Dietary Patterns and Chronic Obstructive Pulmonary Disease: A Meta-analysis

ABSTRACT

Investigation of the relationship between dietary patterns and some chronic noncommunicable diseases has become appealing in nutritional epidemiology. Some studies have reported potential associations between dietary patterns and the risk of chronic obstructive pulmonary disease; however, the results remain conflicting. Thus, we conducted this meta-analysis to pool the results of studies to clarify the associations between dietary patterns and the risk of chronic obstructive pulmonary disease. A literature search of MEDLINE and EBSCO databases was performed to identify relevant studies published from January 1990 up to June 2015. A total of 13 studies met the inclusion criteria and were included in this meta-analysis. The highest category of healthy/prudent dietary patterns when compared with the lowest category was apparently associated with a decreased risk (OR = 0.55; CI: 0.46, 0.66; P < 0.0001). An increase in the risk of chronic obstructive pulmonary disease was shown for the highest compared with the lowest categories of “unhealthy/western-style” dietary patterns (OR = 2.12; CI: 1.64, 2.74; P < (0.0001). The results of this meta-analysis indicate that different dietary pattern may be associated with the risk of chronic obstructive pulmonary disease.

KEYWORDS:

• chronic obstructive pulmonary disease
• dietary patterns
• meta-analysis

Introduction

Chronic obstructive pulmonary disease (COPD) is a progressive multi-organ systemic disease and the third leading cause of death in the world (1). In China, COPD has achieved a prevalence of 8.2% in adults over 40 years old, accounting for more than one million deaths and five millions disabilities each year (2). It is well known that COPD is considered as a product of genetic and environmental factors (3). Among these environmental factors, changes in diet are important risk factors for and progression of COPD (4).

In the past decade, some epidemiological studies have shown that dietary factors play an important role in the prevention of COPD and examined the associations between the intake of individual foods or nutrients and the risk of COPD (5,6). Because foods are consumed together and nutrients may interact (7), it has been proposed that whole-diet should be assessed instead of the individual foods or nutrients. Consequently, the analysis of dietary pattern becomes a more recognizable approach, which takes into account the combined effects of foods and potentially facilitates nutritional recommendations (8).

More recently, the considerable attention has been focused on medical research about the associations between overall dietary patterns and the risk of COPD (9–12). However, the relation between dietary patterns and COPD risk remains unclear. Therefore, we conducted a systematic meta-analysis of studies published from January 1990 up to June 2015, to further clarify the potential associations between different dietary patterns and the risk of COPD,

Methods

Literature search strategy

An electronic literature search of MEDLINE and EBSCO databases was conducted to identify relevant studies written in the English and Chinese languages published from January 1990 up to June 2015, with the following keywords or phrases: diet, dietary, dietary habit, food pattern, eating pattern, dietary pattern, dietary patterns, chronic obstructive pulmonary disease and COPD. In addition, we manually searched all references cited in original studies and reviews identified.

Study-included criteria

Authors Shu and Si read the abstracts of articles retrieved in the initial search to identify studies that examined the associations between dietary patterns and risk of COPD. When Shu, Zhang, and Si agreed, the articles were reviewed against inclusion and exclusion criteria for this meta-analysis. To be eligible, the studies had to fulfill the following criteria: (1) The study was an original report investigating the association between dietary patterns and the risk of COPD; (2) Odds ratios and percentage of COPD (or sufficient information to calculate them) had been listed (5); COPD was diagnosed based on the affirmative response to physician-diagnosed chronic bronchitis or emphysema and by the report of a diagnostic test at diagnosis (pulmonary function testing, chest radiography or chest CT scanning). In total, 427 studies reported the relationship between dietary patterns and the risk of COPD.

Data extraction

Data extracted from all eligible studies including authors, the year of publication, geographic, the study design, the sample size, percentage of COPD, the number in each dietary pattern, the method of dietary assessment, identification of dietary patterns and the factors that were adjusted for in the analysis.

