Background It has been hypothesized that a diet containing n-3fatty acids from fish reduces the risk of coronary heart disease,but few large epidemiologic studies have examined this question.
Methods In 1986, 44,895 male health professionals, 40 to 75years of age, who were free of known cardiovascular diseasecompleted detailed and validated dietary questionnaires as partof the Health Professionals Follow-up Study. During six yearsof follow-up, we documented 1543 coronary events in this group:264 deaths from coronary disease, 547 nonfatal myocardial infarctions,and 732 coronary-artery bypass or angioplasty procedures.
Results After controlling for age and several coronary riskfactors, we observed no significant associations between dietaryintake of n-3 fatty acids or fish intake and the risk of coronarydisease. For men in the top fifth of the group in terms of intakeof n-3 fatty acids (median, 0.58 g per day), the multivariaterelative risk of coronary heart disease was 1.12 (95 percentconfidence interval, 0.96 to 1.31), as compared with the menin the bottom fifth (median, 0.07 g per day). For men who consumedsix or more servings of fish per week, as compared with thosewho consumed one serving per month or less, the multivariaterelative risk of coronary disease was 1.14 (95 percent confidenceinterval, 0.86 to 1.51). The risk of death due to coronary diseaseamong men who ate any amount of fish, as compared with thosewho ate no fish, was 0.74 (95 percent confidence interval, 0.44to 1.23), but the risk did not decrease as fish consumptionincreased.
Conclusions Although the possibility of residual confoundingby unmeasured factors cannot be entirely excluded, these datasuggest that increasing fish intake from one to two servingsper week to five to six servings per week does not substantiallyreduce the risk of coronary heart disease among men who areinitially free of cardiovascular disease.
The low rates of coronary heart disease in Japan and Greenland,where fish is an important component of the diet, suggest thatthe consumption of fish may be protective against such disease.1,2,3Possible mechanisms of this effect include the ability of long-chainn-3 polyunsaturated fatty acids, which are abundant in fish,to decrease plasma levels of very-low-density lipoprotein cholesterol,increase vasodilatation, and reduce platelet aggregation.4,5An inverse association between fish intake and the risk of deathfrom coronary disease has also been found in prospective studiesin the Netherlands,6 Sweden,7 and the United States,8,9 butnot in similar investigations in Norway,10 among Japanese menin Hawaii,11 or among U.S. physicians.12 Evidence concerningthe incidence of coronary heart disease is sparse because moststudies have examined only deaths. The intake of n-3 fatty acidswas assessed in only two studies,9,12 and the validity of reportedfish consumption or calculated n-3 fatty-acid intake was notevaluated in previous investigations.
Methods
The Health Professionals Follow-Up Study
The Health Professionals Follow-up Study began in 1986, when51,529 male health professionals 40 to 75 years of age completeda detailed food-frequency questionnaire and provided informationabout their medical history, risk factors for heart disease,and dietary changes during the past 10 years.13 Follow-up questionnaireswere sent in 1988, 1990, and 1992 in order to determine theincidence of coronary end points. We excluded from our analysis1595 men who did not satisfy the a priori criteria for dailycalorie intake (between 800 and 4200 kcal) and completenessof data on food consumption (fewer than 70 blanks out of 131listed food items). In addition, we excluded 5039 men who reportedon the 1986 questionnaire that they had previously been givena diagnosis of myocardial infarction, angina, stroke, transientischemic attack, or peripheral arterial disease or had undergonecoronary artery surgery. We followed the 44,895 remaining menwho were eligible in 1986 for the occurrence of coronary heartdisease during the subsequent six years. Follow-up was completefor more than 94 percent of the eligible subjects in each two-yearfollow-up cycle. Nonresponding participants were assumed tobe alive if they were not listed in the National Death Index.
