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Previous Volume 331:228-233 July 28, 1994 Number 4 Next

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ABSTRACT

Background Fish contain n-3 polyunsaturated fatty acids, principally eicosapentaenoic acid and docosahexaenoic acid, which are known to interfere with the body's inflammatory response and may be of benefit in chronic inflammatory conditions.

Methods We studied the relation between the dietary intake of n-3 fatty acids and chronic obstructive pulmonary disease (COPD) in 8960 current or former smokers participating in a population-based study of atherosclerosis. Intake of fatty acids was estimated with a dietary questionnaire. The presence of COPD was assessed by a questionnaire on respiratory symptoms and by spirometry. Three case definitions of COPD were used: symptoms of chronic bronchitis (667 subjects), physician-diagnosed emphysema reported by the subject (185 subjects), and spirometrically detected COPD (197 subjects).

Results After control for pack-years of smoking, age, sex, race, height, weight, energy intake, and educational level, the combined intake of eicosapentaenoic acid and docosahexaenoic acid was inversely related to the risk of COPD in a quantity-dependent fashion. The adjusted odds ratio for the highest quartile of intake as compared with the lowest quartile was 0.66 for chronic bronchitis (95 percent confidence interval, 0.52 to 0.85; P<0.001 for linear trend across the range of intake values), 0.31 for physician-diagnosed emphysema (95 percent confidence interval, 0.18 to 0.52; P for linear trend, 0.003), and 0.50 for spirometrically detected COPD (95 percent confidence interval, 0.32 to 0.79; P for linear trend, 0.007).

Conclusions A high dietary intake of n-3 fatty acids may protect cigarette smokers against COPD.

Chronic bronchitis and emphysema, referred to collectively as chronic obstructive pulmonary disease (COPD), are important causes of morbidity and mortality among persons who smoke cigarettes⁸. The pathogenic mechanisms linking cigarette smoke to these diseases are not entirely understood, but inflammatory mediators are likely to be involved,⁹ including those that may be influenced by n-3 fatty acids¹⁰. We therefore hypothesized that smoking-related COPD is inversely related to dietary intake of n-3 fatty acids.

Methods

Study Subjects

The study sample was drawn from the participants in the Atherosclerosis Risk in Communities (ARIC) study,¹¹ a prospective study of atherosclerotic disease. We used probability sampling to recruit a cohort of 15,800 men and women 45 to 64 years of age from 1986 through 1989 in four U.S. communities: Forsyth County, North Carolina; Jackson, Mississippi; the suburbs of Minneapolis; and Washington County, Maryland. Blacks were oversampled in Forsyth County and were sampled exclusively in Jackson, whereas in the other two communities the subjects were overwhelmingly white. The response rate was 46 percent in Jackson and ranged from 65 to 67 percent in the other three communities. After providing informed consent, the subjects underwent a comprehensive examination that included a dietary assessment and measurements of lung function. The study was approved by the institutional review boards of the participating universities.

Smoking-Related Measurements

The subjects were classified as current smokers, former smokers, or persons who had never smoked. The lifetime number of pack-years of cigarette smoking was computed by multiplying the average number of cigarettes smoked per day by the number of years of smoking and dividing by 20. Each subject's respiratory symptoms were elicited by a standardized interviewer-administered questionnaire adapted from the Epidemiology Standardization Project¹².

Anthropometric and Demographic Measurements

Height was measured to the nearest centimeter with a vertical metal ruler. Weight was measured to the nearest pound and converted to kilograms; the subjects wore lightweight examination gowns and no shoes. Educational level was categorized as being below the high-school level, at the level of a high-school diploma or the equivalent, or beyond the high-school level.

Dietary Assessment

Usual dietary intake was estimated from an interviewer-administered questionnaire modified from a 61-item questionnaire developed and validated by Willett and colleagues¹³. The subjects were asked how often, on average, they had consumed certain foods in portions of a specified size (e.g., 85 to 113 g [3 to 4 oz] of canned tuna fish) during the preceding year. There were nine possible responses, ranging from "almost never" to "more than six times per day." Daily intake of nutrients was calculated by multiplying the nutrient content of each food in the portion specified by the frequency of daily consumption and summing the results. The nutrient content of each food was obtained from the Harvard nutrient data base,¹³ for which the primary source was the Department of Agriculture handbook¹⁴.

Fish consumption, the main dietary source of n-3 fatty acids,¹⁵ was estimated by summing the reported consumption of three items: 85 to 113 g of canned tuna fish, 85 to 142 g (3 to 5 oz) of dark-meat fish (e.g., salmon, mackerel, swordfish, sardines, or bluefish), and 85 to 142 g of other fish (e.g., cod, perch, or catfish). The eicosapentaenoic acid and docosahexaenoic acid content of these foods was estimated to be 190 and 500 mg, respectively, for tuna fish, 560 and 780 mg for dark-meat fish, and 240 and 460 mg for other fish.

