Dietary patterns have been widely investigated in relation to cancer, CVD or diabetes [12], but limited data are available on their association with respiratory outcomes with relevance to COPD. As shown in a recent meta-analysis [14], most studies were performed in Europe and North America, limiting the generalizability of study findings, and were observational in design. Overall, the evidence concordantly indicated that the pattern of dietary intake is an important factor in the pathogenesis and prevention of COPD and provided support for specific dietary modifications as a clinically relevant tool to promote lung health. Moreover, examination of dietary patterns complements the evaluation of the effects of individual food and nutrient intake on COPD. Table 1 summarizes findings from main epidemiological studies addressing the relation between diet and lung function, COPD risk, symptoms, and progression.
Table 1. Main findings from epidemiological studies linking dietary patterns to adult lung function and chronic obstructive pulmonary disease (COPD) (incidence, prevalence, and severity).
Dietary Patterns Country
Design (Follow-Up)
Diet Population Sex (Age) Assessment
Method
Outcome Assessment
Main Results Ref
Meat–dim sum pattern and vegetable–fruit–soy pattern
Prudent pattern and Western pattern
Prudent pattern and Western pattern
Prudent pattern and traditional pattern
Prudent pattern,
China (SCHS)
USA (HPFS)
USA (NHS)
United Kingdom (HCS)
Swiss
P
(5.3 year)
P
(12 year)
P
(6 year)
C
General population n = 52,325
Health professionals n = 42,917
Nurses
n = 72,043
General population
n = 1391 (F), n
= 1551 (M)
General
F, M (45–74
year)
M (40–75
year)
F (30–55 year)
F, M (mean 66 year)
F, M (mean
Data-driven dietary patterns
high-CHO diet, Western pattern
(SAPALDIA) C
population
n = 2178
58.6 year)
Dietary Patterns Country
Design (Follow-Up)
Table 1. Cont.
Diet Population Sex (Age) Assessment
Method
Outcome Assessment
Main Results Ref
Western pattern and
USA
General
F, M (mean
Data-driven dietary patterns
Respiratory symptoms (cough,
The Western pattern was associated with higher prevalence of COPD (fifth vs. first quintile: OR = 1.62, 95% CI: 1.33, 1.97, p < 0.001), respiratory
symptoms (wheeze OR = 1.37, 95% CI: 1.11, 1.69,
p = 0.002; cough OR = 1.32, 95% CI: 1.10, 1.59, p =
0.001, phlegm OR = 1.27, 95% CI: 1.05, 1.54, p =
prudent pattern
Cosmopolitan
(ARIC) C
population
n = 15,256
General
54.2 year) FFQ and PCA
phlegm, wheeze), FEV1, FEV1/FVC,
COPD prevalence
FEV1, wheeze,
Spirometry
Spirometry
0.031), and worse lung function (e.g., percent
predicted FEV1: fifth quintile 91.8 vs. first quintile 95.1, p < 0.001). The prudent pattern was associated with lower prevalence of COPD (OR = 0.82, 95% CI: 0.70, 0.95, p = 0.007), cough (OR =
0.77, 95% CI: 0.67, 0.89, p < 0.001), and higher
lung function (e.g., percent predicted FEV1: fifth quintile 94.3 vs. first quintile 92.7, p < 0.001)
The traditional pattern was associated with lower FEV1 (fifth vs. first quintile, −94.4 mL, 95% CI:−123.4, −65.5, p < 0.001) and increased prevalence of COPD (fifth vs. first quintile, OR =
[151]
pattern, traditional pattern, and refined food dietary pattern
Netherlands (MORGEN-EPIC)
P
population
n = 12,648
General
F, M (mean 41 year)
F, M (mean 45
FFQ and PCA
asthma, COPD prevalence
and
self-reported symptoms
1.60, 95% CI: 1.1, 2.3, p for trend = 0.001); the cosmopolitan pattern was associated with increased prevalence of asthma (fifth vs. first quintile, OR = 1.4; 95% CI: 1.0, 2.0; p for trend =
0.047) and wheeze (fifth vs. first quintile, OR =
1.3, 95% CI: 1.0, 1.5; p for trend = 0.001)
The refined food pattern was associated with a
[152]
Alcohol-consumption
(5 y)
population
n = 2911
Smokers with
year) FFQ and PCA FEV1 Spirometry
nonsignificant greater decline in lung function (−48.5 mL, 95% CI: –80.7, −16.3; p for trend = 0.11)
Alcohol-consumption pattern (OR = 4.56, 95% CI: 1.58, 13.18, p = 0.005) and Westernized pattern (in
[152]
pattern, Westernized pattern, and
MED-like pattern
Spain C
no respiratory diseases
n = 207
F, M (35–70
year)
FFQ and PCA Impaired lung
Spirometry
F) (OR = 5.62, 95% CI: 1.17, 27.02, p = 0.031) were
associated with impaired lung function; a nonsignificant trend for preserved lung function was found for MED-like pattern (OR = 0.71, 95% CI: 0.28, 1.79, p > 0.05)
[153]
Dietary Patterns Country
Design (Follow-Up)
Table 1. Cont.