Dietary Assessment
The 1986 questionnaire included items regarding the subject'saverage frequency of consumption during the previous year ofspecified portions of 131 foods. Four fish items were included:dark-meat fish such as bluefish (1.37 g of n-3 fatty acids perportion); canned tuna (0.69 g); other fish (0.17 g); and shrimp,lobster, or scallops (0.46 g). We calculated the average dailyintake during that year of marine n-3 fatty acids as the sumof the daily consumption of each type of fish multiplied bythe n-3 content of the specified portion,14 and we adjustedthis and other nutrient values for total energy intake by meansof regression analysis.15
A question about the use of fish-oil supplements was includedin the 1988 follow-up questionnaire; only 4 percent of the menreported using such supplements. The validity of the food-frequencyquestionnaire was assessed in a random sample of 127 men livingin the Boston area, by comparing their calculated intake ofn-3 fatty acids from fish with the concentrations of the fatsin their adipose tissue.16,17,18 The Spearman correlation coefficientfor the correlation of the intake of eicosapentaenoic acid,adjusted for energy intake, and the percentage of eicosapentaenoicacid in adipose tissue was 0.49 (P<0.001); the mean percentageof eicosapentaenoic acid in adipose tissue was 0.04 percentfor men in the bottom fifth of the sample in terms of theircalculated, energy-adjusted intake of eicosapentaenoic acid,and it was 0.11 for men in the top fifth. In addition, we comparedfish intake as reported in the questionnaire with two one-weekdietary records obtained approximately six months apart.18 Themean fish intake (calculated as the sum of the four fish items)was 3.7 servings per week according to the questionnaire and3.6 servings per week according to the dietary records (Spearmancorrelation coefficient, 0.61; P<0.001). Mean fish consumptionin the dietary records was 1.2 servings per week for the menin the lowest intake category, according to their responsesto the questionnaire, and 5.8 servings per week in the highestintake category.
Ascertainment of End Points
The ascertainment of end points has been described in detailpreviously.19 Briefly, fatal coronary disease (including suddendeath), nonfatal myocardial infarction, coronary-artery bypassgrafting, or angioplasty occurring between the return of thebase-line questionnaire and January 31, 1992, were consideredas end points. Participants who reported a myocardial infarctionon a follow-up questionnaire were asked for permission to reviewtheir medical records. Nonfatal myocardial infarction was consideredconfirmed if the World Health Organization criteria were met20;specifically, this diagnosis required symptoms plus either typicalelectrocardiographic changes or elevated cardiac-enzyme levels.
To validate the report of coronary-artery bypass grafting orangioplasty, we obtained medical records for a sample of 102participants who reported undergoing those procedures. Reportswere confirmed for 98 men (96 percent), and we therefore consideredthe subjects' reports to be sufficiently accurate.
Deaths were reported by family members, coworkers, or postalauthorities or were identified through the National Death Index.Fatal coronary disease was confirmed by reviews of medical recordsor autopsy reports. Fatal coronary disease was also consideredconfirmed if it was listed as the underlying cause of deathon the death certificate and if a diagnosis of coronary diseasewas confirmed by other sources. Sudden death, defined as deathwithin one hour of the onset of symptoms in men with no previousserious illness or plausible cause of death other than coronaryheart disease, was included in our analysis as fatal coronarydisease. Ten men with nonfatal end points (three with coronary-arterybypass procedures and seven with myocardial infarctions) diedduring the follow-up period; they were included in the analysesof the specific nonfatal end points but were counted only oncein analyses of the total numbers with myocardial infarctionor the total with coronary disease. The physicians who reviewedthe subjects' medical records were blinded to the dietary-intakedata.
Statistical Analysis
Participants contributed follow-up time from the date of returnof the 1986 questionnaire up to the date of occurrence of anend point, the date of death, or January 31, 1992. Relativerisks were calculated by dividing the incidence of coronaryheart disease among men in each of five roughly equal quintilegroups (defined by n-3 fatty-acid intake) by the incidence amongmen in the lowest fifth of the sample in terms of intake. Themen were classified in six groups in terms of fish intake, rangingfrom those who never ate fish or consumed it less than onceper month to those who consumed six or more servings per week.We adjusted the relative risks for age (in five-year age groups)using the Mantel–Haenszel method.21 The Mantel extensiontest22 was used to test for linear trend. To adjust for otherrisk factors, we used proportional-hazards models.23 In multivariatemodels, we tested for significant trends by assigning each participantthe median value of his category and modeling this as a continuousvariable. All the reported P values are two-sided.
Results
During 242,029 person-years of follow-up, we documented 1543coronary events (264 deaths due to coronary disease, 547 nonfatalmyocardial infarctions, and 732 coronary-artery bypass or angioplastyprocedures).
Intake of n-3 fatty acids from fish was associated, either inverselyor directly, with a variety of dietary and nondietary risk factors(Table 1). We therefore analyzed the relation between n-3 fattyacids and the risk of coronary heart disease with and withoutadjustment for these variables.
