Blood Levels of Long-Chain n–3 Fatty Acids and the Risk of Sudden Death
Christine M. Albert, M.D., M.P.H., Hannia Campos, Ph.D., Meir J. Stampfer, M.D., Dr.P.H., Paul M. Ridker, M.D., M.P.H., JoAnn E. Manson, M.D., Dr.P.H., Walter C. Willett, M.D., Dr.P.H., and Jing Ma, M.D., Ph.D.
Background Experimental data suggest that long-chain n–3polyunsaturated fatty acids found in fish have antiarrhythmicproperties, and a randomized trial suggested that dietary supplementsof n–3 fatty acids may reduce the risk of sudden deathamong survivors of myocardial infarction. Whether long-chainn–3 fatty acids are also associated with the risk of suddendeath in those without a history of cardiovascular disease isunknown.
Methods We conducted a prospective, nested case–controlanalysis among apparently healthy men who were followed forup to 17 years in the Physicians' Health Study. The fatty-acidcomposition of previously collected blood was analyzed by gas–liquidchromatography for 94 men in whom sudden death occurred as thefirst manifestation of cardiovascular disease and for 184 controlsmatched with them for age and smoking status.
Results Base-line blood levels of long-chain n–3 fattyacids were inversely related to the risk of sudden death bothbefore adjustment for potential confounders (P for trend = 0.004)and after such adjustment (P for trend = 0.007). As comparedwith men whose blood levels of long-chain n–3 fatty acidswere in the lowest quartile, the relative risk of sudden deathwas significantly lower among men with levels in the third quartile(adjusted relative risk, 0.28; 95 percent confidence interval,0.09 to 0.87) and the fourth quartile (adjusted relative risk,0.19; 95 percent confidence interval, 0.05 to 0.71).
Conclusions The n–3 fatty acids found in fish are stronglyassociated with a reduced risk of sudden death among men withoutevidence of prior cardiovascular disease.
We previously reported that fish consumption was associatedwith a reduced risk of sudden death from cardiac causes, butnot a reduced risk of myocardial infarction, in the Physicians'Health Study.1 It is hypothesized that the long-chain n–3polyunsaturated fatty acids found in fish, primarily eicosapentaenoicacid and docosahexaenoic acid, may be responsible for this association.Experimental data from studies in animals and at the cellularlevel suggest that these n–3 fatty acids have antiarrhythmicproperties,2,3 and a recent randomized trial testing supplementsof these n–3 fatty acids in survivors of myocardial infarctionfound a statistically significant 45 percent reduction in therisk of sudden death, with no effect on nonfatal myocardialinfarction.4 However, prospective data on blood levels of long-chainn–3 fatty acids and sudden death from cardiac causes aresparse, and there have been no randomized trials of the effectsof long-chain n–3 fatty acids in the diet or as supplementsamong persons without a history of cardiovascular disease, whorepresent over half of all cases of sudden death from cardiaccauses.5
To address the hypothesis that the long-chain n–3 fattyacids found in fish are associated with a reduced risk of suddendeath from cardiac causes in those without known cardiovasculardisease, we performed a prospective, nested case–controlanalysis of the fatty-acid composition of whole blood in menwithout a confirmed history of cardiovascular disease who wereparticipants in the Physicians' Health Study.
Methods
Study Population and Collection of Whole-Blood Samples
The methods of the Physicians' Health Study have been describedin detail elsewhere.6,7 Briefly, 22,071 male physicians, whowere 40 to 84 years old in 1982 and had no history of myocardialinfarction, stroke, transient ischemic attacks, or cancer, wereassigned at random according to a two-by-two factorial designto receive aspirin, beta carotene, both active drugs, or bothplacebos. Informed consent was obtained from all subjects, andthe research protocol was approved by the institutional reviewboard at Brigham and Women's Hospital in Boston. At base line,the physicians completed questions on their health status andrisk factors for cardiovascular disease. Dietary intake of fishwas ascertained at 12 months with an abbreviated, semiquantitativefood-frequency questionnaire,8 as described previously.1 Informationon cardiovascular events was updated every six months for thefirst year and annually thereafter with follow-up questionnaires.