Diet Population Sex (Age) Assessment
Method
Diet quality scores
Outcome Assessment
Main Results Ref
MED diet score
Spain (ILERVAS)
Nurses n =
73,228 (NHS)
Health professionals n = 47,026 (HPFS)
Stable COPD
n = 121
General population n = 3020
F (30–55 year),
M (40–75)
F, M (mean 66.1 year)
F (50–70 year),
M (45–65
year)
FFQ and diet quality index (AHEI-2010)
FFQ and diet quality index (HEI, and MED score)
FFQ and MED score
COPD incidence Self-reported
COPD severity Spirometry
FEV1, FVC, Spirometry
/
A higher AHEI-2010 diet score was associated with lower COPD risk (for the fourth fifth of the score, HR = 0.67, 95% CI: 0.53, 0.85, p for trend
<0.001)
Higher MED score was associated with lower FEV1 and FCV. MED score and AHEI decreased as COPD severity increased (NS)
A lower MED diet score was associated with impaired lung function in F (low vs. high adherence, OR = 2.07, 95% CI: 1.06, 4.06, p =
0.033) and the presence of obstructive ventilator defects in M (low vs. high adherence, OR = 4.14,
95% CI: 1.42, 12.1, p = 0.009)
[154]
[155]
[156]
Abbreviations: AHEI = Alternate Healthy Eating Index; ARIC = atherosclerosis risk in communities; C = cross-sectional; CHO = carbohydrate; CI = confidence interval; BMI = body mass index; F = female; FEF25-75 = forced expiratory flow at 25-75%; FEV1 = forced expiratory volume in one second; FFQ = food frequency questionnaire; FVC = forced vital capacity; HCS
= Hertfordshire cohort study; HEI = Healthy Eating Index; HPFS = Health Professionals Follow-up Study; HR = hazard ratio; ILERVAS = Ilerda vascular project; M = male; MED = Mediterranean; MORGEN-EPIC = Monitoring Project on Risk Factors and Chronic Diseases in the Netherlands—European Prospective Investigation into Cancer and Nutrition; NHS = Nurses’ Health Study; NS = not significant; OR = odds ratio; P = prospective; PCA = principal component analysis; RR = relative risk; SAPALDIA = Swiss Cohort Study on Air Pollution and Lung and Heart Diseases in Adults; SCHS = Singapore Chinese Health Study.