Assessment of heterogeneity

Heterogeneity of study results was estimated by the chi-squared test. P values less than 0.05 were considered to be significant. In our analyses, a random-effects model was used to account for possible heterogeneity between studies, while a fixed-effects model was adopted in the absence of heterogeneity (13).

Quality assessment

The Newcastle–Ottawa Quality Assessment scale was used for quality assessment (14). Eight questions were assessed and each satisfactory answer received 1 point (may receive 2 points in comparability categories), resulting in a maximum score of 9. Only those studies in which most of the questions were deemed satisfactory (i.e., with a score of 6 or higher) were considered to be of high methodological quality.

Statistical analysis

Statistical analyses were conducted using Review Manager, version 5.0 (Nordic Cochrane Centre Copenhagen, Denmark) and STATA, version 12 (Stata Corp, College Station, TX, USA). All statistical tests were two-sided and P values less than 0.05 were considered significant. The original papers reported the results of dietary patterns in terms of tertiles, quartiles, and quintiles of dietary factor scores and the risk of COPD. We conducted meta-analysis to assess the risk of COPD in the highest versus the lowest categories of healthy/prudent and unhealthy/western-style dietary patterns. Random-effect models were used to calculate the pooled odd ratio (OR) for dietary patterns in highest categories compared with lowest categories. Odds ratios and 95% CIs from individual studies were combined to produce an overall OR. Publication bias was assessed using Begg's test and Egger's test and funnel plots (15).

Results

Overview of included studies for the systematic review

An electronic literature search in the database of MEDLINE and EBSCO identified 427 studies, 414 of which were excluded based on the reasons listed in Figure 1. Thirteen articles (9–12, 16–24) met the inclusion criteria and were included in this meta-analysis, including seven (9–11, 17, 18, 22– 23) cohort studies, three (12, 20, 21) cross-sectional studies, and three (16, 19, 24) case-control studies. Descriptive information for each included study was presented in Table 1.

Table 1. Characteristics of 13 studies included in the meta-analysis (1990–2015).

Author Publication Year	Location	Study design	Total number of subjects	Age	Diet-assessment method	Factors adjusted for in analysis	Dietary patterns Identified
Varraso et al (n = 2)2007[9)	United States	Cohort	72043 women	30-55y	FFQ	Age, smoking status, pack-years, exposure to secondhand tobacco smoke, menopausal status, race/ethnicity, spouse's educational attainment, physician visits, U.S. region, physical activity, multivitamin use, and energy intake.	Prudent; western
Shaheen et al 2010 [10)	United Kingdom	Cohort	Male:1551; Female:1391	Male:65.7 Female:66.6y	FFQ	Age, height, smoking status, pack-years, smoke in home, age left education, home ownership status, number of rooms, cars, social class, fat mass, activity score, energy intake, alcohol dietary supplement use, birth weight, father's social class at birth, inhale or oral steroids use, paracetamol use	Prudent
Varraso et al (n = 3) 2007[11)	United States	Cohort	42917 men	40-75y	FFQ	Age, energy intake, smoking status, pack-years, race/ethnicity, physician visits, U.S. region, body mass index, physical activity and multivitamin use	Prudent; western
McKeever et al 2010[12)	Netherlands	Cross-sectional	12648	20-59y	FFQ	Age, sex, age squared, height, age*height, smoking status, pack-years of smoking, BMI, and educational level	Cosmopolitan diet; traditional diet; refined-foods diet
Waston et al 2002 [16)	Ireland	Case-control	115 cases 115 controls	> 45y	FFQ	Age, body mass index and total energy.	Total vegetables and fruit
Varraso et al 2015 [17)	United States	Cohort	73228 female 47026 male	Female 30-55y Male 40-75y	FFQ	Age,physical activity, body mass index, total energy intake, smoking status, pack years of smoking, secondhand tobacco exposure, race/ethnicity, physician visits, U.S. region, spouse, Highest education attainment, and menopausal status	Alternate healthy eating index
Yin et al 2011 [18)	China	Cohort	48974	15-69y	FFQ	Age, sex, region, smoking, history of COPD	Vegetables and fruit consumption
Hirayama et al 2009[19]	Japan	Case-control	278 cases 340 controls	50-75y	FFQ	Age, gender, BMI, education level, alcohol drinking, cigarette smoking, smoking pack-years, lifelong physical activity involvement, and daily intake of red meat, chicken and fresh fish.	Total vegetables and fruits
Jiang et al 2007[20]	United States	Cross-sectional	7352	>45y	FFQ	Age, sex, race/ethnicity, smoking variables, smoking status, pack-years of smoking, serum cotinine concentration, household environmental tobacco smoking, education, family income, BMI	Cured meat consumption
Kan et al 2007 [21]	United States	Cross-sectional	15792	44-66y	FFQ	Age, sex, study center, ethnicity, smoking status, pack-years of smoking, body mass index, occupation, education, diabetes status, traffic density, total energy intake, glycemic index, micronutrients	Total fiber
Varraso et al 2007[22]	United States	Cohort	51529	40-75y	FFQ	Age, energy intake, smoking status, pack-years, pack-years squared, race/ethnicity, U.S. region, body mass index, and physical activity	Cured meats consumption
Varraso et al 2010[23]	United States	Cohort	121700 female 51529 male	Female: 30-55y Male: 40-75y	FFQ	Age, sex, smoking status, pack-years, energy intake, U.S. region, physician visits, BMI, physical activity, diabetes, omega-3 polyunsaturated fatty acid intake, cured meat intake, and other sources of fiber	Total fiber intake
Yang et al 2015[24]	China	Case-control	1025 cases 1061 controls	—	Questionnaire	Age, sex, BMI, educational experience, and center	Cured meat consumption; Vegetables/fruits consumption

