracted. This was then evaporated in a N atmosphere at 50°C. The lipid residue was then reconstituted in 100 μl of a mobile phase (70 % acetonitrile, 20 % dichloromethane, 10 % methanol). Separation was performed using a Supelcosil LC-18 column (4·6×250 nm; 5 μm particle size) at a flow rate of 1·7 ml/min. Detection was performed using a UV detector at 436 nm (CV=3·3 %)( Reference Bieri, Brown and Smith 31 ).

Vitamin C was determined via ascorbic acid enzymatic oxidation( Reference Beutler and Beinstingl 32 ) and the formation of quinoxaline to produce a fluorescent compound that was detectable spectrofluorimetrically( Reference Speek, Schrijver and Schreus 33 ). The method followed was that of Vuilleumier & Keck( Reference Vuilleumier and Keck 34 ) without automation (CV=2·9 %).

Statistical analysis

Values were recorded as means and standard deviations or percentages. The dietary data were adjusted by energy intake using the residuals method. Differences between means were examined using the Student’s t test or using the Mann–Whitney test when the distribution of the results was not normal. Linear correlation coefficients were determined between some variables. Categorical variables were compared using the χ 2 test. Logistic regression analysis was used to examine the risk factors associated with COPD; these results are presented as OR and 95 % CI. Significance was set at P<0·05. All calculations were performed using RSIGMA BABEL software (Horus Hardware).

Results

In all, twenty-one (11·5 %) subjects had COPD. A high percentage of the population had an inadequate vitamin E and β-carotene status (Table 1). The TAC of the diet, as measured by the ORAC method, was positively and significantly associated with the consumption of fruits (r 0·7357; P<0·001).

Table 1 Characteristics of the study population (Mean values and standard deviations)

COPD, chronic obstructive pulmonary disease; BF, body fat; RI, recommended intake; ORAC, oxygen radical absorbance capacity; TE, trolox equivalent; FRAP, ferric-reducing antioxidant power; TRAP, trapping antioxidant parameter; TEAC, trolox equivalent antioxidant capacity.

Subjects with COPD were more commonly men and smokers, and their diets had a lower TAC compared with control subjects (Table 2). No significant differences were detected in terms of intake of the studied nutrients. However, the RI of vitamin C was better covered among the control subjects (Table 2). In addition, subjects with a vitamin intake <150 % of RI were three times more likely of having COPD than those with higher intakes (OR 2·94; 95 % CI 1·11, 7·75; P<0·05). The main source of vitamin C was fruits (r 0·8091; P<0·001), and consumption of fruits was higher among the control subjects (Table 2). There were no differences between the control and the COPD groups regarding vitamin A intake. However, those with a vitamin A intake <75 % of the RI were 2·69 times more likely of having COPD than those with higher intakes (OR 2·79; 95 % CI 1·01, 7·23; P<0·05).

Table 2 Characteristics of the study population depending on chronic obstructive pulmonary disease (COPD) statusFootnote (Mean values and standard deviations)

BF, body fat; RI, recommended intake; ORAC, oxygen radical absorbance capacity; TE, trolox equivalent; FRAP, ferric-reducing antioxidant power; TRAP, trapping antioxidant parameter; TEAC, trolox equivalent antioxidant capacity.

Significant correlations: * P<0·05; ** P<0·01.

Student’s t test (or the Mann–Whitney test if the distribution of results was not homogeneous) was used to compare variables between groups. The χ 2 test was used to determine the significance of differences between proportions.

Subjects with COPD had lower serum vitamin C and α-tocopherol levels than the control subjects, although no significant differences were seen between the two groups regarding the percentage of people with deficient levels (Table 2).

Logistic regression analysis showed that subjects with a serum vitamin C concentration <42μmol/l (i.e. below 50th percentile) were 3·59 times more likely of having COPD than those with concentrations ≥42μmol/l (OR 3·59; 95 % CI 1·13, 11·41; P<0·05). Similarly, subjects with serum α-tocopherol <14·1 µmol/l (i.e. below 50th percentile) were 4·17 times more likely of having COPD than those with higher levels (OR 4·17; 95 % CI 1·11, 15·69; P<0·05). When taking the covariables sex, age, use of tobacco, BF and vitamin C or E (as required) into account, this relationship was lost for vitamin C (OR 4·31; 95 % CI 0·97, 19·30; P>0·05) but was significant for α-tocopherol (OR 6·43; 95 % CI 1·17, 35·24; P<0·05).