7.1. Data-Driven Dietary Patterns and COPD
A cohort study in Chinese Singaporeans found that the meat–dim sum dietary pattern (red meat, preserved foods, rice, noodles, deep-fried foods) was associated with an increased incident cough with phlegm (odds ratio (OR) = 1.43 comparing fourth to first quartile, p for trend = 0.02) [146], indicating a deleterious effect of a diet rich in meat, starchy foods, and high-fat dairy products on respiratory symptoms. Two prospective studies in US health professionals identified two distinct major dietary patterns, the “prudent pattern”, loaded by a high intake of fruits and vegetables, oily fish, poultry, wholegrain products, and low-fat dairy products, and the “Western pattern”, characterized by a high consumption of refined grains, cured and red meats, desserts, French fries, and high-fat dairy products [147,148]. Both studies consistently found that the “prudent” pattern was negatively and the Western pattern positively associated with the risk of self-reported newly diagnosed COPD in women [148] and men [147] after adjustment for several potential confounders, including measures of tobacco exposures. In contrast with findings for COPD, the dietary patterns were not associated with the risk of adult-onset asthma. Notably, the effect of each dietary pattern was stronger in men than in women [147,148]. For the prudent pattern, the relative risk (RR) for highest vs. lowest quintile was
0.50 (p for trend = 0.02) in the men cohort [147], and 0.75 (p for trend = 0.02) in the women cohort [148]. For the Western pattern, the RR for highest vs. lowest quintile was 4.56 (p for trend <0.001) in the men cohort [147], and 1.31 (p for trend = 0.02) in the women cohort [148]. As several individual foods of the “prudent” or the “Western” diet might be related to COPD, as discussed in previous paragraphs, the “prudent” and the “Western” diet patterns reflect the possible combinatory effects of these diverse but highly correlated foods.
Cross-sectional studies confirmed the associations between dietary patterns and respiratory symptoms, lung function, and COPD. A study in the UK population observed that a similar “prudent” dietary pattern was positively associated with lung function (FEV1) in males and females (difference in mean FEV1 between highest vs. lowest quintiles of pattern score = 180 mL in men, p for trend <0.001, and 80 mL in females, p for trend = 0.008), and negatively associated with COPD prevalence in males (54% reduction, p for trend = 0.012) [149]. Associations in males were stronger among smokers than nonsmokers [149]. In this study, the second dietary pattern identified in the study subjects, i.e., the “traditional” pattern, was similar to the unhealthy Western dietary pattern of other studies [147,148], but here, it was not associated with any negative outcome, probably because of its relatively high fish and vegetables content. A “prudent” diet was confirmed to be associated positively with FEV1 and negatively with COPD prevalence, not significantly in a large sample (n = 2,178) of Swiss adults (changes in FEV1 per unit increment in the dietary pattern score = 23 mL, p = 0.08; COPD prevalence OR = 0.90, p = 0.21) [150], as well as in a significant manner in a US population-based study (COPD prevalence OR = 0.82, p for trend = 0.007) where protective effects by the prudent pattern were also observed on respiratory symptoms (cough), whereas a Western diet was associated with higher prevalence of COPD (OR = 1.62, p for trend <0.001), worse respiratory symptoms, and lower lung function [151].