FFQ: Food frequency questionnaire; BMI: Body mass index.

Figure 1. Flow chart of article screening and selection process.

Healthy/prudent dietary pattern

The healthy/prudent dietary pattern is characterized by high intakes of vegetables, fruit, fish and whole-grain products. The association between healthy dietary pattern and the risk of COPD was shown in Figure 2. There was evidence of a decrease in the risk of COPD in the highest compared with the lowest category of healthy dietary pattern (OR = 0.55; CI: 0.46, 0.66; P = 0.005) where all studies were combined in the random-effects model. The heterogeneity was apparent in all the studies (P < 0.00001; I² = 80%).

Figure 2. Funnel plots for COPD in the highest compared with the lowest category of intake of the healthy/ prudent dietary pattern in all studies.

Unhealthy/western-style dietary pattern

The unhealthy/western-style dietary pattern is characterized by high intakes of all kinds of red and/or processed meats, refined grains, sweets, desserts and French fries. Figure 3 showed the association between unhealthy/western-style dietary pattern and the risk of COPD. There was evidence of a increased risk of COPD in the highest compared with the lowest category of “western-style” dietary pattern (OR = 2.12; CI: 1.64, 2.74; P = 0.0002). A random-effects model was used to assess the data. The heterogeneity was apparent in all the studies (P = 0.0004; I² = 71%).

Figure 3. Funnel plots for COPD in the highest compared with the lowest category of intake of the unhealthy/western-style dietary pattern in all studies.

Publication bias

Inspection of funnel plots revealed little evidence of asymmetry (Appendix 1), and Egger's test for publication bias was not statistically significant (highest compared with lowest category: healthy/prudent dietary pattern Begg's test P = 0.583; and unhealthy/Western-style dietary pattern Begg's test P = 0.573).

Quality assessment

Quality of each study in terms of population and sampling methods, description of exposure and outcomes, and statistical adjustment of data, is summarized in Appendix 2. All studies received 6 scores or higher on the Newcastle-Ottawa Quality assessment scale and were considered to be of high methodological quality (9–12, 17, 18, 20–24).