Table 1. Relation of the Intake of n23 Fatty Acids from Fish to Selected Risk Factors for Coronary Heart Disease (CHD) at Base Line.
In age-adjusted analyses, the intake of n-3 fatty acids fromfish was directly associated with the overall risk of coronaryevents; the relative risk for the men with the highest intake,as compared with those with the lowest, was 1.19 (95 percentconfidence interval, 1.02 to 1.39; P for trend, 0.03) (Table 2).This positive association was mostly due to an increasedfrequency of bypass grafting among men with a higher intakeof n-3 fatty acids from fish. The risk of sudden death (89 cases,data not shown) was also found not to be inversely associatedwith the intake of n-3 fatty acids; the relative risk for themen with the highest intake, as compared with those with thelowest intake, was 1.10 (95 percent confidence interval, 0.56to 2.13). After adjustment for coronary risk factors, the associationbetween n-3 fatty-acid intake and the risk of coronary diseasewas attenuated (Table 2). However, further adjustment for physical-activitylevel and intake of vitamin E and carotene strengthened theassociation; the relative risk for the men with the highestintake of n-3 fatty acids, as compared with those with the lowestintake, was 1.22 (95 percent confidence interval, 1.03 to 1.44).
Table 2. Relative Risk of Coronary Heart Disease (CHD) According to Dietary Intake of n–3 Fatty Acids.
To reduce the possibility of residual confounding by the men'sperceptions of their high risk of coronary events, we conductedtwo separate analyses, one after excluding the 12,614 men withdiabetes, hypertension, or hyperlipidemia, and the other afterexcluding the 17,339 men who knew their serum cholesterol levelsat base line. The results of the two analyses were similar:the multivariate relative risks of coronary heart disease forthe men with the highest intake of n-3 fatty acids as comparedwith those with the lowest intake were 1.12 (95 percent confidenceinterval, 0.90 to 1.40) and 1.20 (95 percent confidence interval,0.95 to 1.52), respectively. Also, we reduced the possibilityof confounding by unreported coronary disease at base line byexcluding events that occurred during the first four years offollow-up. We still found no inverse association between n-3fatty-acid intake and the risk of coronary disease; the relativerisk for the highest intake group as compared with the lowestwas 1.29 (95 percent confidence interval, 0.99 to 1.68).
The relation of coronary risk to fish intake was similar tothat for intake of n-3 fatty acids. The relative risk of anycoronary event for the men who consumed the most fish, as comparedwith those who consumed the least, was 1.16 (95 percent confidenceinterval, 0.89 to 1.53) in the age-adjusted analyses (Table 3)and 1.14 (95 percent confidence interval, 0.86 to 1.51) afteradjustment for coronary risk factors (Table 3). The slightlyhigher risk of coronary disease among the men with the highestfish intake was once again due to an excess of coronary bypassgrafting and angioplasty procedures. As was the case with n-3fatty acids, only slight differences in these estimates werecaused by further adjustment for the level of physical activityand intake of vitamin E or carotene; by the exclusion of menwith a history of diabetes, hypertension, or high cholesterollevels or those who knew their base-line serum cholesterol levels;or by the exclusion of coronary events that occurred duringthe first four years of follow-up. In none of these analyseswas there a significant inverse relation between fish intakeand the risk of coronary heart disease. In analyses accordingto type of fish, the relative risk for the men in the highestintake group (three or more servings per week) as compared withthose in the lowest intake group (less than one serving permonth) was 1.18 (95 percent confidence interval, 0.95 to 1.48)for dark-meat fish and 0.92 (95 percent confidence interval,0.76 to 1.10) for other fish.
Table 3. Relative Risk of Coronary Heart Disease (CHD) According to Dietary Fish Intake.
The results of a secondary-prevention trial suggested that fishintake may reduce mortality due to coronary disease, but notthe incidence of myocardial infarction.24 We found the highestrisk of fatal coronary disease among men who reported no fishconsumption, but the risk did not decrease with increasing fishintake. The relative risk for men who ate any amount of fish,as compared with men who ate no fish, was 0.74 (95 percent confidenceinterval, 0.44 to 1.23) after adjustment for established riskfactors (as in the multivariate model in Table 3) and 0.77 (95percent confidence interval, 0.46 to 1.28) after further adjustmentfor physical-activity level and the intake of vitamin E andbeta carotene.