Discussion

Oxidative stress appears to play an important role in the pathogenesis of COPD. An adequate intake of antioxidant nutrients, and an adequate status of these nutrients, might therefore be beneficial in the maintenance of pulmonary function in patients with this condition( Reference Deslee, Woods and Moore 35 ). A study involving 14 120 adults over 17 years of age showed that higher serum concentrations of vitamins A, C, E and β-cryptoxanthine were independently associated with higher FEV1 scores( Reference McKeever, Lewis and Smit 9 ) – a finding in line with the results of the present study.

Although the contribution of vitamin C intake towards covering its RI was indeed high, over 100 %, it was even higher among the control subjects. These results suggest that a coverage >150 % may offer protection against the appearance of COPD. This agrees with that reported by other authors. For example, Ahmadi et al.( Reference Ahmadi, Haghighat and Hakimrabet 36 ) and Lin et al.( Reference Lin, Wu and Chen 12 ) reported smaller intakes of vitamin C among patients with COPD compared with healthy controls, and the latter authors also reported greater consumption of fruits and vegetables among control subjects. In addition, in a study of 2917 Finnish men who were followed-up for 20 years, it was noticed that for every 100 g increase in fruit consumption, the risk of developing COPD fell by 24 %( Reference Walda, Tabak and Smit 37 ). This finding also agrees with the present results: greater fruit consumption – the main source of vitamin C – was seen among the healthy subjects.

As seen at the dietary level, and in agreement with other authors( Reference McKeever, Lewis and Smit 9 , Reference Lin, Wu and Chen 12 ), higher serum vitamin C concentrations seemed to offer protection against COPD. When use of tobacco was taken into account as a covariable, this effect was lost. Certainly, it has been reported that, in vitro, the plasma concentration of this vitamin falls significantly in the presence of tobacco smoke as a consequence of lipid peroxidation( Reference Cross, O’Neill and Reznick 38 ). As the majority of our subjects with COPD were smokers (Table 2), and given that smoking is an important risk factor for low serum vitamin C concentrations, it would seem reasonable to recommend that the intake of this vitamin/the consumption of fruits be increased and that smoking be ceased.

In addition to having antioxidant activity, vitamin E exerts anti-inflammatory effects; maintaining an adequate vitamin E status might therefore be beneficial to patients with COPD( Reference Reiter, Jiang and Christen 39 ). In a recent study involving 38 507 women followed-up over 10 years, it was determined that the administration of 400mg vitamin E reduced the risk of developing COPD by 10 %( Reference Agler, Kurth and Gaziano 40 ). In the present study, subjects with COPD not only had less vitamin E intakes compared with healthy controls but also had poorer serum concentrations of the same. Further, serum values below the 50th percentile were associated with four times higher risk of having COPD than higher levels. This relationship held even when smoking was taken into account as a covariable. These results are consistent with those reported by Ahmadi et al.( Reference Ahmadi, Haghighat and Hakimrabet 36 ), who reported vitamin E intake to be lower in patients with COPD than in healthy controls. Similarly, Lin et al.( Reference Lin, Wu and Chen 12 ) reported serum vitamin E concentrations to be lower in patients with COPD, and Tug et al.( Reference Tug, Karatas and Terzi 41 ) observed lower serum concentrations in twenty-four patients with COPD during times of disease exacerbation than during times of stability.

