Francine Grodstein, Sc.D., Meir J. Stampfer, M.D., Graham A. Colditz, M.B., B.S., Walter C. Willett, M.D., JoAnn E. Manson, M.D., Marshall Joffe, M.D., Bernard Rosner, M.D., Charles Fuchs, M.D., Susan E. Hankinson, Sc.D., David J. Hunter, M.B., B.S., Charles H. Hennekens, M.D., and Frank E. Speizer, M.D.
Background Postmenopausal hormone therapy has both benefitsand hazards, including decreased risks of osteoporosis and cardiovasculardisease and an increased risk of breast cancer.
Methods We examined the relation between the use of postmenopausalhormones and mortality among participants in the Nurses' HealthStudy, who were 30 to 55 years of age at base line in 1976.Data were collected by biennial questionnaires beginning in1976 and continuing through 1992. We documented 3637 deathsfrom 1976 to 1994. Each participant who died was matched with10 controls alive at the time of her death. For each death,we defined the subject's hormone status according to the lastbiennial questionnaire before her death or before the diagnosisof the fatal disease; this reduced bias caused by the discontinuationof hormone use between the time of diagnosis of a potentiallyfatal disease and death.
Results After adjustment for confounding variables, currenthormone users had a lower risk of death (relative risk, 0.63;95 percent confidence interval, 0.56 to 0.70) than subjectswho had never taken hormones; however, the apparent benefitdecreased with long-term use (relative risk, 0.80; 0.67 to 0.96,after 10 or more years) because of an increase in mortalityfrom breast cancer among long-term hormone users. Current hormoneusers with coronary risk factors (69 percent of the women) hadthe largest reduction in mortality (relative risk, 0.51; 95percent confidence interval, 0.45 to 0.57), with substantiallyless benefit for those at low risk (13 percent of the women;relative risk, 0.89; 95 percent confidence interval, 0.62 to1.28).
Conclusions On average, mortality among women who use postmenopausalhormones is lower than among nonusers; however, the survivalbenefit diminishes with longer duration of use and is lowerfor women at low risk for coronary disease.
Whether to take postmenopausal hormones is a difficult decision.Hormone use carries many benefits, including decreased risksof osteoporosis1 and cardiovascular disease,2 as well as hazards,especially an increase in the risks of breast and endometrialcancers.1 Observational studies have reported reduced mortalityamong women taking hormones,3,4,5,6,7,8,9 but many of the studieshave had methodologic flaws that limit firm conclusions. Specifically,women for whom estrogens are prescribed are often healthierinitially, and those who continue to take hormones tend to befree of disease (for example, women in whom cancer is diagnosedoften stop taking hormones).8,10,11 Thus, lower mortality amonghormone users may be attributed erroneously to the hormone itself.In addition, studies that combine current and past use intoan "ever" category may underestimate the benefits of postmenopausalhormones, since the decrease in cardiovascular disease appearsto be limited largely to current users.12
In this prospective study, we addressed these issues and examinedthe relation between postmenopausal hormones and mortality toprovide a balanced assessment of the risks and benefits of hormoneuse. Moreover, because of the increase in the incidence of breastcancer with long-term hormone use and the decrease in heartdisease previously observed in this cohort,12,13 we also examinedthe relation between hormones and mortality among women at highrisk and those at low risk for these diseases.
Methods
The Nurses' Health Study Cohort
The Nurses' Health Study began in 1976 when 121,700 female registerednurses, 30 to 55 years of age, completed a mailed questionnaireconcerning their medical history, including information on menopause,cardiovascular disease, and cancer. We also obtained informationon risk factors for cardiovascular disease and cancer and onthe use of postmenopausal hormones. Biennial follow-up questionnaireswere mailed to update information on risk factors and identifynewly diagnosed cases of major illnesses.
