Fish Consumption and the 30-Year Risk of Fatal Myocardial Infarction
Martha L. Daviglus, M.D., Ph.D., Jeremiah Stamler, M.D., Anthony J. Orencia, M.D., Ph.D., Alan R. Dyer, Ph.D., Kiang Liu, Ph.D., Philip Greenland, M.D., Molly K. Walsh, Ph.D., Douglas Morris, M.A., and Richard B. Shekelle, Ph.D.
Background Epidemiologic data on the possible benefit of eatingfish to reduce the risk of coronary heart disease have beeninconsistent. We used data from the Chicago Western ElectricStudy to examine the relation between base-line fish consumptionand the 30-year risk of death from coronary heart disease.
Methods The study participants were 1822 men who were 40 to55 years old and free of cardiovascular disease at base line.Fish consumption, as determined from a detailed dietary history,was stratified (0, 1 to 17, 18 to 34, and >35 g per day).Mortality from coronary heart disease, ascertained from deathcertificates, was classified as death from myocardial infarction(sudden or nonsudden) or death from other coronary causes.
Results During 47,153 person-years of follow-up, there were430 deaths from coronary heart disease; 293 were due to myocardialinfarctions (196 were sudden, 94 were nonsudden, and 3 werenot classifiable). Cox proportional-hazards regression showedthat for men who consumed 35 g or more of fish daily as comparedwith those who consumed none, the relative risks of death fromcoronary heart disease and from sudden or nonsudden myocardialinfarction were 0.62 (95 percent confidence interval, 0.40 to0.94) and 0.56 (95 percent confidence interval, 0.33 to 0.93),respectively, with a graded relation between the relative risksand the strata of fish consumption (P for trend = 0.04 and 0.02,respectively). These findings were accounted for by the relationof fish consumption to nonsudden death from myocardial infarction(relative risk, 0.33; 95 percent confidence interval, 0.12 to0.91; P for trend = 0.007).
Conclusions These data show an inverse association between fishconsumption and death from coronary heart disease, especiallynonsudden death from myocardial infarction.
The idea that the consumption of fish reduces the risk of coronaryheart disease is supported by data from five prospective epidemiologicstudies,1,2,3,4,5,6 two case–control studies,7,8 and onesecondary-prevention trial.9 However, the results of other studiesare apparently inconsistent with these findings.10,11,12,13,14We report on the association between fish consumption and the30-year risk of death from myocardial infarction (sudden ornonsudden), coronary heart disease, cardiovascular diseases,and all causes in the Chicago Western Electric Study.
Methods
Population
The Chicago Western Electric Study comprises 2107 men who were40 to 55 years old in 1957. Participants had been employed forat least two years at the Western Electric Company HawthorneWorks in Chicago and worked in occupations related to the manufactureof telephones. The selection of participants, their demographiccharacteristics, the initial examination, and follow-up procedureshave been described elsewhere.15,16
Dietary Assessment
Dietary information was obtained at the first and second examinations,performed one year apart by two nutritionists using standardquestionnaires.17 The information elicited included a typicalworkday eating pattern, a typical weekend eating pattern, thetime and place of meals, special diets, changes in eating habitsover the previous 20 years, and the consumption (frequency andquantity) of 195 foods during the previous 28 days. Each participant'sdaily intake of nutrients was determined with the use of a food-compositiontable.15,16,17,18,19,20
Food-profile scores, based on information obtained at the secondexamination, indicated the level of consumption of 26 foodsover the previous 28 days: soft drinks; coffee; decaffeinatedcoffee; whole milk; skim milk; cream; cheese; eggs; ice cream;puddings or custards; soups; fish; beef, veal or lamb; pork,ham, or bacon; liver; poultry; mixed dishes; vegetables; breadsor cereals; potatoes; fruits; pastries; sweets or sugars; butter;margarine; and fried foods. Each item was coded on a four-pointscale (0 for none and 1, 2, or 3 for a low, moderate, or highlevel of consumption, respectively). Fish consumption, in 120-gunits per 28 days, was coded as 0 for none, 1 for less than4 units, 2 for 4 to 8 units, and 3 for more than 8 units, correspondingto the following average daily intakes: none, 1 to 17 g, 18to 34 g, or 35 g or more.