All the subjects had low serum α-tocopherol concentrations (below 23·2 μmol/l( Reference Gámez, Artacho and Ruiz-López 42 )), yet all had intakes of >100 % of that recommended. Different factors can be related to this fact. First, absorption of vitamin E could be decreased by the use of cholesterol medication. Therefore, the elderly with high cholesterol and cholesterol medication might suffer from inadequate vitamin E intake( Reference Herrmann and Obeid 43 ). Second, a relationship between increased oxidative stress and the most important age-related pathologies (i.e. CVD and neurodegenerative disease, cancer and diabetes) has been largely demonstrated( Reference Dato, Crocco and D’Aquila 44 ), and antioxidant status has been demonstrated to be compromised in people with chronic diseases( Reference Wang, Chun and Song 45 ). According to these, although we did not find any relationship between the use of anticholesterolaemic drugs and serum α-tocopherol concentrations, we found that elderly people with α-tocopherol serum values below the 50th percentile showed higher percentage of anaemia and ischaemia/heart failure than people with values above the 50th percentile (5·8 v. 0 %; P<0·05 and 49·3 v. 29·0 %; P<0·05, respectively). Thus, the condition of these diseases may compromise the status of vitamin E in elderly people and, although in our study all subjects had intakes above the RI, the current intake could be insufficient to maintain an adequate status of this vitamin. For this reason, the vitamin E RI in elderly people could be insufficient and should be revised. At the moment, it may be a good idea for these subjects to further increase their intake. It should also be remembered that low serum α-tocopherol can result in a low retinyl palmitate concentration( Reference Schäffer, Roy and Mukherjee 46 ), making the antioxidant status even worse.

Good coverage of vitamin A intake appeared to offer protection against COPD in our subjects. Similar observations have been reported by other authors. For example, Lin et al.( Reference Lin, Wu and Chen 12 ) reported lower serum retinol and β-carotene in patients with COPD compared with healthy controls, and Tug et al.( Reference Tug, Karatas and Terzi 41 ) indicated serum vitamin A concentrations to be lower during periods of exacerbation of the disease. In the present study, however, no relationship was seen between COPD and serum β-carotene – a circumstance also reported by Walda et al.( Reference Walda, Tabak and Smit 37 ) in their large Finnish study.

The TAC (as measured by the ORAC method – the method of choice according to Awika et al.( Reference Awika, Rooney and Wu 47 )) of the diets of the present subjects with COPD was not as great as that of the healthy subjects. Although the literature contains no other reports relating dietary TAC to COPD, some authors report the antioxidant capacity of patients with COPD to be lower. For example, the plasma antioxidant capacity of the eighty patients with COPD, as determined by the FRAP method, was lower than that of the twenty healthy controls (0·936 v. 1·110 mmol Fe2+/l)( Reference Emin, Yordanova and Dimov 48 ). It was also found to be lower, as determined by the TEAC method, in ninety-five patients with COPD compared with thirty-seven healthy controls (0·81 v. 1·31 mmol/l)( Reference Rahman, Swarska and Henry 49 ). As the antioxidant capacities of the plasma and diet are related( Reference Wang, Yang and Lee 50 ), the results of the present study, and of others studies, suggest that patients with COPD should follow diets rich in components with antioxidant power, especially fruits (note above the significant relationship between fruit intake and the present ORAC results).

Finally, fruit consumption of healthy controls was higher than that of subjects with COPD, which could also be related to a higher intake of phytochemicals such as catechin and flavonoids from this food group. Moreover, in a study carried out in 13 651 adults from three Dutch cities, consumption of solid fruits was inversely associated with the prevalence of one or more COPD symptoms (cough, phlegm and breathlessness). Indeed, catechin intake was independently associated with all three COPD symptoms. Nevertheless, flavonol and flavone intakes were independently associated with chronic cough only( Reference Tabak, Arts and Smit 51 ).

Intake of phytochemicals was not assessed in the present study because of the lack of available data in the Spanish food composition database used. As the present study is a case–control study, it suffers the limitation in that it cannot identify causal relationships. Moreover, the statistical power of the study was low to detect associations for different exposure factors including the deficiency of vitamin C (37·4 %), deficiency of β-carotene (14·7 %), deficiency of vitamin A (13 %) and deficiency of vitamin E (28·1 %) owing to the small sample size. Therefore, these results should be interpreted with caution.

In conclusion, the present subjects with COPD had a poorer antioxidant status (especially in terms of vitamins C and E) than the healthy controls, especially those who smoked. It would therefore seem recommendable that the intake of these nutrients, especially via fruit consumption, be increased in such patients.