Population for Analysis
Women who reported a history of cardiovascular disease (stroke,myocardial infarction, angina, or coronary revascularization)or cancer (except nonmelanoma skin cancer) on the 1976 questionnairewere excluded from the study. We classified women as postmenopausalfrom the time they reported having a natural menopause or hysterectomywith bilateral oophorectomy. Women who underwent hysterectomywithout bilateral oophorectomy were considered postmenopausalwhen they reached the age at which natural menopause had occurredin 90 percent of the cohort (54 years for smokers and 56 fornonsmokers).14 Women were eligible for the analysis when theybecame postmenopausal; those in whom cardiovascular diseaseor cancer was diagnosed before menopause were excluded, becausethis might have influenced their subsequent use of hormonesand risk of death.
Identification of Case and Control Subjects
We included deaths that occurred after the completion of the1976 questionnaire and before June 1, 1994. Most deaths werereported by the participants' families. We searched the NationalDeath Index to identify deaths among nonrespondents; mortalityfollow-up was more than 98 percent complete.15 For all deaths,we sought death certificates and, when appropriate, requestedpermission from the next of kin (subject to state regulations)to review medical records. The underlying cause of death wasassigned according to the International Classification of Diseases,Eighth Revision (ICD-8).16 The primary end point was death fromany cause, but we also examined mortality from coronary heartdisease (ICD-8 codes 410 to 414), stroke (codes 430 to 438),and cancer (codes 140 to 207). We identified 3637 deaths amongwomen who provided information about postmenopausal hormones.
For each case subject, 10 controls were chosen at random, withoutreplacement, from among women alive either at the time of thecase subject's death or, where relevant, at the time of thediagnosis of the disease leading to death. The control poolconsisted of all the women who met the same criteria as thecase subjects (that is, they were postmenopausal and free ofcancer and cardiovascular disease at base line or before menopause)and did not include women who died during follow-up. Controlswere chosen for each case subject, beginning with the earliestdeaths and proceeding systematically through the end of follow-up.Controls were matched to case subjects for age (within one year),age at menopause (within one year), and type of menopause (natural,bilateral oophorectomy, or hysterectomy or other), and the periodof the case patient's death (two-year time period). For 50 casesubjects, we were unable to identify 10 controls who met thesecriteria, and thus fewer than 10 were chosen; in all, 36,097controls were selected, of whom 34,625 provided informationabout hormone use for the relevant questionnaire cycle and wereincluded in this analysis. Since our focus was mortality, womenwho acquired major illnesses during follow-up but did not dieof their diseases were eligible to be controls. However, only3.2 percent of the controls had confirmed cardiovascular diseaseor cancer.
Ascertainment of Hormone Use
In 1976, women were asked about hormone therapy after menopauseand about the duration of their hormone use. Subsequent biennialquestionnaires, from 1978 to 1992, collected information onthe types of hormones used and updated information about currentuse.
For each death, we defined the woman's hormone status accordingto the report on the last questionnaire completed before herdeath or before diagnosis of the disease that led to her death(e.g., if breast cancer was diagnosed in 1983 in a participantwho died of the disease in 1988, hormone use was defined accordingto her 1982 questionnaire report). We thereby reduced bias causedby the discontinuation of hormone use between the diagnosisof a potentially fatal disease and subsequent death. For 71percent of the case subjects, we used the last questionnairecompleted before death (i.e., no change was made in the assignmentof exposure); for 11 percent, we used the questionnaire completedtwo time periods before death; for 8 percent, three time periodsbefore death; and for the remaining 10 percent, more than threetime periods before death. Each control's hormone use was identifiedon the basis of her report on the same questionnaire as thatof the matched case subject, thereby taking account of the increasingtrend toward prescribing hormones during the course of the study.