Before randomization, which occurred between August 1982 andDecember 1984, potential participants were asked to providebase-line blood samples, which were collected in EDTA and processedfor long-term storage at –80°C. Of the randomizedstudy participants, 14,916 (68 percent) provided base-line bloodsamples. More than 70 percent of these specimens were receivedbetween September and November 1982.
Confirmation of End Points and Selection of Controls
The end point of sudden death from cardiac causes was ascertainedby a two-step process. First, deaths from any cause were generallyreported by postal authorities or next of kin, and an end-pointreview committee confirmed deaths from cardiovascular causesby examining medical records obtained from hospitals and attendingphysicians. A participant's next of kin was interviewed aboutthe circumstances of the death if they were not adequately documentedin the medical record.
Second, to ascertain the specific end point of sudden deathfrom cardiac causes, two cardiologists who were unaware of thesubject's exposure status reviewed medical records and reportsfrom the next of kin of all deaths from cardiovascular causes(excluding strokes). In this second review, sudden death fromcardiac causes was defined as death within one hour after theonset of symptoms or a witnessed cardiac arrest or abrupt collapsethat occurred within one hour after the onset of symptoms andthat resulted in death. For all these deaths, no probable noncardiaccause was suggested by the history or autopsy. To increase specificityfor death from cardiac arrhythmia, we excluded any death forwhich there was evidence of collapse of the circulation (hypotension,exacerbation of congestive heart failure, or altered mentalstatus) before the disappearance of the pulse.9 Unwitnesseddeaths with no information on timing but with an autopsy reportconsistent with death from cardiac arrhythmia (i.e., acute coronarythrombosis or severe coronary artery disease without myocardialnecrosis or other pathological findings to explain death) wereconsidered possible sudden deaths from cardiac causes. Analyseswere performed both including and excluding these deaths, withsimilar results.
Over the 17 years of study follow-up, 201 sudden deaths fromcardiac causes were documented; for 119 of these, an adequatebase-line blood sample was available for analysis. Ninety-fourof these subjects had been free of confirmed cardiovasculardisease before death. Each of these subjects was matched withtwo control subjects, who had also provided an adequate base-lineblood sample and who were alive and remained free of confirmedcardiovascular disease at the time of case ascertainment. Adiagnosis of confirmed cardiovascular disease required a reportof angina with a positive stress-test result or coronary angiographydocumenting clinically significant coronary artery disease,myocardial infarction confirmed according to World Health Organizationcriteria, or stroke confirmed by a typical neurologic deficitlasting longer than 24 hours. Using a risk-set sampling method,we randomly selected controls from among study participantswho met the matching criteria for age (within one year), smokingstatus (formerly, currently, or never), and length of time sincerandomization (in six-month intervals). For four case subjects,only one adequate control could be found.
Laboratory Analysis
Whole blood collected and stored at base line was thawed. Althoughthere are no data on their long-term storage in blood, long-chainn–3 fatty acids have been documented to have high reliabilitycoefficients (0.64 to 0.66) and minimal oxidation in serum samplesstored at –80°C for up to 12 years.10 The fatty acidsfrom whole blood were extracted11,12 and quantitated by gas–liquidchromatography on a fused silica capillary cis–trans column(SP2560, Supelco, Bellefonte, Pa.). We identified the peak retentiontimes from 47 peaks and the percentage of total fatty-acid peakarea representing 95.2 percent of the total peak area by injectingknown standards (NuCheck Prep, Elysian, Minn.), with the useof ChemStation A.08.03 software for analysis (Agilent Technologies).Blood specimens were analyzed in groups of three blinded samples,with the position of the case subject's specimen varied at randomwithin the groups to reduce the possibility of systemic biasand to decrease variability between assays. Coefficients ofvariation for all fatty-acid peaks were measured by analyzingquality-control samples (indistinguishable from other studysamples) randomly distributed throughout the study samples.The major peaks of long-chain n–3 fatty acids includeddocosahexaenoic acid (C22:6n–3), eicosapentaenoic acid(C20:5n–3), and docosapentaenoic acid (C22:5n–3).The coefficients of variation for these major long-chain n–3fatty acids were 7.7, 13.7, and 9.2, respectively. These threepeaks were summed for each participant to arrive at the totallong-chain n–3 fatty acid level.