Acknowledgements

This work was financed by Unilever Netherlands via the Universidad-Empresa project 138/2000 and the ‘Creation and Consolidation Program for Research Groups’ at the ‘Complutense University of Madrid’ (ref no. GR3/14).

R. M. O., A. M. L.-S., E. R.-R. and A. A. contributed to the study design, and E. R.-R., A. A., B. N., J. M. P., L. G. G.-R. and P. R.-R. performed the data collection. R. M. O., A. M. L.-S., E. R.-R., A. A. and P. A. were involved in data analysis and the interpretation of the results. R. M. O., A. A., P. A. and P. R.-R. contributed to the writing of the manuscript.

None of the authors has any conflicts of interest to declare.

References

1. Martínez, N (2013) Guía GesEPOC y pacientes ancianos (Spanish COPD guide and elderly patients). Arch Bronconeumol 49, 367368.Google Scholar
2. Miravitllesa, M, Soler-Cataluñab, JJ, Callec, M, et al. (2014) Guía española de la EPOC (GesEPOC). Actualización 2014 (Spanish COPD guide (GesEPOC). Update 2014). Arch Bronconeumol 50, Suppl. 1, 116.Google Scholar
3. World Health Organization (2016) Burden of COPD. http://www.who.int/respiratory/copd/en/ (accessed January 2016).Google Scholar
4. Kobayashi, S, Yanai, M, Hanagama, M, et al. (2014) The burden of chronic obstructive pulmonary disease in the elderly population. Respir Investig 52, 296301.Google Scholar
5. Miravitlles, M, Soriano, JB, Garcia-Rio, F, et al. (2009) Prevalence of COPD in Spain: impact of undiagnosed COPD on quality of life and daily life activities. Thorax 64, 863868.Google Scholar
6. MacNee, W (2005) Pulmonary and systemic oxidant/antioxidant imbalance in chronic obstructive pulmonary disease. Proc Am Thorac Soc 2, 5060.CrossRefGoogle ScholarPubMed
7. Guenegou, A, Boczkowski, J, Aubier, M, et al. (2008) Interaction between a heme oxygenase-1 gene promoter polymorphism and serum beta-carotene levels on 8-year lung function decline in a general population: the European Community Respiratory Health Survey (France). Am J Epidemiol 167, 139144.Google Scholar
8. Siedlinski, M, Postma, DS, van Diemen, CC, et al. (2008) Lung function loss, smoking, vitamin C intake, and polymorphisms of the glutamate-cysteine ligase genes. Am J Respir Crit Care Med 178, 1319.Google Scholar
9. McKeever, TM, Lewis, SA, Smit, HA, et al. (2008) A multivariate analysis of serum nutrient levels and lung function. Respir Res 9, 67.Google Scholar
10. Ochs-Balcom, HM, Grant, BJ, Muti, P, et al. (2006) Antioxidants, oxidative stress, and pulmonary function in individuals diagnosed with asthma or COPD. Eur J Clin Nutr 60, 991999.CrossRefGoogle ScholarPubMed
11. McKeever, TM, Scrivener, S, Broadfield, E, et al. (2002) Prospective study of diet and decline in lung function in a general population. Am J Respir Crit Care Med 165, 12991303.Google Scholar
12. Lin, YC, Wu, TC, Chen, PY, et al. (2010) Comparison of plasma and intake levels of antioxidant nutrients in patients with chronic obstructive pulmonary disease and healthy people in Taiwan: a case-control study. Asia Pac J Clin Nutr 19, 393401.Google Scholar
13. Bermejo, LM, Aparicio, A, Rodríguez-Rodríguez, E, et al. (2009) Dietary strategies for improving folate status in institutionalized elderly persons. Br J Nutr 101, 16111615.Google Scholar
14. Lobo, A & Ezquerra, J (1979) El Mini-Mental cognoscitivo: un test sencillo y práctico para detectar alteraciones intelectivas en pacientes médicos (The Cognitive Mini-Mental: a simple and practical test to detect cognitive impairment in medical patients). Actas Luso Esp Neurol Psyquiatr 3, 149153.Google Scholar