Spirometric Measurements

Lung function was measured according to a standard protocol based on the guidelines of the Epidemiology Standardization Project¹² and the American Thoracic Society,¹⁶ using a Collins Survey II volume-displacement spirometer (Warren E. Collins, Braintree, Mass.) that was connected to an IBM PC/XT computer by the calibration and analytic programs of the Pulmo-Screen II system (S&M Instrument, Doylestown, Pa.). The computer programs were modified to accommodate the ARIC protocols for linearity and electronic storage of spirograms. The technicians were trained and certified, and their performance was closely monitored by the staff of the pulmonary-function reading center.

During at least five forced expirations, the technician attempted to obtain three acceptable spirograms at least two of which had similar results, within 5 percent, for forced expiratory volume in one second (FEV₁) and forced vital capacity (FVC). The acceptability and reproducibility of the spirograms were indicated by the computer program, confirmed by the technician observing the volume-time spirograms, and ultimately determined at the reading center. The largest FEV₁ and the largest FVC on any of the acceptable tests were used¹⁶. Sex-specific predicted values for FEV₁ and FVC, adjusted for age and height, were computed from Crapo's equations¹⁷. For blacks, equation-derived predictions were multiplied by 0.88¹⁸.

Definitions of COPD

Three definitions were used to identify subjects with COPD: symptoms of chronic bronchitis, emphysema diagnosed by a physician and reported by the subject, and spirometrically detected COPD. Chronic bronchitis was defined by persistent cough and production of phlegm on most days for at least three consecutive months of the year for two or more years. Emphysema was defined by a positive response to three questions: Have you ever had emphysema? Do you still have it? and Was it confirmed by a doctor? Spirometrically detected COPD was defined by a measured FEV₁ value 65 percent of the predicted value in the presence of a normal FVC value ( 80 percent of the predicted value). The cutoff point chosen for an abnormal FEV₁ corresponded to the fifth percentile of the distribution in the cohort, as recommended elsewhere¹⁸. A fourth, composite group comprised subjects who met any of the three case definitions.

For each of the four groups a comparison group was selected, composed of subjects in the cohort who had ever smoked. For the chronic-bronchitis group, the comparison group included subjects with no persistent cough or production of phlegm. For the emphysema group, the comparison group included subjects who responded negatively to the question "Have you ever had emphysema?" and who had normal FEV₁/FVC values ( 70 percent). For the group with spirometrically detected COPD, the comparison group included subjects with measured FEV₁ values 80 percent of the predicted value. Finally, for the composite group (those with COPD according to any of the three case definitions), the comparison group included subjects who were defined as not having COPD according to any of the three definitions.

Statistical Analysis

Because COPD is related to cigarette smoking, these analyses focused on the 9178 subjects who had ever smoked. To improve the validity of the dietary data, we excluded subjects from the study if their reported daily energy intake seemed implausible (below the 1st or above the 99th percentile of the sex-specific distribution in the entire cohort). After the exclusion of these subjects, there remained 8960 subjects who had ever smoked. The analyses involving spirometric measurements were limited to 7902 subjects for whom reproducible spirograms had been obtained.

The relation between dietary intake of n-3 fatty acids (the intake of eicosapentaenoic acid and docosahexaenoic acid combined) and COPD in each of the four groups of subjects with COPD was first studied according to quartiles of intake. Crude odds ratios were computed, with the lowest quartile used as the reference group. Multiple logistic-regression models were used to adjust the odds ratios for energy intake and potentially confounding variables, including pack-years of cigarette smoking, age, race, sex, height, weight, and level of education. The models for spirometrically detected COPD did not include age, race, sex, and height as covariates, because adjustment for these variables was made in computing the predicted FEV₁ and FVC values^17,18. The results of the center-specific analyses were generally consistent with those of the main analysis, but there were fewer subjects and therefore the estimates were less stable. Also, modeling of interaction terms between quartiles of n-3 fatty acid intake and site revealed no statistical evidence of interaction. Linear trends were examined by modeling n-3 fatty acid intake as a continuous variable. The possibility of multiplicative interactions of race and sex with fatty acid intake was examined in several models; none were detected. Finally, sex- and race-specific multiple linear regression analysis was used to evaluate the association between fatty acid intake and spirometric measurements (FEV₁, FVC, and FEV₁/FVC). Computations were performed with SAS software¹⁹. All reported P values are two-tailed.