Follow-Up
Vital status was determined at the annual examination for thefirst 10 years and by means of mailed questionnaires or telephoneinterviews for the next 15 years; data were available for all2107 men. For the 31st year, data on vital status were obtainedfrom the National Death Index, the Health Care Financing Administration,and surviving participants' responses to questionnaires; datawere available for 2084 of the participants (98.9 percent).The causes of death were determined from death certificatesaccording to codes in the International Classification of Diseases,Eighth Revision (ICD-8).21 For the purposes of the analysespresented here, follow-up began after the second examinationand continued through the 31st anniversary of the date of enrollmentin the study.
End Points
The end points of the study were death from myocardial infarction(ICD-8 code 410), death from coronary heart disease (ICD-8 codes410 through 414), and death from cardiovascular diseases (ICD-8codes 400 through 445). Death from myocardial infarction wasclassified as sudden or not sudden according to the durationof the terminal illness and the place of death, as recordedon the death certificate.
Statistical Analysis
Average base-line (1957 to 1959) dietary intake and cardiovascularrisk factors were calculated for four strata of fish consumption:none, 1 to 17 g, 18 to 34 g, and 35 g or more per day. Age-adjustedmortality rates for fatal myocardial infarction (all deaths,sudden deaths, and nonsudden deaths), all deaths from coronaryheart disease, all deaths from cardiovascular diseases, anddeaths from all causes were calculated per 10,000 person-yearsfor each stratum of fish consumption. Cox proportional-hazardsregression22 was used to estimate the relative risk of deathand 95 percent confidence interval for each stratum of fishconsumption (as compared with no consumption), with adjustmentfor possible confounding variables, and to test for linear trend(for the four strata of fish intake classified as indicatorvariables). This model was also used to test for possible interactions(the statistical power was limited in this regard).
Results
Of the 2107 men in the Chicago Western Electric Study, 62 wereexcluded because they did not attend the second examination.Another 223 men were excluded because of prior coronary heartdisease (74) or missing data on diet (93), education (38), body-massindex (9), serum total cholesterol level (5), smoking status(2), or blood pressure (2), leaving a total of 1822 men.
Characteristics at Base Line
Sixty-eight percent of the study participants were blue-collarworkers; 42 percent were Catholic (Table 1). (Religion was includedas a variable because of religious dietary practices.) On average,the study participants were overweight, with higher-than-desirablelevels of blood pressure, serum cholesterol, and intake of totalfat, saturated fat, and cholesterol. Over half (58 percent)were smokers, with a mean of 18 cigarettes smoked per day. Most(85 percent) were drinkers, who consumed an average of 18.8ml of alcohol per day (4.2 percent of kilocalories).
Table 1. Base-Line Characteristics of 1822 Men According to the Level of Fish Consumption.
Religion and the intake of total energy, ethanol, several macronutrients,and several micronutrients differed significantly among thefour strata (Table 1). For all the nutritional variables exceptcarbohydrate and saturated and monounsaturated fatty acid, thehighest levels were in the men with the highest level of fishconsumption. Age, education, body-mass index, blood pressure,serum cholesterol level, smoking status and number of cigarettessmoked, heart rate, presence or absence of a history of diabetes,and presence or absence of electrocardiographic abnormalitiesdid not differ significantly among the four strata.
30-Year Mortality
During 30 years of follow-up, there were 293 deaths from myocardialinfarction (196 sudden deaths, 94 nonsudden deaths, and 3 thatwere not classifiable), 430 deaths from any type of coronaryheart disease, 573 from any type of cardiovascular disease,and 1042 from any cause. Of the 137 deaths from coronary heartdisease other than myocardial infarction (ICD-8 codes 411 through414), few were sudden.
Fish Consumption and Age-Adjusted Mortality
The age-adjusted rates of death from myocardial infarction,coronary heart disease, cardiovascular diseases, and all causeswere lowest for the men with the highest consumption of fish,with a trend toward lower mortality rates with higher levelsof consumption (Table 2). The men who consumed 35 g or moreof fish per day had a 42 percent lower rate of death from myocardialinfarction than the nonconsumers, a relation accounted for bythe inverse association between nonsudden death from myocardialinfarction and fish consumption. In contrast, there was onlya moderate association between fish intake and sudden deathfrom myocardial infarction.
Table 2. Age-Adjusted Mortality Rate at 30 Years According to Base-Line Fish Consumption.
The trend toward an association between higher fish consumptionand lower rates of death from coronary heart disease, cardiovasculardiseases, and all causes was attributable to the inverse relationbetween fish consumption and death from myocardial infarction,particularly nonsudden death from myocardial infarction. Thus,when deaths from myocardial infarction were subtracted fromdeaths from coronary heart disease, deaths from cardiovasculardiseases, and deaths from all causes, there was no significantgraded relation between the four strata of fish consumptionand death rates; the result was similar with the subtractionof nonsudden deaths from myocardial infarction (Table 2).