Statistical Analysis
For base-line risk factors, means or proportions were calculatedfor men who died suddenly (case subjects) and controls. Thesignificance of associations was tested with the chi-squarestatistic for categorical variables and with Student's t-testfor continuous variables. Associations between base-line riskfactors and levels of long-chain n–3 fatty acids, expressedas percentages of total fatty acids, were tested with Student'st-test. The Spearman rank-correlation coefficient was used totest the association between base-line levels of long-chainn–3 fatty acids and fish consumption, measured at 12 months.
Means (expressed as percentage of total fatty acids) for eachfatty-acid peak were calculated for case and control subjects,and the significance of differences was tested by Student'st-test for those that were normally distributed and the Wilcoxonrank-sum test for those that were not normally distributed.To estimate the relative risk of sudden death according to theblood level of long-chain n–3 fatty acids, we first categorizedeach subject according to quartiles determined by the distributionof fatty acid levels in the controls. We then performed logistic-regressionanalysis, conditioned on the matching variables of age and smoking.Adjusted estimates of risk were obtained with multivariate modelsthat also controlled for body-mass index; presence or absenceof a history of diabetes, hypertension, or hyperlipidemia; presenceor absence of a parental history of premature myocardial infarction;alcohol intake; frequency of physical activity; and random assignmentto aspirin and beta carotene or placebo. After the quartileanalysis suggested a linear relation, tests for trend were performedby entering a continuous variable in the conditional-regressionmodel.
In secondary analyses, to assess for confounding by other fattyacids, each fatty-acid group (saturated, monounsaturated, n–6polyunsaturated, and trans unsaturated fatty acids) was enteredseparately according to quartile into the multivariate model,and the change in the parameter estimate for the continuousvalue of long-chain n–3 fatty acid was observed. If achange of more than 15 percent was noted, the fatty acid remainedin this multivariate model. All P values were two-tailed, andall confidence levels were computed at the 95 percent level.
Results
Table 1 shows the base-line characteristics of the 94 subjectsin whom sudden death was the first manifestation of cardiovasculardisease and the 184 matched controls. The mean time from studyenrollment to sudden death was 8.7 years (range, 0.7 to 16.9).In this sample, the men who died suddenly were significantlymore likely to have a history of hypertension, significantlymore likely to have a parental history of early coronary arterydisease (i.e., before 60 years of age), and significantly lesslikely to have been randomly assigned to receive aspirin. Therelation with alcohol intake was U-shaped: men who died suddenlywere more likely to drink less than once a week or daily, andless likely to drink one to six drinks per week. Of the riskfactors listed in Table 1, significantly lower levels of long-chainn–3 fatty acids were found among current smokers thanamong former smokers or those who had never smoked (mean [±SD],4.47±1.31 vs. 5.20±1.30 percent of total fattyacids; P=0.002). In addition, the base-line blood level of long-chainn–3 fatty acids was significantly correlated with fishintake at 12 months (R2=0.24, P=0.001) (data not shown).
Table 1. Base-Line Characteristics of the Study Participants.
The base-line blood levels of each major fatty acid among menwho died suddenly and controls are shown in Table 2. The meanlevel of total long-chain n–3 fatty acids was significantlylower among the men who died suddenly than among the controls(4.82±1.31 vs. 5.24±1.32 percent of total fattyacids, P=0.01). In contrast, the levels of the other fatty acids,including the short-chain n–3 polyunsaturated fatty acid(-linolenic acid), saturated fatty acids, monounsaturated fattyacids, n–6 polyunsaturated fatty acids, and trans unsaturatedfatty acids, did not differ significantly between men who diedsuddenly and control subjects.