To increase the probability of detecting an effect of fish intakethat may occur only after several years of high levels of consumption,we repeated the analyses, including only the 14,230 men whoreported at base line that there had been no change in theirfish intake during the previous 10 years. There were 506 coronaryevents in this group. In these analyses the relative risk forthe men with the highest intake of n-3 fatty acids from fish,as compared with those with the lowest intake, after adjustmentfor coronary risk factors (as in the multivariate model in Table 2),was 1.04 (95 percent confidence interval, 0.75 to 1.44).The comparable figure for fish intake was 1.25 (95 percent confidenceinterval, 0.71 to 2.19).
The use of fish-oil supplements (reported by 4 percent of thecohort in 1988) was not significantly associated with risk.The multivariate relative risk for users as compared with nonusersof such supplements was 0.96 (95 percent confidence interval,0.68 to 1.35). There was also no significant inverse associationbetween the intake of fish or n-3 fatty acids from fish andthe risk of myocardial infarction in any of the subgroups definedaccording to risk factors for coronary disease.
Discussion
In this large prospective cohort study, we found no evidenceof an association between the intake of either marine n-3 fattyacids or fish and the risk of coronary heart disease. Potentialbias due to incomplete follow-up was minimized by the high rateof follow-up. We also excluded from the analyses men with previousevidence of cardiovascular disease, who might have changed theirdiets as a consequence of the disease. A previous diagnosisof hypercholesterolemia, diabetes, or hypertension might alsohave caused an increase in fish intake among some participantsin the study, but the exclusion of men with these disordersdid not appreciably change the results.
Errors in assessing fish intake may have weakened the evidenceof a protective effect of marine n-3 fatty acids or fish intakeagainst coronary disease. However, our validation study indicatedthat there was a genuine fourfold difference in fish consumptionbetween men in the lowest and highest intake categories basedon the questionnaire. A related source of potential error isa change in fish intake in the years before the beginning ofthe study. In 1986, two thirds of the men reported having greatlyincreased their intake of fish during the past 10 years. However,the lack of association between fish intake and the risk ofcoronary disease among men who did not change their fish intakeargues against this possibility. Although we cannot excludethe possibility of residual confounding — as might occurif men at higher risk because of unmeasured or imperfectly measuredcovariates ate more fish in an attempt to lower their risk —the small change in the relative-risk estimates caused by adjustmentfor the known risk factors makes such confounding unlikely.
A true protective effect of n-3 fatty acids from fish couldalso have been missed if the fish consumed by the men in ourcohort was mainly fried commercially in cholesterol-raisingfat. However, the consumption of fried food away from home atleast once per week was reported more frequently by men withthe lowest intake of fish (31 percent) than by those with thehighest intake (25 percent); a difference in the same directionwas reported for food fried at home (35 percent vs. 20 percent).These results, which are consistent with the overall healthierlifestyle of the men with higher fish intake, make increasedconsumption of fried food an unlikely explanation of our findings.In addition, no inverse relation was observed between the riskof coronary disease and the intake of dark-meat fish, whichis usually not fried.
In a prospective investigation of the risk of coronary diseaseamong 852 middle-aged Dutch men who were followed for 20 years,men who consumed more than 30 g of fish per day at base linehad only about half the risk of fatal coronary disease of menwho consumed none.6 Similar findings were reported among 1931men in the Western Electric Study who were followed for 25 years.8Inverse relations between fish intake and mortality from coronarydisease among men and women were also observed in two prospectivestudies7,9 and a case–control study.25 However, no associationbetween fish intake and deaths due to coronary disease was observedin a large study of Norwegian men10 or in a study of Japanesemen living in Hawaii11; both cohorts — like that in ourstudy — were characterized by high fish intake. In a preliminaryreport from the Physicians' Health Study, no association betweenintake of either fish or n-3 fatty acids and the incidence ofcoronary disease was observed.12
Levels of long-chain n-3 fatty acids in adipose tissue or bloodhave been found to be inversely associated with the risk orseverity of coronary disease in some investigations,27,28,29but not all.26,30,31 An important limitation of those studies,however, is the lack of control for other dietary risk factorsfor coronary disease.