Fish Consumption and Multivariate-Adjusted Mortality
Three Cox proportional-hazards models were used to calculatethe relative risks of death for the men in the four strata offish consumption. Model 1 was adjusted only for age. Model 2was adjusted for age; education; religion; systolic blood pressure;serum cholesterol; number of cigarettes smoked per day; body-massindex; presence or absence of diabetes; presence or absenceof electrocardiographic abnormalities; daily intake of energy,ethanol, macronutrients, and cholesterol; and daily intake ofiron, thiamine, riboflavin, niacin, vitamin C, beta carotene,and retinol. Model 3 was adjusted for all the non-nutrient variablesin model 2 plus daily intake of energy, alcohol, and the fourcategories of food correlated with fish consumption and deathfrom myocardial infarction or other coronary causes (cheese,margarine, mixed dishes, and vegetables).
The results were similar with all three models; the data frommodel 2 are shown in Table 3. With adjustment for multiple confounders,a significant inverse relation prevailed between fish consumptionand the risk of a fatal myocardial infarction. For the men whoconsumed 35 g or more of fish daily as compared with the nonconsumers,the relative risk of any death from myocardial infarction was0.56, and the relative risk of nonsudden death from myocardialinfarction was 0.33 (Table 3). The results were similar withthe addition of occupation to model 2 (r = 0.51 for the correlationwith education) and with the use of other definitions of suddendeath (instantaneous, within one hour after the onset of symptoms,and within three hours after the onset of symptoms).
Table 3. Multivariate-Adjusted Relative Risk of Death at 30 Years According to Base-Line Fish Consumption.
The trend toward an inverse relation between fish consumptionand death from coronary causes, cardiovascular causes, and allcauses was accounted for by the data on fatal myocardial infarction— specifically, by the trend toward a lower risk of nonsuddendeath from myocardial infarction with higher fish consumption.No significant relation was found between fish consumption andsudden death from myocardial infarction (Table 3).
In these analyses, serum cholesterol level, blood pressure,number of cigarettes smoked per day, major electrocardiographicabnormalities, age, dietary cholesterol intake, and Keys dietarylipid score23 were also significantly and independently relatedto mortality from myocardial infarction.
In analyses with model 3, which was adjusted for foods (insteadof nutrients) and other variables, fish consumption was significantlyand independently related to the risk of any death from myocardialinfarction and to the risk of nonsudden death from myocardialinfarction. With the variables for consumption of cheese, margarine,mixed dishes, and vegetables included individually in the modeland with all four included together, the relative risks of fatalmyocardial infarction for the men who consumed 35 g or moreof fish per day (as compared with the nonconsumers) ranged from0.53 to 0.58, with 95 percent confidence intervals that excludedvalues of 1.00 or higher (P for linear trend = 0.004 to 0.019).The relative risks of nonsudden death from myocardial infarctionranged from 0.22 to 0.26, with 95 percent confidence intervalsthat excluded values of 1.00 or higher (P for linear trend =0.001 or 0.002).
To assess the stability and independence of the relation betweenfish consumption and the risk of death from myocardial infarction(all deaths and nonsudden deaths), we included an interactionterm in the Cox models for fish consumption and each variablelisted in Table 1, as well as for each of the four food categoriesincluded in model 3. For any death from myocardial infarction,there were significant interactions between fish consumptionand age, major electrocardiographic abnormalities, and consumptionof mixed dishes; for nonsudden death from myocardial infarction,there was a significant interaction between fish consumptionand major electrocardiographic abnormalities. No other interactionterms were statistically significant.