Table 2. Base-Line Blood Fatty-Acid Levels of Study Participants Who Died Suddenly from Cardiac Causes without Evidence of Cardiovascular Disease and Controls Matched for Age and Smoking Status.
Table 3 shows the relation of base-line blood levels of long-chainn–3 fatty acids to the risk of sudden death. The levelof long-chain n–3 fatty acids was significantly inverselyrelated to the risk of sudden death in both the analysis adjustedfor age and smoking status (P for trend = 0.004) and the multivariateanalysis (P for trend = 0.007). As compared with the men withlevels of long-chain n–3 fatty acids in the lowest quartile(mean, 3.58 percent of total fatty acids), those with levelsin the highest quartile (mean, 6.87 percent) had a relativerisk of sudden death of 0.19 (95 percent confidence interval,0.05 to 0.71) after known confounders were controlled for (multivariatemodel 1). These results were not materially affected when 15possible sudden deaths were excluded from the analysis (relativerisk for highest vs. lowest quartile, 0.14; 95 percent confidenceinterval, 0.03 to 0.75; P for trend = 0.01).
Table 3. Relative Risk of Sudden Death from Cardiac Causes According to Base-Line Blood Level of Long-Chain n_ Polyunsaturated Fatty Acids.
Since the level of long-chain n–3 fatty acids was significantlyassociated with levels of other fatty acids (inversely withsaturated, trans unsaturated, and monounsaturated fatty acidsand directly with n–6 polyunsaturated fatty acids), eachfatty-acid group was entered in the multivariate model to evaluatethe independent association of long-chain n–3 fatty acidswith the risk of sudden death. Adjustment for saturated andn–6 polyunsaturated fatty acids did not appreciably alterthe association between long-chain n–3 polyunsaturatedfatty acids and the risk of sudden death. Adjustment for monounsaturatedand trans unsaturated fatty acids resulted in a further strengtheningof the relation (Table 3, multivariate model 2). With this adjustment,the relative risk of sudden death among men with levels of long-chainn–3 fatty acids in the highest quartile as compared withthe lowest quartile was 0.10 (95 percent confidence interval,0.02 to 0.48; P for trend = 0.001).
Discussion
In this prospective, nested case–control study of healthymale physicians without evidence of cardiovascular disease atenrollment, the base-line blood level of long-chain n–3fatty acids was inversely associated with the subsequent riskof sudden death, even after known confounders had been controlledfor. The association was linear, with a statistically significantinverse trend across quartiles of levels of long-chain n–3fatty acids. As compared with men with levels of long-chainn–3 fatty acids in the lowest quartile, those with levelsin the highest quartile had an 81 percent lower risk of suddendeath. This relation persisted when blood levels of other fatty-acidgroups were controlled for in the model. Therefore, the associationdid not appear to depend on compensatory changes in the levelsof other fatty acids.
These prospective findings are remarkably similar to those reportedin a population-based case–control study involving 82cases of primary cardiac arrest.13 That study found a stronginverse association between red-cell n–3 fatty-acid compositionat the time of the arrest and the risk of primary cardiac arrestamong subjects with no history of clinically recognized cardiacdisease. Taken together, these data support the hypothesis thatlong-chain n–3 fatty acids are responsible for the observedinverse association between fish consumption and sudden death.1,13There was no evidence of a threshold effect for blood levelsof long-chain n–3 fatty acids, although a threshold effectwas previously reported for fish intake in this cohort.1
Because the present study did not examine other cardiovascularend points or death from other causes, we cannot present directdata on the selectivity of the association between long-chainn–3 fatty acids and sudden death. However, previous studiesof this cohort found no association between plasma levels oflong-chain n–3 fatty acids14 or fish intake1 and the riskof myocardial infarction. In addition, a selective beneficialeffect on the risk of sudden death was found in a randomizedtrial.4 In that trial, men with a history of myocardial infarctionwho were assigned to a fish-oil supplement had a statisticallysignificant 45 percent reduction in the risk of sudden death,which translated into an overall significant reduction in totalmortality. However, there was no reduction in the risk of nonfatalcardiovascular events or in other causes of mortality.
