Charles S. Fuchs, M.D., Meir J. Stampfer, M.D., Graham A. Colditz, M.B., B.S., Edward L. Giovannucci, M.D., JoAnn E. Manson, M.D., Ichiro Kawachi, M.B., Ch.B., David J. Hunter, M.B., B.S., Susan E. Hankinson, R.N., Sc.D., Charles H. Hennekens, M.D., Bernard Rosner, Ph.D., Frank E. Speizer, M.D., and Walter C. Willett, M.D.
Background Studies in men suggest that light-to-moderate alcoholintake is associated with a reduction in overall mortality,due primarily to a reduced risk of coronary heart disease. Amongwomen with similar levels of alcohol consumption, an increasedrisk of breast cancer has been noted that complicates the balanceof risks and benefits.
Methods We conducted a prospective study among 85,709 women,34 to 59 years of age and without a history of myocardial infarction,angina, stroke, or cancer, who completed a dietary questionnairein 1980. During the 12-year follow-up period, 2658 deaths weredocumented.
Results The relative risks of death in drinkers as comparedwith nondrinkers were 0.83 (95 percent confidence interval,0.74 to 0.93) for women who consumed 1.5 to 4.9 g of alcoholper day (one to three drinks per week), 0.88 (95 percent confidenceinterval, 0.80 to 0.98) for those who consumed 5.0 to 29.9 gper day, and 1.19 (95 percent confidence interval, 1.02 to 1.38)for those who consumed 30 g or more per day, after adjustmentfor other predictors of mortality. Light-to-moderate drinking(1.5 to 29.9 g per day) was associated with a decreased riskof death from cardiovascular disease; heavier drinking was associatedwith an increased risk of death from other causes, particularlybreast cancer and cirrhosis. The benefit associated with light-to-moderatedrinking was most apparent among women with risk factors forcoronary heart disease and those 50 years of age or older.
Conclusions Among women, light-to-moderate alcohol consumptionis associated with a reduced mortality rate, but this apparentsurvival benefit appears largely confined to women at greaterrisk for coronary heart disease.
In prospective cohort studies, conducted predominantly amongmen, light-to-moderate drinkers of alcoholic beverages havebeen found to have lower total mortality rates than either nondrinkersor heavier drinkers.1,2,3,4,5,6,7,8,9,10,11,12,13,14 This reducedmortality is due largely to a reduced risk of fatal coronaryheart disease. Studies among women have been fewer, and theresults have been conflicting.3,8,9,11,15,16
Whether the apparent overall benefit of light-to-moderate alcoholintake among men can be extrapolated to women is unclear. Ascompared with men, women have a lower risk of coronary heartdisease,17 attain higher blood alcohol concentrations for agiven amount of alcohol consumed,18 and are more susceptibleto alcoholic liver disease.19,20 Moreover, women who consumemoderate quantities of alcohol have an increased risk of breastcancer.21,22,23
We therefore examined prospectively the relation between alcoholintake and mortality in a large cohort of women. Furthermore,we specifically examined this relation among women at low riskfor coronary heart disease, for whom increased rates of breastcancer and other adverse events may outweigh the reduction incoronary heart disease.
Methods
Study Cohort
The Nurses' Health Study was established in 1976 when 121,700female registered nurses 30 to 55 years of age, residing inthe United States, completed a mailed questionnaire on knownor suspected risk factors for cancer22 and coronary heart disease.24Every two years since then, the participants have been sentfollow-up questionnaires to update information on potentialrisk factors and to identify newly diagnosed cases of cancer,coronary heart disease, and other diseases.