Results

Of the 8960 subjects who had ever smoked (Table 1), 55 percent were former smokers and 45 percent were current smokers. Symptoms compatible with chronic bronchitis were reported by 667 subjects (7 percent). Two percent (185 subjects) reported having been given a diagnosis of emphysema, and 2 percent (197 subjects) met the spirometry-based definition of COPD. Although the three groups of subjects with COPD overlapped only partially (e.g., 26 subjects were included in both the emphysema group and the group with spirometrically detected COPD, whereas 39 were included in both the chronic-bronchitis group and the group with spirometrically detected COPD), the subjects with chronic bronchitis and those who reported having emphysema both had evidence of airway obstruction. For example, the mean FEV₁, expressed as a percentage of the predicted value, was 61 percent among the subjects with emphysema and 77 percent among the subjects with chronic bronchitis; among the 4313 subjects classified as not having COPD according to any of the three definitions, the mean FEV₁ was 100 percent.

View this table: [in this window] [in a new window]   Table 1. Characteristics of 8960 Subjects Who Had Ever Smoked Cigarettes.

 
The average reported consumption of any type of fish was only about two servings per week (Table 2). Ten percent of the subjects reported almost never consuming fish. There was a very close correlation between the intake of eicosapentaenoic acid and that of docosahexaenoic acid (Pearson correlation coefficient, 0.97) and between the combined intake of these fatty acids and fish consumption (correlation coefficient, 0.96). Intake of n-3 fatty acids correlated only weakly with indexes of lifetime smoking, such as the number of pack-years of cigarette smoking or the average number of cigarettes smoked per day (correlation coefficient, -0.06 for both).

View this table: [in this window] [in a new window]   Table 2. Dietary Intake of Fish and Selected n-3 Polyunsaturated Fatty Acids by 8960 Subjects Who Had Ever Smoked Cigarettes.

 
For all three case definitions, COPD was strongly and inversely related to the intake of n-3 fatty acids in a dose-response fashion (Table 3). The crude odds ratios for the highest quartile of intake as compared with the lowest quartile ranged from 0.34 (95 percent confidence interval, 0.21 to 0.54) for the emphysema group to 0.59 (95 percent confidence interval, 0.47 to 0.75) for the chronic-bronchitis group. Multivariate adjustment did not alter the crude estimates materially (Table 3), nor did further adjustment for alcohol consumption (data not shown). The results of tests for linear trend using the continuous variable for intake were all statistically significant (P<0.001 for chronic bronchitis, P = 0.003 for emphysema, P = 0.007 for spirometrically detected COPD, and P<0.001 for COPD by any definition). The results were similar in analyses stratified according to current and former smoking status.

View this table: [in this window] [in a new window]   Table 3. Relation between COPD and Dietary Intake of n-3 Polyunsaturated Fatty Acids in Subjects Who Had Ever Smoked Cigarettes.

 
Fish consumption had a similarly inverse relation to smoking-related COPD (Table 4). The highest quartile, in which the subjects had a median intake of four servings of fish per week, had an adjusted odds ratio of COPD about half that of the lowest quartile, whichever definition of COPD was used (all P<0.005 for linear trend).

View this table: [in this window] [in a new window]   Table 4. Adjusted Odds Ratios for COPD in Subjects Who Had Ever Smoked Cigarettes, According to Quartile of Fish Consumption.

 
Since COPD reflects the most severe impairment of lung function, we evaluated further the relation of n-3 fatty acid intake and fish consumption to continuous measurements of lung function. Among the 6228 white subjects who had ever smoked and had reproducible spirograms, higher intake of n-3 fatty acids and fish predicted better lung function in both men and women (Table 5). For the 1674 black subjects who had ever smoked, the associations were not consistently positive, and none were statistically significant (data not shown).

View this table: [in this window] [in a new window]   Table 5. Differences in Lung Function Predicted among White Subjects in Association with Specified Increments in Intake of n-3 Polyunsaturated Fatty Acids or Fish.

 
There were too few cases of COPD to evaluate among the 6546 subjects who had never smoked. Only 13 of these subjects reported a diagnosis of emphysema, and only 20 met the definition of spirometrically detected COPD. The predictions from linear regression models for those of either race who had never smoked were, for the most part, not statistically significant. The results derived from linear models for the 4179 white subjects who had never smoked are shown in Table 5.

Discussion

Although this study does not establish that the dietary intake of n-3 fatty acids or fish protects against smoking-related COPD, that hypothesis is biologically plausible. The pathogenesis of chronic bronchitis, emphysema, and deterioration of lung function in smokers is likely to involve inflammatory processes^9,10,20. Cigarette smoking is associated with an accumulation of neutrophils in the lung,²¹ increased leukocyte production of leukotriene B₄,²² a potent inflammatory metabolite of arachidonic acid, and enhanced release of reactive oxygen metabolites (e.g., superoxide anions) by alveolar macrophages²³. Both leukotriene B₄ and reactive oxygen metabolites may stimulate mucus secretion in the airways,¹⁰ and the latter have also been implicated in the proteinase-antiproteinase theory of emphysema²⁴.