The apparent beneficial effect on the risk of sudden death fromcardiac causes in observational studies and randomized trialscould be due in part to the antiarrhythmic effects of n–3fatty acids, as reported from experimental models.3,15,16 Plausiblemechanisms for these antiarrhythmic effects include modulationof sodium, potassium, and L-type calcium channels2,17,18; inhibitionof thromboxane production19,20; and beneficial effects on heart-ratevariability.21,22 Other indirect effects of long-chain n–3fatty acids include lowering of the nonesterified fatty-acidconcentration in plasma and cell membranes. Nonesterified fattyacids have multiple proarrhythmic properties and have recentlybeen associated with an increased risk of sudden death, butnot of fatal myocardial infarction, among men enrolled in theParis Prospective Study I.23
The limitations of these data merit consideration. First, ouranalyses are based on a single base-line measurement and thereforemay not accurately reflect levels of long-chain n–3 fattyacids over long periods. Furthermore, although the coefficientsof variation were low, misclassification due to laboratory errorcannot be ruled out. It is important to note, however, thatneither of these sources of variability can account for thestrong inverse association we observed between long-chain n–3fatty acid levels and sudden death, since any random misclassificationwould bias results toward the null hypothesis. The use of asingle base-line measurement does, however, limit our abilityto assess accurately the relation between the shorter-chainn–3 fatty acid, -linolenic acid, and sudden death, sincethis fatty acid is largely metabolized,24 and if it is stored,it is elongated to docosahexaenoic acid. Therefore, blood levelsof -linolenic acid would be more dependent on what foods wereeaten recently and less likely to reflect average dietary intake.
The use of whole blood is a possible limitation, because itcombines two different pools of long-chain n–3 fatty acids,the plasma and the stored red-cell pools. Alternatively, thiscomposite measure may be viewed as a strength, since these poolshave different half-lives and provide complementary information.Finally, as with any observational study, the inverse associationbetween blood levels of long-chain n–3 fatty acids andsudden death could be due, at least in part, to residual confoundingby other dietary and lifestyle factors. However, control formajor known confounders and other fatty-acid groups had littleeffect on the estimates of relative risk.
In summary, taken together with previous data from observationalstudies and randomized trials, these prospective data suggestthat the long-chain n–3 fatty acids found in fish mayreduce the risk of sudden death from cardiac causes, even amongmen without a history of cardiovascular disease. Because morethan 50 percent of all sudden deaths from cardiac causes occurin people with no history of cardiac disease,5 preventive effortsmust address this segment of the population to have a substantialeffect on the overall incidence of sudden death from cardiaccauses. If the observed association is causal, increasing theintake of n–3 fatty acids by eating more fish or by takingsupplements is an intervention that could be applied to thissegment of the population at low cost and little risk.
Supported by grants from the National Institutes of Health (CA-34944,CA-40360, HL-26490, and HL-34595) and by a Mentored ClinicalScientist Development Award (1-K08-HL-03783) from the NationalHeart, Lung, and Blood Institute (to Dr. Albert).
Source Information
From the Division of Preventive Medicine (C.M.A., P.M.R., J.E.M.), the Channing Laboratory (M.J.S., J.E.M., W.C.W., J.M.), and the Division of Cardiovascular Medicine (P.M.R.), Department of Medicine, Brigham and Women's Hospital; the Cardiovascular Division, Department of Medicine, Massachusetts General Hospital (C.M.A.); and the Departments of Nutrition (H.C., M.J.S., W.C.W.) and Epidemiology (M.J.S., J.E.M., W.C.W.), Harvard School of Public Health — all in Boston.
Address reprint requests to Dr. Albert at the Division of Preventive Medicine, Brigham and Women's Hospital, 900 Commonwealth Ave. East, Boston, MA 02215-1204, or at calbert{at}partners.org.
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