Semiquantitative Food-Frequency Questionnaire
In 1980, 1984, and 1986, the participants were asked to reporttheir average frequency of consumption of specified foods andbeverages during the previous 12 months. In 1980, we also askedwhether consumption of each item had greatly increased or greatlydecreased during the previous 10 years. The reproducibilityand validity of these questionnaires have been documented previously.25,26,27,28,29
Questions about the consumption of beer, wine, and spirits wereincluded as separate items. Total alcohol intake was the sumof the values for all three beverages; a 12-oz (360-ml) canor bottle of beer was assumed to contain 13.2 g of alcohol,a 4-oz (120-ml) glass of wine 10.8 g, and a standard drink ofspirits 15.1 g.30 The Spearman rank-correlation coefficientfor alcohol intake as measured by the questionnaire and as calculatedfrom the dietary records of participants was 0.90.22 Similarly,the correlation between the alcohol consumption reported inresponse to the 1984 questionnaire and that found in the 1980diet records was 0.84.29 In addition, alcohol intake as measuredby each of the methods was correlated with plasma concentrationsof high-density lipoprotein (r = 0.40, P<0.001).22,23,24,25,26,27,28,29
Population for Analysis
The dietary questionnaire was returned by 98,462 nurses in 1980.We excluded from our study women with 10 or more food itemsleft blank (4 percent) or with implausibly high or low scoresfor total food intake (2.7 percent). We also excluded womenwith a history of cancer (except nonmelanoma skin cancer), angina,myocardial infarction, or stroke. Because the group of womenwho now abstain from alcohol may include former heavy drinkersand women who stopped drinking because of illness, we excludedfrom our primary analysis 2957 women who reported no alcoholintake in 1980 but had greatly decreased their alcohol intakein the previous 10 years. This left 85,709 women in the analysis.
Identification of Deaths
Our primary end point was death from any cause. We made systematicsearches of the vital records of the states and the NationalDeath Index to discover deaths among women who did not respondduring each questionnaire cycle. This search was supplementedby reports from family members or from postal authorities. Weestimate that we were able to ascertain more than 98 percentof the deaths in the cohort by these methods.31
A physician, blinded to data on alcohol consumption and otherrisk factors, reviewed death certificates and medical recordsto classify the cause of death according to the InternationalClassification of Diseases, Eighth Revision (ICD-8).32 The followingsubgroups were analyzed: participants whose deaths were dueto any cardiovascular disease (ICD-8 codes 390 to 459 and 795);coronary heart disease (codes 410 to 414); stroke (codes 430to 437); any noncardiovascular cause (all codes except 390 to459 and 795); any cancer (codes 140 to 207); breast cancer (code174); cirrhosis of the liver (code 571); and any injury withan external cause (codes 800 to 999 and all "E" codes), whichincluded accidents and suicides.
Statistical Analysis
In our primary analysis, we used incidence rates with person-yearsof follow-up as the denominators. For each woman, person-yearsof follow-up were counted from the date of return of the 1980questionnaire to May 31, 1992 or, for those who died, untilthe date of death. Because our focus was on mortality, and becausepeople tend to reduce alcohol consumption markedly or to discontinueconsumption after a major illness is diagnosed, levels of alcoholintake reported after 1980 were not taken into considerationin the primary analysis. For all other covariates, person-yearsof follow-up were assigned according to the risk-factor statusreported on the most recently completed questionnaire. Follow-upterminated at the date of death. If no questionnaire was returnedfor a follow-up cycle, the most recently recorded data wereused for the subsequent follow-up period.
We calculated relative risk as the incidence of death amongwomen with a given alcohol intake divided by the correspondingrate among women who did not consume alcohol. Relative riskswere adjusted for age, in five-year categories, and for thehistory and amount of cigarette smoking (participants were groupedinto those who never smoked, those who had formerly smoked,and those who smoked less than 15, 15 to 24, and more than 24cigarettes per day)33; 95 percent confidence intervals werecalculated.34 We used a proportional-hazards model to adjustfor multiple risk factors simultaneously.35 Any curvilinearassociation between alcohol intake and mortality was assessedby including both linear and quadratic terms (average alcoholintake and that value squared) in our model.36 Stratified analyseswere conducted to determine whether the effect of alcohol consumptionwas modified by age or coronary-risk-factor status. In boththese analyses, the value for the relevant variable, age orcoronary-risk-factor status, was updated biennially. Tests forinteraction were performed by entering into the proportional-hazardsmodel cross-product terms for alcohol consumption (as indicatorvariables for each level of intake) and either age or coronary-risk-factorstatus.36
To address the potential misclassification of alcohol intakedue to the passage of time, secondary analyses were performedon the basis of updated measurements of alcohol consumption,although these data were not used in the primary analysis.