In a population of around 12,000 adults from the Netherlands, McKeever et al. [152] identified three major dietary patterns, the “cosmopolitan pattern” (higher intakes of vegetables, fish, chicken, wine, and lower intakes of high-fat dairy products, added fat, added sugar, and potato), the “traditional pattern” (higher intakes of red meat, processed meat, potato, boiled vegetables, added fat, coffee, and beer and lower intakes of soy products, low-fat dairy products, tea, breakfast cereal, brown rice, pizza, juice, and fruit), and the “refined food dietary pattern” (higher intakes of mayonnaise, salty snacks, candy, high-sugar beverages, French fries, white bread, and pizza and lower intake of boiled vegetables, wholegrains, fruit, and cheese). These dietary patterns were analyzed for their relation to lung function (FEV1) and symptoms of COPD as well as to longitudinal change in FEV1. When nutrient intake associated with the diets was analyzed, the “cosmopolitan” diet was positively correlated with intake of alcohol, vitamin C, and beta-carotene, the “traditional” diet was positively associated with alcohol and total fat intake, and negatively with carbohydrate intake, and the “refined food” diet was negatively associated with magnesium, fiber, and vitamin C intake [152]. In the cross-sectional analysis, the “traditional” diet was associated with a lower lung function (−94.4 mL, p for trend <0.001) and an higher prevalence of COPD (OR = 1.6, p for trend = 0.001), while the “cosmopolitan” diet was associated with a small increased prevalence of asthma and wheeze. None of the dietary patterns were associated with a decline in lung function over 5 years, although a higher intake of refined foods was associated with a greater decline in lung function (−48.5 mL, p for trend = 0.11) [152]. Accordingly, in a Spanish population of adult smokers without respiratory diseases, three major dietary patterns were derived: alcohol-consumption pattern (loaded by intake of wine, beer, and/or distilled drinks), Westernized pattern (loaded by high consumption of cured and red meats, dairy products, and sugary drinks, desserts and sweets, and low in fruits, vegetables, legumes, and fish), and Mediterranean-like pattern (loaded by high intake of poultry, eggs, fish, vegetables, legumes, potatoes, dairy desserts, fruits, nuts, and dried fruit) [153]. When the prevalence of impaired lung function (as determined by spirometry) across tertiles of dietary patterns was analyzed, impaired lung function was observed in all participants with an alcohol consumption pattern (OR = 4.56, p for trend = 0.005) especially in women (OR = 11.47, p for trend = 0.003), and in women with the Westernized pattern (OR = 5.62, p for trend = 0.031). By contrast, the Mediterranean-like dietary pattern was not significantly associated with impaired lung function, but with a trend for preserved lung function (OR = 0.71, p for trend >0.05), suggesting that it may protect lung function against the deleterious effects of smoking [153].
The study by Sorli-Aguilar et al. [153] provides some new information: (1) it restricted the observation to smokers, thus stressing the importance of eating pattern, in addition to smoking cessation, as a possible preventive measure for improving lung health; (2) it provides a first report on the association between a Mediterranean-like diet and lung function. An impressive and unprecedented accrual of high-quality evidence from observational and interventional studies converges to the recognition of the traditional Mediterranean diet as one of the healthiest dietary patterns, being protective against incidence and mortality of major chronic diseases, mainly CVD and cancer [157,158]. However, limited evidence exists for a role in obstructive respiratory diseases and mostly regards asthma [159]. As discussed above, many individual foods and nutrients characteristic of the Mediterranean diet and endowed with anti-inflammatory, antioxidant, and beneficial metabolic properties (fruits, vegetables, seafood, nuts, legumes, vitamins, polyphenols, etc.) have been associated to improved lung function and COPD prevention in several studies. The Mediterranean-like diet pattern described by Sorli-Aguilar et al., the healthiest one compared to the other dietary patterns identified, included key foods of the traditional Mediterranean diet (fruits, vegetables, legumes, wholegrains, nuts, olive oil, fish) [160] and was similar to the “prudent” patterns that have been previously found to protect against impaired lung function and COPD risk [147–149]. However, it cannot be strictly defined as a traditional Mediterranean diet because it also included non-Mediterranean diet/unhealthy components, such as red and processed meats, desserts, sweets, and refined grains [153]. This may have diluted or masked the possible positive effect on lung function by other beneficial components. Of course, more investigations (mostly interventional in design) in different populations and countries are needed to confirm Mediterranean diet health benefits in COPD.