Discussion

Limited epidemiological studies have reported the relationship between dietary patterns and the risk of COPD in Chinese population. To our knowledge, this is the first meta-analysis evaluating the evidence for different dietary patterns and the risk of COPD. The results indicate that healthy/prudent dietary pattern may decrease the risk of COPD, and unhealthy/western-style dietary pattern may increase the risk of COPD. Data from 13 studies involving 550,614 participants were included in our analyses. A recent review of healthy behaviours and COPD risk concluded that an increase in the consumption of vegetables, fruit and fiber may contribute to the prevention of COPD, while cured and red meats, desserts, and refined grains constitute potential risk factors for COPD (25). Although our results were consistent with previous review (25), overall dietary pattern has been considered as an important factor for the prevention of COPD in this study. Our findings have further confirmed the potential association between different dietary patterns and the risk of COPD, and provide the information that may be translated into public health action for primary prevention of COPD.

In our analyses, the healthy/prudent dietary pattern was associated with a decrease in the risk of COPD. This dietary pattern was characterized by high intakes of vegetables, fruit, fish and whole-grain products. Our results are consistent with previous studies (9, 11), suggesting that the favorable effect of healthy/prudent dietary pattern on the prevention of COPD.

The potential protective effect of vegetables and fruits may be due to their high concentration of antioxidant substances (e.g., vitamin C, vitamin E, and other carotenoids compounds). To our knowledge, vitamin A can protect against the development of airway obstructive, reducing the risk of COPD (26). In addition, other studies have suggested that vitamin E not only protected polyunsaturated fatty acids in cell membranes from oxidative damage but also represented the body's principal defense against oxidant-induced membrane injury (27). More specially, greater intake of dietary fiber has been consistently associated with a reduced risk of COPD (21, 23).

Although the mechanism is unclear, the benefit association of dietary fiber with COPD risk may be due to the anti-inflammatory and antioxidant properties of fiber (28–30). Previous studies have reported that dietary fiber intake was associated with reduced level of C-reactive protein, a marker of systemic inflammatory (30). Besides, dietary fiber may modulate inflammation through slowing the absorption of glucose, decreasing lipid oxidation, or influencing the production of anti-inflammatory cytokines by the gut flora (31,32). Furthermore, previous some studies have found that dietary fiber, especially water-soluble fiber (deriving mainly from fruit and vegetables) can also delay the absorption of starch, thus reducing the glucose load and the consequent hyperinsulinemia (33), which is related to the risk of COPD (34).

The unhealthy/western-style dietary pattern was associated with an increased risk of COPD in this meta-analysis. Our findings were in agreement with previous findings (9, 11, 20), which indicated that red or processed meat intake was associated with increased risk of COPD. To our knowledge, there are several possible explanations for the positive association between unhealthy/western-style dietary pattern and the risk of COPD. First, cured or processed meat often contains a high content of nitrates or nitrites, and nitrosamine compounds.

Nitrites generate reactive nitrogen species which may amplify inflammatory processes in the airways and lung parenchyma causing DNA damage, inhibition of mitochondrial respiration, and nitrosative stress, thereby contributing to the progressive deterioration in pulmonary function (35). Second, some food (such as defined grains and desserts) in western-style dietary pattern has a high glycaemic index. Previous studies have suggested that hyperglycaemia is associated with impaired lung function, which is the main measurement for diagnosis of COPD (34, 36).

In addition, COPD has yet been found to be associated with some traditional factors (e.g., smoking, physical activity, educational level). A recent systematic review of smoking and COPD risk concluded that smoking was associated with an increased risk of COPD (37). In fact, smoking has been consistently considered as a major risk factor for COPD. A case-control study conducted from 2000 to 2001 in Nanjing indicated there was a significant dose-response relationship between COPD and total amount of cigarettes smoked, after adjusting for other risk factors (38). Meantime, the association between COPD and obesity has been extensively studied.

Previous studies have found that obesity may contribute to other respiratory illnesses, including asthma, sleep apnea, pulmonary embolism, and hypoventilation syndrome (39). Additionally, low BMI have also been reported to be closely associated with a high incidence of COPD (40).