Employing a model with separate continuous variables for alcoholintake according to type of beverage — beer, wine, orspirits — we used the Wald test to examine differencesbetween logistic-regression coefficients.36
Results
Among the 85,709 women eligible for analysis, 29.8 percent reportedno alcohol consumption in 1980, and the majority reported consumingonly low-to-moderate amounts (Table 1). Approximately 1 percentof the cohort drank more than 50 g per day. Most base-line characteristicswere distributed similarly among drinkers and nondrinkers, althoughdiabetes mellitus and obesity were more common among nondrinkersand regular aspirin use, oral-contraceptive use, and smokingwere more common among drinkers.
Table 1. Base-Line Characteristics of the Cohort, According to Alcohol Intake.
During the 12 years of follow-up (1,010,209 person-years), 2658of the women died. A total of 503 women died of cardiovasculardisorders; 1495 of any cancer, including 350 of breast cancer;203 of injury from external causes, including accidents andsuicides; 52 of cirrhosis of the liver; and 405 from other causes.
As compared with nondrinkers and heavy drinkers, light-to-moderatedrinkers (1.5 to 29.9 g of alcohol per day) had a significantlylower overall risk of death (Table 2). Even after we controlledfor several known or suspected predictors of mortality, thedata for mortality according to alcohol consumption fitted aU-shaped curve with a nadir at approximately 1.5 to 4.9 g perday (one to three drinks per week). The lower risk associatedwith light drinking was principally due to a lower risk of fatalcardiovascular disease. The higher death rate among women whoconsumed 30 g or more per day was largely due to a higher numberof deaths from noncardiovascular diseases, including breastcancer and cirrhosis. Furthermore, controlling for risk factorsfor breast cancer (age at menarche less than 13 years, one ormore pregnancies, age at first pregnancy less than 22 years,history of benign breast disease, or family history of breastcancer) did not materially affect the association of alcoholconsumption with mortality from all causes.
Table 2. Number of Deaths and Relative Risks of Death According to Cause and Alcohol Intake.
To assess the nonlinear relation between alcohol intake andmortality from all causes, we performed analyses in which alcoholconsumption, measured continuously, was entered into the multivariatemodel as both linear and quadratic terms (average alcohol intakeand that value squared). A negative regression coefficient forthe linear term ( = -1.3 x 10-2, P = 0.02) and a positive coefficientfor the quadratic term ( = 4.9x10-4, P = 0.001) were derived,results consistent with the observed U-shaped relation.
We excluded from our primary analysis former heavy drinkerswho reported current abstinence, but we examined the data onthese women separately. As compared with long-term nondrinkers,these former drinkers had a relative risk of death, after adjustmentfor age and smoking status, of 1.49 (95 percent confidence interval,1.27 to 1.74) as well as a significantly higher risk of deathfrom any cardiovascular cause (relative risk, 2.48; 95 percentconfidence interval, 1.88 to 3.25) and from any noncardiovascularcause (relative risk, 1.24; 95 percent confidence interval,1.02 to 1.50).
Age strongly affected the relation between alcohol intake andmortality from all causes. For women 34 to 39 years of age,the relative risk of death in all categories of drinkers wasslightly but not significantly increased (Table 3). Among womenin this age group who consumed 5.0 g or more of alcohol perday, external causes of injury accounted for 50 percent of thedeaths. In contrast, among women 50 or older, light-to-moderatedrinkers (1.5 to 29.9 g per day) had a significant reductionin mortality from all causes, which appeared to be the resultof a substantially lower risk of fatal cardiovascular disease.Among light-to-moderate drinkers, the relative risk of deathfrom a cardiovascular cause was 0.59 (95 percent confidenceinterval, 0.47 to 0.73) for women 50 years of age or older.To test whether age significantly affected the association betweenalcohol intake and total mortality, we added to the multivariatemodel the cross-product interaction terms of age (measured continuously)and each of the levels of alcohol consumption specified in Table 3.For light-to-moderate drinkers, the decrease in the relativerisk of death with increasing age was at the margin of statisticalsignificance (P for trend = 0.05).