Supplementing the diet with n-3 fatty acids interferes with all these pathogenic mechanisms, because n-3 fatty acids reduce the chemotactic responsiveness of neutrophils, inhibit the production of leukotriene B₄ from arachidonic acid in leukocytes, and decrease the production of superoxide anions in leukocytes^2,3. These fatty acids also decrease the production of other putative mediators of pulmonary inflammation, including platelet-activating factor, interleukin-1, and tumor necrosis factor^4,5. Although most of the antiinflammatory effects of n-3 fatty acids have been demonstrated with dietary supplements that provide doses much higher than the average intake in this study, very small increments in intake may have health benefits, possibly the result of a cumulative effect¹.

Little information is available about a potential protective effect of dietary n-3 fatty acids or fish consumption against COPD. Data from the Second National Health and Nutrition Examination Survey suggested an inverse relation between fish consumption and current bronchitis²⁵. In a study of telephone workers in the United States and Japan, societies with low and high fish consumption, respectively,²⁶ the Japanese workers had less evidence of chronic bronchitis and somewhat higher mean FEV₁ values than their American counterparts with equivalent levels of cigarette smoking²⁷. Mortality from COPD is low in Japan despite a high prevalence of cigarette smoking²⁸. Of course, numerous factors other than fish consumption could account for these findings.

We are uncertain why n-3 fatty acid intake was not associated with continuous measurements of lung function in the black subjects we studied who had ever smoked. Since the number of blacks was smaller, the statistical power of our study to detect a weak association was limited. Another explanation may be the somewhat lower reproducibility of the dietary data among the black subjects in the study (unpublished data). In the logistic-regression models, however, there was no statistical evidence of a differential effect according to race.

Several limitations of this cross-sectional analysis should be noted. First, fish consumption may be a surrogate for some other protective factor against COPD among the subjects who have ever smoked, or COPD may have changed their dietary habits and reduced their fish consumption. Spurious cross-sectional associations may also have been observed if the relation of fish consumption to COPD was different among the study subjects as compared with either nonparticipants who smoked or those who died of COPD at a young age. Second, dietary intake is hard to measure accurately, although estimates of n-3 fatty acid intake based on similar questionnaires correlate with concentrations of these fatty acids in plasma phospholipids and adipose tissue^29,30. Finally, confounding by cigarette smoking or other variables may not have been eliminated through statistical modeling.

The findings reported here suggest a role for dietary intake of n-3 fatty acids and fish consumption as protective factors against COPD and deterioration of lung function among cigarette smokers.

Supported under contracts (NO1-HC-55015, NO1-HC-55016, NO1-HC-55018, NO1-HC-55019, NO1-HC-55020, NO1-HC-55021, and NO1-HC-55022) with the National Heart, Lung, and Blood Institute.

We are indebted to Donna Neal and Patricia Smith, of the ARIC Project Office; to Kay Paton, Jeannette Bensen, Delilah Posey, Amy Haire, Carol Summers, Catherine Burke, Deanna Horwitz, and Carmen Woody, of the Forsyth County Field Center; to Bobbie Alliston, Jane Johnson, Clinton Smith, and Robert Smith, of the Jackson Field Center; to Elizabeth Justiniano, John O'Brien, Leone Reed, and Shirley Van Pilsum, of the Minneapolis Field Center; to Carol Christman, Sonny Harrell, Joel Hill, and Joan Nelling, of the Washington County Field Center; to Valerie Stinson, Pam Pfile, Hoang Pham, and Teri Trevino, of the Central Hemostasis Laboratory; to Louis Wijnberg, of the Collaborative Studies Coordinating Center; and to Laura Kemmis and Mike Wickersheimer for assistance in the preparation of the manuscript.

Source Information

From the Division of Epidemiology, School of Public Health, University of Minnesota, Minneapolis (E.S., A.R.F., S.L.M.); the Johns Hopkins School of Hygiene and Public Health, Baltimore (M.S.T., G.W.C., M.S.); the Environmental Epidemiology Service, Istituto Nazionale per la Ricerca sul Cancro, Genoa, Italy (V.G.); the Division of Epidemiology and Clinical Applications, National Heart, Lung, and Blood Institute, Bethesda, Md. (M.W.H., P.D.S.); and the Collaborative Studies Coordinating Center, University of North Carolina, Chapel Hill (W.-J.K.). Presented in part at a meeting of the Society for Epidemiologic Research, Minneapolis, June 10-12, 1992.

Address reprint requests to Dr. Shahar at the Division of Epidemiology, School of Public Health, University of Minnesota, 1300 S. Second St., Suite 300, Minneapolis, MN 55454-1015.

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