15. Maisey, S, Loughridge, J, Southon, S, et al. (1995) Variation in food group and nutrient intake with day of the week in an elderly population. Br J Nutr 73, 359373.Google Scholar
16. Ortega, RM, López-Sobaler, AM, Andrés, P, et al. (2013) DIAL software for assessing diets and food calculations (for Windows, version 3.0.0.5), Department of Nutrition (UCM) & Alceingeniería, S.A. Madrid. http://www.alceingenieria.net/nutricion.htm (accessed October 2014).Google Scholar
17. Benzie, IF & Strain, JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of ‘antioxidant power’: the FRAP assay. Anal Biochem 239, 7076.CrossRefGoogle ScholarPubMed
18. Ghiselli, A, Serafini, M, Maiani, G, et al. (1995) A fluorescence based method for measuring total plasma antioxidant capability. Free Radic Biol Med 18, 2936.Google Scholar
19. Rice-Evans, C & Miller, NJ (1994) Total antioxidant status in plasma and body fluids. Methods Enzymol 234, 279293.Google Scholar
20. Prior, RL, Hoang, H, Gu, L, et al. (2003) Assays for hydrophilic and lipophilic antioxidant capacity (oxygen radical absorbance capacity (ORAC(FL))) of plasma and other biological and food samples. J Agric Food Chem 51, 32733279.CrossRefGoogle ScholarPubMed
21. Ortega, RM, López-Sobaler, AM, Requejo, AM, et al. (2010) La Composición De Los Alimentos. Herramienta Básica Para La Valoración Nutricional (Food Composition. A Basic Tool for Assessing Nutritional Status). Madrid: Editorial Complutense.Google Scholar
22. Pauwels, RA, Buist, AS, Calverley, PM, et al. (2001) Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease. NHLBI/WHO Global Initiative for Chronic Obstructive Lung Disease (GOLD) Workshop summary. Am J Respir Crit Care Med 163, 12561276.CrossRefGoogle Scholar
23. Rabe, KF, Hurd, S, Anzueto, A, et al. (2007) Global initiative for chronic obstructive pulmonary disease. Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: GOLD executive summary. Am J Respir Crit Care Med 176, 532555.CrossRefGoogle Scholar
24. Chumlea, CW (1985) Estimating stature from knee height for persons 60 to 90 years of age. J Am Geriatr Soc 33, 116120.Google Scholar
25. Durnin, JVGA & Fidanza, F (1985) Evaluation of nutritional status. Bibl Nutr Dieta 35, 2030.Google Scholar
26. Becque, MD, Katch, VL & Moffatt, RJ (1986) Time course of skin-plus-fat compression in males and females. Hum Biol 58, 3342.Google Scholar
27. Siri, WE (1956) The gross composition of the body. Adv Biol Med Phys 4, 239280.CrossRefGoogle ScholarPubMed
28. Durnin, JVGA & Womersley, J (1974) Body fat assessed from total body density and its estimation from skinfold thickness: measurements on 481 men and women aged from 16 to 72 years. Br J Nutr 32, 7797.CrossRefGoogle ScholarPubMed
29. Méndez, J & Lukaski, HC (1981) Variability of body density in ambulatory subjects measured at different days. Am J Clin Nutr 34, 7881.CrossRefGoogle ScholarPubMed
30. Driskel, WJ, Neese, JW, Bryant, CC, et al. (1982) Measurement of vitamin A and vitamin E in human serum by high performance liquid chromatography. J Chromatogr 231, 439444.CrossRefGoogle Scholar
31. Bieri, JG, Brown, ED & Smith, JC (1988) Determination of individual carotenoids in human plasma by high performance liquid chromatography. J Liq Chromatogr 8, 473484.Google Scholar
32. Beutler, HO & Beinstingl, G (1980) Bestimmung von L-Ascorbinsäure in Lebensmitteln (Determination of L-ascorbic acid in food). Dtsch Lebensmitt Rundsch 76, 6975.Google Scholar
33. Speek, AJ, Schrijver, J & Schreus, WH (1984) Fluorometric determination of total vitamin C in whole blood by high-performance liquid chromatography with pre-column derivatization. J Chromatogr 305, 5360.Google Scholar