Table 3. Number of Deaths and Relative Risk of Death According to Age and Alcohol Intake.
The apparent benefit associated with light-to-moderate alcoholconsumption was greatest among women with one or more risk factorsfor coronary heart disease (Table 4). Among women reportingat least one coronary risk factor (73.2 percent of the studypopulation in 1980), light-to-moderate drinkers had a significantlylower total mortality (P<0.001). In contrast, among womenwith no coronary risk factors (26.8 percent of the populationin 1980), light-to-moderate drinking was not associated withany appreciable reduction in total mortality (P = 0.70); consumptionof 30 g or more of alcohol per day by these women markedly increasedmortality. This higher total mortality among heavier drinkerswithout coronary risk factors was largely due to a higher riskof death from noncardiovascular disease (relative risk, 2.22;95 percent confidence interval, 1.31 to 3.72), most notablybreast cancer (relative risk, 3.43; 95 percent confidence interval,1.36 to 8.66). The result of a test for interaction betweenthe consumption of 1.5 to 29.9 g of alcohol per day and thepresence or absence of cardiac risk factors was not significantin a multivariate model (P = 0.09), although the relative risksassociated with the consumption of 30 g or more per day diddiffer significantly among women with and without cardiac riskfactors (P = 0.04).
Table 4. Number of Deaths from All Causes and Relative Risk of Death According to Cardiac Risk Status and Alcohol Intake.
To determine whether the interaction between alcohol consumptionand coronary-risk-factor status was independent of age, we thenlimited our analysis to women 50 years of age or older. Amongthese older women, the reduction in mortality associated withlight-to-moderate drinking was again confined to women withone or more coronary risk factors. As was the case when youngerwomen were included, the interaction between the risk of deathassociated with the consumption of 1.5 to 29.9 g of alcoholper day and coronary-risk-factor status was not significant(P = 0.08).
Although we excluded women with serious illnesses at base line,the group of long-term nondrinkers could include women who refrainedfrom drinking because of early symptoms of disease. If so, thehigher mortality among nondrinkers might be due in part to undiagnosed,preexisting disease. Such an effect would account for higherrates of death in the earlier years of follow-up but would beexpected to diminish in later years of observation. To addressthis issue, we repeated our analyses after excluding deathsin the first four years of follow-up (Table 5). With the analysisrestricted to the final eight years of follow-up, a significantU-shaped relation remained between the average alcohol intakereported in 1980 and total mortality (P = 0.002 for the quadraticterm [average alcohol intake]2).
Because people may alter their drinking habits over time, longitudinalstudies that assess alcohol intake only at base line may resultin misclassification. Therefore, we repeated our analyses usingupdated measurements of alcohol consumption obtained in 1984and 1986, and still observed a significant U-shaped relationbetween alcohol consumption and mortality (P<0.001 for thequadratic term [average alcohol intake]2) (Table 5). In performinganalyses in which the data on alcohol intake were updated, weconsidered the possibility that a disproportionate number ofthe women who had recently stopped drinking did so because ofill health, which might have resulted in a misleading elevationof mortality among abstainers. Therefore, we performed furtheranalyses in which women were excluded from follow-up if theyreported nonfatal myocardial infarction, angina, stroke, orcancer during subsequent assessments of alcohol intake. With2043 deaths left in the analysis, we continued to observe asignificant U-shaped relation between alcohol intake and totalmortality (P = 0.001 for the quadratic term [average alcoholintake]2).
We examined separately the association between mortality andalcohol intake according to type of beverage — beer, wine,or spirits. In a regression model controlled for other predictorsof mortality, the associations between alcohol intake (measuredas a continuous variable) from beer, wine, or spirits and therisk of death did not differ significantly, although there wasa nonsignificant trend toward more protection with wine (datanot shown).