7.2. Diet Quality Scores and COPD
In addition to data-driven approaches to derive dietary pattern, a priori-defined diet quality scores have also been used to assess and/or confirm the relationship of diet with lung function and risk and outcomes of COPD (Table 1). In order to measure compliance to the Dietary Guidelines for Americans (DGAs) and provide dietary guidance for healthy eating, two dietary indices, the Healthy Eating Index (HEI) [161] and the Alternate Healthy Eating Index (AHEI) (2005 and 2010 editions) [162], a modified version of the HEI, have been developed and used in the US population and subpopulations. Apart from some distinctive features, such as more attention to fat quality, inclusion of moderate alcohol intake, cereal fiber, red-to-white meat ratio, and duration of multivitamin use in the AHEI compared to the original HEI, both scores reflect a dietary pattern characterized by high intakes of wholegrains, PUFAs, nuts, and long-chain n-3 fats and low intakes of red/processed meats, refined grains, and sugar sweetened beverages, and have been found to beneficially impact health outcomes. Indeed, the AHEI was inversely associated with incidence and mortality from chronic diseases (CVD, diabetes, and cancer) [163,164]. Using the AHEI-2010 score, a recent several year-long prospective study in participants of the US Nurses’ Health Study (NHS, n = 73,000 women) and Health Professionals Follow-up Study (HPFS, n = 47,000 men) [154] found that higher AHEI-2010 diet score was associated with a 33% lower risk of newly diagnosed COPD in both men and women, without any effects by smoking status and after adjustment for several confounding factors (multivariable HR for eating the healthiest diet compared to eating the least healthy diet = 0.67, p for trend <0.001). This negative association also persisted after excluding participants with cancer and CVD at baseline (multivariable HR for eating the healthiest diet compared with eating the least healthy diet = 0.71, p for trend = 0.007), indicating a direct effect of a healthy diet on COPD beyond its association with other chronic diseases. Contrarily, no association was found between AHEI and the risk of adult onset asthma. Although obtained in health professionals with differences in health awareness, socioeconomic status, and smoking behavior compared to the general population, these results extend the relevance of the AHEI-2010 diet score and its main dietary features to COPD. When the association between individual components of the score and the risk of COPD was analyzed, high intake of fruit and wholegrains, and low intake of red and processed meat and sugar sweetened drinks and fruit juice were associated with lower risk of COPD [154], confirming some previous findings about the respiratory benefits of similar dietary patterns, in agreement with the antioxidant and anti-inflammatory diet hypothesis [148,149].
Another more recent study used the HEI (2005 and 2010 editions) diet score and a modified version
of the Mediterranean diet score [165] to assess the cross-sectional association of these two diet quality scores with COPD severity (according to GOLD stages) and parameters of lung function (FEV1 and FVC) in 121 patients with stable COPD [155]. Both scores reflected high intakes of fruits, vegetables, wholegrains, PUFAs, MUFA, nuts, legumes, and low intakes of refined grains, red/cured meat (and red meat to white meat ratio), saturated fat, empty calories, and sodium. In particular, the Mediterranean diet score, from its original conception [165] to the latest modifications [166], is intended to capture compliance to the plant-based eating patterns of olive tree-growing areas of the Mediterranean basin. According to both HEI and Mediterranean diet scores, the diet quality of the study subjects appeared to need improvements. Although not reaching significance, reduced HEI and Mediterranean diet scores were observed with increased COPD severity, mostly stage 4, and a one-unit increase of the Mediterranean diet score was significantly associated with 2.9 (p = 0.002) and 2.8 (p = 0.007) increase of FEV1 and FVC, respectively [155]. Although obtained in a small sample of already diseased subjects, these results further suggest protective effects on lung function by the Mediterranean diet pattern. Further high-powered confirmatory studies as well as the evaluation of diet effect on COPD progression over time are highly warranted.
In a very recent cross-sectional study conducted in middle-aged healthy subjects at low-to-moderate CV risk but without pulmonary diseases (Ilerda Vascular Project, ILERVAS) [156], low adherence to the Mediterranean diet as well as low physical activity practice were independently associated with the presence of impaired spirometric values and with ventilatory defects, compared with high adherence to the Mediterranean diet and vigorous physical activity. Therefore, although we are still awaiting interventional studies providing causality, these results agree with those previously obtained with dietary pattern analysis [153] and collectively suggest a beneficial association between the Mediterranean diet and lung function with relevance to both the prevention of respiratory diseases as well as the improvement of COPD.