On the basis of these four significant interactions, Cox analyseswere performed with the following dichotomized variables: anage of less than 47 years versus an age of 47 or older, thetwo lower strata of consumption of mixed dishes versus the twohigher strata, and the absence of major electrocardiographicabnormalities versus their presence. Among the 917 men who wereyounger than 47 years at base line, there were 116 deaths frommyocardial infarction and 32 nonsudden deaths from myocardialinfarction, with no significant relation between fish consumptionand either end point (P for trend = 0.678 and 0.628, respectively);among the 905 men who were 47 or older, there were 177 deathsfrom myocardial infarction and 62 nonsudden deaths, with fishconsumption significantly related to both end points (relativerisks for consumers of 35 g or more per day as compared withnonconsumers, 0.41 and 0.15 [P for trend = 0.019 and 0.005],respectively). For low and high levels of consumption of mixeddishes (946 and 875 men, respectively), the relation of fishconsumption to the risk of fatal myocardial infarction was similar:the men who consumed 35 g or more of fish per day (as comparedwith the nonconsumers) had low relative risks (0.42 and 0.58for any death [P for trend = 0.089 and 0.051, respectively]and 0.10 and 0.63 for nonsudden death [P for trend = 0.126 and0.059, respectively]). For the 1761 men without major electrocardiographicabnormalities, there was a graded relation between fish consumptionand the risks of any death from myocardial infarction and nonsuddendeath from myocardial infarction: relative risks for the menin the highest stratum of fish consumption were 0.66 and 0.43(P for trend = 0.093 and 0.028), respectively.
Two other subgroup analyses also yielded significant associationsbetween fish consumption and the risk of fatal myocardial infarction.Among the 1535 men who had no evidence of major organ diseaseat base line, the relative risks for those in the highest stratumof fish consumption were 0.55 for any death and 0.48 for nonsuddendeath (P for trend = 0.035 and 0.030, respectively). Among the1693 men who were classified as light or medium drinkers (consumingless than 50 ml of alcohol per day), the relative risks forthose in the highest stratum of fish consumption were 0.58 and0.31 (P for trend = 0.040 and 0.022), respectively.
Model 2 Cox analyses were repeated for the first, second, andthird decades of follow-up, with 68, 97, and 128 total deathsfrom myocardial infarction and 14, 34, and 46 nonsudden deathsfrom myocardial infarction, respectively. The findings wereconsistent for the three periods. In the highest stratum offish consumption, the relative risks of any death from myocardialinfarction were 0.57, 0.59, and 0.59 (P for trend = 0.563, 0.329,and 0.039) for the first, second, and third decades, respectively;the relative risks of nonsudden death from myocardial infarctionwere 0.16, 0.61, and 0.38, respectively (P for trend = 0.019,0.413, and 0.109). In other words, the relation between fishconsumption and the risk of fatal myocardial infarction persistedthroughout the 30 years of follow-up.
Discussion
We found significant, independent, inverse graded associationsbetween base-line fish consumption and the 30-year risk of deathfrom coronary heart disease, particularly nonsudden death frommyocardial infarction. Differences in death from coronary heartdisease, cardiovascular diseases, and all causes among the fourstrata of fish consumption were attributable to differencesin death from myocardial infarction, especially nonsudden death.Correspondingly, fish consumption was not significantly associatedwith the risk of death from other coronary causes.
The findings from four of seven prospective population studies— the Zutphen and Rotterdam (the Netherlands) studies,the Swedish study, and the study of U.S. physicians (12-yeardata)1,2,4,6 — are broadly concordant with our data showinga significant inverse relation between fish consumption andthe risk of death from coronary heart disease, as are the resultsfrom the two case–control studies7,8 and the one interventiontrial.9 However, in regard to one specific aspect of death fromcoronary heart disease — whether it was sudden or notsudden — our findings apparently differ from those ofthe Physicians' Health Study6 and the Seattle Study.8 Both thesestudies found that higher consumption of fish was associatedwith a lower rate of sudden death, whereas our data indicatea significantly lower rate of nonsudden but not sudden death.
In contrast to these studies, the Bergen (Norway), Hawaiian,and U.S. Health Professionals studies found no relation betweenfish consumption and coronary heart disease.10,11,14 This apparentinconsistency may be due to different methods of assessing dietand categorizing fish consumption; different distributions ofreported fish consumption; differences in study sites and times,with associated dietary differences (e.g., levels of intakeof cholesterol, saturated fats, antioxidants, and fiber) thatmight influence the relation between fish consumption and therisk of coronary heart disease; and different periods of follow-up,ranging from four years to several decades.