Discussion
Our results, from a large prospective study of women, providestrong evidence for a U-shaped relation between alcohol intakeand mortality in women. As compared with abstinence, light-to-moderatealcohol consumption was associated with a significantly reducedrisk of death due largely to a lower risk of fatal cardiovasculardisease. In contrast, heavier drinking was associated with increasedmortality, due largely to an increased risk of death from noncardiovasculardiseases, including breast cancer. In a manner consistent withthese competing effects, the apparent benefit of light-to-moderatealcohol consumption was mainly confined to women at greaterrisk for coronary heart disease, specifically older women andwomen with one or more coronary risk factors.
Bias is unlikely to explain the observed relations. The dietaryquestionnaires reliably measured alcohol intake.29 Moreover,our results remained unchanged even after we accounted for variationsin alcohol consumption over time. The prospective design precludedrecall bias. Differential follow-up is unlikely to have madea material contribution to these findings, since we estimatethat we accurately identified more than 98 percent of the deathsin this cohort.31
We observed a reduction in mortality for light-to-moderate drinkersonly among women 50 years of age or older, although our cohortdid not include women over 70. For women 34 to 39 years of age,we observed elevated risks of death for all levels of alcoholconsumption, but the number of deaths in this subgroup was small.Two previous studies have reported an increased mortality amongyounger drinkers, largely as a result of alcohol-related accidents.11,37Although a recent analysis of British physicians reported lowermortality for moderate drinkers at all ages, the study populationconsisted of men over the age of 50 who were predominantly formeror current smokers.5
The women in the Nurses' Health Study have patterns of alcoholconsumption that are quite similar to those found in a generalsurvey of U.S. women.38 Thus, our results may be applicableto the wider population of women. Since only a small percentageof our cohort consumed more than 50 g of alcohol per day, ourability to examine the health consequences of excessive drinkingis limited.
The relations between alcohol consumption and the risk of deathfrom breast cancer or cardiovascular disease reflect the previouslydescribed association of alcohol with the incidence of theseillnesses.21,22,23,39,40,41,42 In addition, several other diseaseshave been positively linked to alcohol consumption, includingcolorectal cancer, cancers of the upper aerodigestive tract(the oral cavity and esophagus), hemorrhagic stroke, cirrhosisof the liver, accidents, and suicide.2,11,43,44 Our mortalityanalysis does not address nonfatal disease and may thereforebe less useful in addressing causal relations. However, dataon mortality provide one measure of the overall balance of risksand benefits of alcohol consumption.
In conclusion, these findings indicate that for women as a grouplight-to-moderate alcohol consumption confers a significantoverall survival advantage. Among younger women and those withoutrisk factors for coronary heart disease, however, light-to-moderatealcohol consumption is not associated with a reduction in totalmortality and heavier drinking is associated with a substantialincrease in mortality. For older women and women with coronaryrisk factors, light-to-moderate alcohol consumption is associatedwith a reduction in total mortality, although with heavier intakemortality is increased.
Supported by grants (HL 34594 and CA 40356) from the NationalInstitutes of Health and by Faculty Research Awards from theAmerican Cancer Society (FRA-398 to Dr. Colditz and FRA-455to Dr. Hunter).
Source Information
From the Channing Laboratory (C.S.F., M.J.S., G.A.C., E.L.G., J.E.M., I.K., D.J.H., S.E.H., C.H.H., B.R., F.E.S., W.C.W.) and the Division of Preventive Medicine (J.E.M., C.H.H., B.R.), Brigham and Women's Hospital and Harvard Medical School; the Division of Medical Oncology, Dana–Farber Cancer Institute (C.S.F.); and the Departments of Epidemiology (M.J.S., G.A.C., D.J.H., S.E.H., C.H.H., W.C.W.), Nutrition (M.J.S., W.C.W.), Health and Social Behavior (I.K.), and Biostatistics (B.R.), Harvard School of Public Health — all in Boston.
Address reprint requests to Dr. Fuchs at the Dana–Farber Cancer Institute, 44 Binney St., Boston, MA 02115.
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A correction has been published: N Engl J Med 1997;336(7):523.
= -1.3 x 10-2, P = 0.02) and a positive coefficient for the quadratic term (