In a large prospective Asian cohort study, adherence to several recommended dietary patterns as reflected in the AHEI-2010, the alternate Mediterranean diet score, the dietary approaches to stop hypertension (DASH) score, and the healthy diet indicator (HDI), and based on healthy plant-based foods and fish, was associated with a substantially lower risk of 17-year all-cause and disease-specific
(CVD, cancer and respiratory disease) mortality, specifically with a 14–28% lower risk of mortality for respiratory diseases [167]. Interestingly, COPD was one of the predominant respiratory conditions contributing to respiratory disease mortality in the study cohort. These results agree with earlier reports of an inverse association between intake of single dietary components of these dietary patterns, such as fruits, and COPD mortality [53]. Other studies in different populations confirmed the beneficial association between adherence to the DASH diet and COPD risk [168], and adherence to the healthy Dutch dietary guideline and the risk of all-cause mortality and COPD development [169].
Collectively, although needing further confirmations, published studies concordantly suggest a significant role for high-quality whole diet on lung function outcomes and COPD incidence and prevalence, as well as on mortality. Adhering to dietary patterns resembling the general principles of the Mediterranean diet and the prudent diets, which emphasize a variety of healthy plant-based foods (vegetables, fruit, nuts, wholegrains) and fish, avoidance of heavy alcohol intake, and low consumption of foods typical of Westernized patterns (red/processed meat, refined grains, sweets/desserts), exerts beneficial effects in contrast with Western diets (Figure 2). Interestingly, the Western diet has been shown to be positively associated while the prudent/Mediterranean diet inversely associated with serum levels of inflammatory markers [170,171]. Moreover, beneficial effects have also been documented for bioactive nutrients of the healthy diets, such as polyphenols and PUFAs, against visceral adiposity and related inflammation/oxidative stress, mitochondrial dysfunction, as well as insulin resistance [172], thus potentially providing the opportunity to favorably manage the risk associated with metabolic derangements observed in some patients with COPD (obesity and/or abdominal visceral adiposity).
Western-like diet Mediterranean/prudent-like diets
Refined and high energy- dense foods, red/processed meat, added sugar:
Salt Preservatives
Low antioxidants/vitamins Low fiber
High glycemic index Saturated/trans fat
Pollution
• Inflammation
• Oxidative/nitrosative stress
• Antioxidant depletion
• Mucus hypersecretion
• Alveolar wall destruction
• Defective tissue repair
• Airway remodeling
Fruits, vegetables, whole grains, alcohol/wine, legumes, coffee, nuts, fish: High antioxidants/vitamins High fiber
Low glycemic index Unsaturated (n-3 PUFA, MUFA) fat
Genetics
Smoking Age
Figure 2. A framework model of the interactions of diets and dietary factors with lung function and COPD development and progression.
In addition to directly improving inflammation, oxidative stress, and immune and metabolic deregulation, dietary factors may act by inducing modification of gut microbiota, which can influence
immune system, systemic inflammation, and metabolism through the production of locally- and systemically-active metabolites, such as the fiber fermentation-derived short chain fatty acids (SCFAs) (butyrate, propionate and acetate) or the carnitine/choline-derived trimethylamine-N-oxide (TMAO). Human studies have found that plant-based diets such as the Mediterranean diet (rich in fiber) shaped the composition of gut microbiota so as to increase the circulating levels of anti-inflammatory SCFAs, while animal-based diets such as the Western diet (rich in carnitine and choline from meat, egg yolks, and high-fat dairy products) were associated with increased levels of the pro-inflammatory TMAO, which is linked to risk of atherosclerosis, CV disorders, and mortality [173]. An emerging concept and potential therapeutic opportunity for dietary modulation is the gut–lung axis, where intestinal microbial modulation can influence the respiratory system [174]. Indeed, high dietary fiber intake was shown to protect against inflammatory airways disease via systemic SCFAs [175]. Moreover, increased circulating TMAO levels were associated with long-term all-cause mortality in patients with COPD [176]. Of course, further studies are required to address whether gut–lung axis modulation by nutrition would beneficially impact lung function and the risk or evolution of COPD.
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