In our analyses, we deliberately focused on the end point offatal myocardial infarction (ICD-8 code 410) and its componentsof sudden and nonsudden death, rather than on overall mortalityfrom coronary heart disease. This attention to fatal myocardialinfarction was stimulated by recent research findings. In randomized,controlled trials, the lower rates of death from coronary heartdisease in the intervention groups reflected, in full or inpart, lower rates of death from myocardial infarction.24,25,26Most of the overall decline in the rate of death from coronaryheart disease in the United States in recent decades can beattributed to a decline in the rate of fatal myocardial infarction;there has been a relatively small decrease in the rates of deathfrom other coronary causes (ICD-8 codes 411 through 414).27,28Also, the results of local studies — including studiesof men in Chicago cohorts — indicate that much of thisdecline in the rate of fatal myocardial infarction is due todecreased rates of sudden death from myocardial infarction.29,30,31,32,33,34,35On the basis of these findings, our hypothesis was that fishconsumption is inversely related to sudden death from myocardialinfarction. Thus, our finding that base-line fish consumptionis independently and significantly related to the risk of nonsuddenbut not sudden death from myocardial infarction was unexpected.It will be important to determine whether this finding is reproducible.Two other observational studies recently reported an inverserelation between fish consumption and sudden death,6,8 whichis inconsistent with our results. One problem may be the definitionof sudden death, which may differ among studies.
If fish consumption is indeed protective against fatal myocardialinfarction, data from some of the epidemiologic studies indicatethat the ingestion of small amounts of fish, including mainlylean (nonfatty) fish, provides sufficient protection.1 Couldthe protective effect of consuming small amounts of fish overa period of decades be due to the very small amounts of n-3long-chain polyunsaturated fatty acids ingested?36,37,38,39,40,41,42,43,44,45,46This seems unlikely, since most studies show that effects onplasma lipids and thrombogenic factors require much larger amountsof these fatty acids. Recent findings, however, suggest favorableinfluences on total and intermediate-density lipoprotein triglycerides(but not on cholesterol).47 Could the protective effect be relatedto the influences of these fatty acids on cell membranes?8,48Could the components of fish protein (e.g., particular combinationsof amino acids) be involved?
In conclusion, data from the Chicago Western Electric Studyshow a significant, graded, independent inverse associationbetween base-line fish consumption and the 30-year risk of fatalmyocardial infarction, particularly nonsudden death from myocardialinfarction. This relation accounted for the lower rates of deathfrom all coronary causes, all cardiovascular causes, and allcauses in association with higher fish consumption, which persistedthroughout the 30 years of the study and in analyses adjustedfor potentially confounding demographic, biomedical, and dietaryfactors. Further studies — observational and interventional— are needed to determine whether regular ingestion ofmoderate amounts of fish provides substantial protection againstmyocardial infarction.
Supported in part by grants from the American Heart Association;the National Heart, Lung, and Blood Institute (HL 15174, HL21010, and HL 03387); the Chicago Health Research Foundation;the Otho S. Sprague Foundation; Presbyterian–St. Luke'sHospital; and the Illini Foundation.
We are indebted to the officers, executive leadership, and laborforce of the Western Electric Company, Chicago, whose cooperationmade this study possible; to Oglesby Paul and Mark Lepper, fortheir role in the initiation of the Chicago Western ElectricStudy and in its leadership for many years; to Anne MacMillanShryock, for the collection of the nutritional data; to thephysicians who participated in the annual examinations of thecohort (Maurice Albala, Harry Bliss, Herschel Browns, MarvinColbert, Henry De Young, Peter Economou, Sanford Franzblau,Robert Felix, John Graettinger, Buford Hall, Wallace Kirkland,Joseph Muenster, Hyman Mackler, Adrian Ostfield, Robert Parsons,Charles Perlia, William Phelan, Norman Roberg, Marvin Rosenberg,George Saxton, Armin Schick, John Sharp, Jay Silverman, DonaldTarun, and Walter Wood); to Daniel Garside, for assistance withWestern Electric data files and analyses; to Carol Maliza, forsupervising the 20- and 25-year follow-up surveys; to RonaldPrineas and the members of the Electrocardiographic Coding Laboratory,School of Public Health, University of Minnesota, for the electrocardiographiccoding and quality control; and to David M. Berkson, PatriciaCollette, Mary Newman, Rose Stamler, and Linda Van Horn, Departmentof Preventive Medicine, Northwestern University Medical School,for their contributions to the study.
Source Information
From the Department of Preventive Medicine, Northwestern University Medical School, Chicago (M.L.D., J.S., A.R.D., K.L., P.G., M.K.W., D.M.); the Department of Neurology, Indiana University School of Medicine, Indianapolis (A.J.O.); and the Department of Epidemiology, School of Public Health, University of Texas Health Science Center, Houston (R.B.S.).
Address reprint requests to Dr. Daviglus at the Department of Preventive Medicine, Northwestern University Medical School, 680 North Lake Shore Dr., Suite 1102, Chicago, IL 60611.
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