34. Vuilleumier, JP & Keck, E (1989) Fluorometric assay of vitamin C in biological materials using a centrifugal analyser with fluorescence attachment. J Micronutr Anal 5, 2534.Google Scholar
35. Deslee, G 1, Woods, JC, Moore, C, et al. (2009) Oxidative damage to nucleic acids in severe emphysema. Chest 135, 965974.Google Scholar
36. Ahmadi, A, Haghighat, N, Hakimrabet, M, et al. (2012) Nutritional evaluation in chronic obstructive pulmonary disease patients. Pak J Biol Sci 15, 501505.CrossRefGoogle ScholarPubMed
37. Walda, IC, Tabak, C, Smit, HA, et al. (2002) Diet and 20-year chronic obstructive pulmonary disease mortality in middle-aged men from three European countries. Eur J Clin Nutr 56, 638643.Google Scholar
38. Cross, CE, O’Neill, CA, Reznick, AZ, et al. (1993) Cigarette smoke oxidation of human plasma constituents. Ann N Y Acad Sci 686, 7289.Google Scholar
39. Reiter, E, Jiang, Q & Christen, S (2007) Anti-inflammatory properties of alpha- and gamma-tocopherol. Mol Aspects Med 28, 668691.Google Scholar
40. Agler, AH, Kurth, T, Gaziano, JM, et al. (2011) Randomised vitamin E supplementation and risk of chronic lung disease in the Women’s Health Study. Thorax 66, 320325.Google Scholar
41. Tug, T, Karatas, F & Terzi, SM (2004) Antioxidant vitamins (A, C and E) and malondialdehyde levels in acute exacerbation and stable periods of patients with chronic obstructive pulmonary disease. Clin Invest Med 27, 123128.Google Scholar
42. Gámez, C, Artacho, R, Ruiz-López, MD, et al. (1996) Nutritional status of vitamin A and E in institutionalized elderly people in Granada (Spain). J Nutr Sci Vitaminol (Tokyo) 42, 397405.CrossRefGoogle Scholar
43. Herrmann, W. & Obeid, R (2011) Vitamins in the Prevention of Human Diseases. Berlin/New York: Walter de Gruyter GmbH & Co.Google Scholar
44. Dato, S, Crocco, P, D’Aquila, P, et al. (2013) Exploring the role of genetic variability and lifestyle in oxidative stress response for healthy aging and longevity. Int J Mol Sci 14, 1644316472.CrossRefGoogle ScholarPubMed
45. Wang, Y, Chun, OK & Song, WO (2013) Plasma and dietary antioxidant status as cardiovascular disease risk factors: a review of human studies. Nutrients 5, 29693004.Google Scholar
46. Schäffer, MW, Roy, SS, Mukherjee, S, et al. (2013) Vitamin A, vitamin E, lutein and β-carotene in lung tissues from subjects with chronic obstructive pulmonary disease and emphysema. Open J Res Dis 3, 4451.Google Scholar
47. Awika, JM, Rooney, LW, Wu, X, et al. (2003) Screening methods to measure antioxidant activity of sorghum (Sorghum bicolor) and sorghum products. J Agric Food Chem 51, 66576662.Google Scholar
48. Emin, S, Yordanova, K, Dimov, D, et al. (2010) Total antioxidant capacity of plasma determined as ferrous reducing ability of plasma in patients with COPD. Trakia J Sci 8, 205213.Google Scholar
49. Rahman, I, Swarska, E, Henry, M, et al. (2000) Is there any relationship between plasma antioxidant capacity and lung function in smokers and in patients with chronic obstructive pulmonary disease? Thorax 55, 189193.Google Scholar
50. Wang, Y, Yang, M, Lee, SG, et al. (2012) Dietary total antioxidant capacity is associated with diet and plasma antioxidant status in healthy young adults. J Acad Nutr Diet 112, 16261635.Google Scholar
51. Tabak, C, Arts, IC, Smit, HA, et al. (2001) Chronic obstructive pulmonary disease and intake of catechins, flavonols, and flavones: the MORGEN Study. Am J Respir Crit Care Med 164, 6164.Google Scholar
Figure 0

Table 1 Characteristics of the study population (Mean values and standard deviations)

Figure 1

Table 2 Characteristics of the study population depending on chronic obstructive pulmonary disease (COPD) status† (Mean values and standard deviations)