A wide variety of presumably favorable physiologic effects areassociated with n-3 fatty acids: a reduction in very-low-densitylipoprotein cholesterol levels; inhibition of thromboxane productionand an increase in prostacyclin synthesis, with a resultingreduction in the likelihood of thrombosis; a reduction in bloodviscosity; and a reduced risk of cardiac arrhythmias.4,5 However,these cardiovascular effects occur at doses of 3 g or more ofn-3 fatty acids per day, amounts several times higher than thoseconsumed by men in the highest intake categories in epidemiologicstudies. Thus, it seems unlikely that the reduction in mortalitydue to coronary disease in some of these studies is caused bythe known cardiovascular effects of n-3 fatty acids.
Several factors may contribute to the apparently discordantresults of studies of fish consumption and coronary heart disease.A possible explanation is that fish intake is protective invery small amounts (one to two servings per week), perhaps providingan essential minimal amount of long-chain n-3 polyunsaturatedfatty acids or of some still unidentified nutrient. If so, thelack of association in our study could be explained by the smallproportion of men who consumed less than one serving of fishper week. Moreover, dietary fish intake could be unrelated tothe incidence of myocardial infarction but might reduce mortalitydue to coronary disease, perhaps by reducing the risk of fatalarrhythmias. Consistent with this interpretation are the resultsof previous prospective studies, which reported inverse associationsbetween fish intake and mortality due to coronary events,5,6,7,8,9the reduction in mortality but not in the incidence of reinfarctionin the Diet and Reinfarction Trial,24 and the lower (albeitnot significantly lower) risk of death due to coronary diseaseamong men who consumed any amount of fish, as compared withthose who consumed none, in this study.
Finally, other factors may modify the effect of the intake offish or of n-3 fatty acids from fish on the risk of coronarydisease. Linolenic acid can be elongated after ingestion toeicosapentaenoic acid,4 and high intake of this n-3 fatty acidfrom nonmarine sources may compensate for low intake of thelong-chain n-3 fatty acids provided by fish. However, we didnot find an association between fish intake or the intake ofn-3 fatty acids from fish and the incidence of coronary diseaseamong men with low linolenic acid intake. Because n-3 fattyacids may compete with n-6 polyunsaturated fatty acids for conversionto eicosanoids,4 high intake of linoleic acid may dampen thecardiovascular effects of small changes in intake of n-3 fattyacids from fish. In view of changes over time in diet,32 linoleicacid intake is likely to have been higher in our cohort thanamong participants in the studies that support an inverse associationbetween fish intake and mortality due to coronary disease. Wefound no association, however, between the ratio of n-3 to n-6fatty acids and the risk of coronary disease.
We have no convincing explanation for the suggestion of an increasedfrequency of coronary-artery bypass surgery among men with higherfish intake in this study. Perhaps men with higher fish intakeare more health-conscious and more willing to undergo angiographyand elective coronary surgery. We also cannot exclude the possibilitythat coronary surgery is less likely to be performed in geographicareas where fish may be less available. However, relative-riskestimates for coronary-artery bypass grafting or myocardialinfarction did not change materially after adjustment for theregion of residence (data not shown).
Our results suggest that increasing fish intake from one totwo servings per week to five to six servings per week is unlikelyto reduce the risk of coronary disease substantially among menwithout preexisting cardiovascular disease. However, an effectof fish or fish oil at lower or higher levels of intake, oramong persons with dietary habits or other risk factors thatare markedly different from those of the men in our cohort,cannot be excluded by these data.
Supported by grants (HL35464 and CA55075) from the NationalInstitutes of Health.
We are indebted to the participants in the Health ProfessionalsFollow-up Study for their continued cooperation and participation;to Al Wing, Mira Koyfman, Karen Corsano, and Steve Stuart forcomputer assistance; and to Jill Arnold, Betsy Frost-Hawes,Kerry Pillsworth, Mitzi Wolff, Jan Vomacka, and Cindy Dyer fortheir assistance in the compilation of the data and the preparationof the manuscript.
Source Information
From the Departments of Epidemiology (A.A., E.B.R., M.J.S., E.L.G., W.C.W.) and Nutrition (A.A., E.B.R., M.J.S., W.C.W.), Harvard School of Public Health, and the Channing Laboratory, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School (M.J.S., E.L.G., W.C.W.) — all in Boston.
Address reprint requests to Dr. Ascherio at the Department of Nutrition, Harvard School of Public Health, 665 Huntington Ave., Boston, MA 02115.
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