Furthermore, a previous observational study found that educational level and the individual^’s socioeconomic status were also correlated to the prevalence of COPD (10). To our knowledge, other factors such as outdoor and indoor air pollution, reduced physical activities, and occupation have all been reported to contribute to the increased incidence of COPD (25, 41). Annesi-Maesano et al. (25) reported that COPD was associated with a decrease in physical activity, which is thought to occur primarily as a consequence of dyspnoea included by increased ventilatory constraints.

Strengths and limitations

This meta-analysis holds its own strengths and limitations. First, this is the first meta-analysis reporting the associations between dietary patterns and the risk of COPD. Second, the cases of COPD have been confirmed through the affirmative response to physician-diagnosed chronic bronchitis or emphysema and by the report of a diagnostic test at diagnosis (pulmonary function testing, chest radiography or chest CT scanning), avoiding misdiagnosis. Third, all ORs are statistically significant in two dietary patterns and they make our review more credible in this meta-analysis. Finally, no signs of publication bias were evident in the funnel plot, and the statistical test for publication bias was non-significant. However, some limitations should be considered in present meta-analysis.

First, the principal limitation of this study was the use of potentially biased evidence. There was an inconsistent adjustment for potential confounders among the included studies. As a result, the data included in our analyses might suffer from differing degrees of completeness and accuracy. Second, 6 of 13 studies used a case-control or cross-sectional design, which is more susceptible to recall and selection bias, especially dietary recall bias, than a cohort design. Finally, this meta-analysis involved 13 studies, most from Europe and North America (10 studies). Thus, the association between dietary patterns and COPD may be reflected in European and North American people and could not be expanded to all populations.

Conclusion

In summary, this meta-analysis indicate that healthy/prudent dietary pattern is associated with a decreased risk of COPD, whereas the unhealthy/western-style dietary pattern is associated with an increased risk of COPD. Our findings may highlight the importance of diet changing for the primary prevention of COPD. Nowadays, dietary patterns are changing rapidly worldwide, while the prevalence of some chronic non-communicable diseases, including COPD, hypertension, diabetes, et al, which are associated with diet, are increasing rapidly. It makes it necessary to study the associations between different dietary patterns and some chronic non-communicable diseases.

Acknowledgments

The authors thank all participants from the Department of Nutrition, Zhejiang Hospital, Zhejiang, China.

Declaration of interest statement

The authors declared no conflict of interest. The authors alone are responsible for the content and writing of the paper.

Funding

This study was supported by the Joint Construction of Projects by Provinces and the Ministry of Education (Grant No. 2014PYA002).

Appendix 1

Dietary patterns and chronic obstructive pulmonary disease: Assessment of Study Quality

	Selection				Comparability		Outcome
Studies	1	2	3	4	5A	5B	6	7	8	Score
Cohort
Varraso et al. (n = 2) (2007)	*	*	*	*	*	*	*	*	*	*********
Shaheen et al. (2010)		*	*	*	*		*	*		******
Varraso et al. (n = 3) (2007)	*	*	*	*	*	*	*	*	*	*********
Varraso et al. (2015)	*	*	*	*	*		*	*	*	********
Yin et al. (2011)	*		*	*	*		*	*		******
Varraso et al. (2007)	*		*	*	*		*	*	*	*******
Varraso et al. (2010)	*	*	*	*	*	*	*	*	*	*********
Case-control
Waston et al. (2002)			*	*	*		*	*		*****
Hirayama et al. (2009)	*			*	*		*	*		*****
Yang et al. (2015)	*		*	*	*		*	*		******
Cross-sectional
McKeever et al. (2010)	*		*	*	*		*	*		******
Jiang et al. (2007)	*		*	*	*		*	*		*******
Kan et al. (2007)	*	*	*	*	*		*	*		*******

FFQ: Food frequency questionnaire; BMI: Body mass index.

Appendix 2

Forest plot for ORs of the highest compared with the lowest category of intake of the healthy/prudent dietary pattern and COPD.

Forest plot for ORs of the highest compared with the lowest category of intake of the unhealthy/western-style dietary pattern and COPD.