Statistical Analysis
The standard prospective analysis used for incident diseasesin this cohort12,13,14 would have been inappropriate to usefor mortality. Because of the need to establish hormone useat the time of diagnosis of the fatal disease rather than uniformlyat death, we would have thereby truncated follow-up for casesubjects but not for other subjects in a prospective analysis,thus exaggerating any apparent benefit of estrogen. In our nestedcase–control analysis, we could end follow-up simultaneouslyfor each case subject and her matched controls. This analysishas been used previously in examining mortality in the Nurses'Health Study.13
We used analytic techniques for matched data, including conditionallogistic regression17 to estimate the relative risks, calculatedas odds ratios, of death associated with hormone use, and thecorresponding 95 percent confidence intervals. Relative riskswere adjusted for the following risk factors: body-mass index(quintiles of the weight in kilograms divided by the squareof the height in meters), cigarette smoking (never a smoker,past smoker, or current smoker [1 to 14, 15 to 24, 25 to 34,or 35 or more cigarettes per day]), hypertension (yes, no),high cholesterol (yes, no), diabetes (yes, no), parental myocardialinfarction before the age of 60 (yes, no), history of breastcancer in mother or sister (yes, no), previous use of oral contraceptives(yes, no), parity (no children, one or more), and menarche before13 years of age (yes, no). In some analyses, we further adjustedfor quintiles of saturated-fat and alcohol intake; use of multivitamins(yes, no), vitamin E (yes, no), and aspirin (none, 1 to 6 aspirintablets per week, daily); and regular exercise (yes, no). Theseanalyses included only case subjects and matched controls from1980 to 1994, because data on these variables were not availableuntil 1980. In subgroup analyses limited to women with specificrisk factors, we used unconditional logistic regression17 andcontrolled for the matching factors.
Results
We included in the analysis 3637 deaths that occurred between1976 and 1994 among postmenopausal women; 461 of the women diedof coronary heart disease, 167 of stroke, and 1985 of cancer.Of the women who died of cancer, 425 died of breast cancer and58 (of whom 5 were hormone users) of endometrial cancer. Amongall the case subjects, 15.8 percent reported current hormoneuse on the last questionnaire completed before death or beforethe diagnosis of fatal disease, 27.8 percent were past users,and 56.4 percent had never used hormones. Among the controls,24.5 percent reported current use on the same questionnaireas their matched case subjects, 24.9 percent reported past use,and 50.6 percent reported that they had never used hormones.
Overall, we found an inverse association between current hormoneuse and death from all causes (crude relative risk, 0.58; 95percent confidence interval, 0.52 to 0.64) (Table 1). Adjustmentfor a wide variety of risk factors attenuated this estimateslightly, primarily because fewer hormone users than nonuserssmoked cigarettes; after adjustment, we observed a 37 percentdecrease in the risk of death for current hormone users as comparedwith those who had never used hormones (relative risk, 0.63;95 percent confidence interval, 0.56 to 0.70). Additional adjustmentfor dietary factors, alcohol intake, vitamin or aspirin use,and exercise did not materially affect the relative risk (0.67;95 percent confidence interval, 0.59 to 0.76). Because adjustmentfor these additional variables had little effect on the findingsbut would limit the population to those alive in 1980, whenwe began collecting these data, subsequent estimates are notadjusted for these factors. There was no apparent survival benefitfor past hormone users (relative risk, 1.03; 95 percent confidenceinterval, 0.94 to 1.12).
Table 1. Risk of Death among All Postmenopausal Hormone Users in the Nurses' Health Study, 1976 to 1994.
Among specific causes of death, as expected, the most markedreduction was in death due to coronary heart disease (relativerisk, 0.47; 95 percent confidence interval, 0.32 to 0.69 forcurrent users) (Table 1). The apparent decrease in mortalitydue to stroke among current hormone users was less certain becauseof the small number of deaths from stroke (relative risk, 0.68;95 percent confidence interval, 0.39 to 1.16). Mortality dueto cancer was also lower in current hormone users (relativerisk, 0.71; 95 percent confidence interval, 0.62 to 0.81). Additionaladjustment for diet, alcohol intake, vitamin or aspirin use,and exercise did not materially affect these cause-specificresults.
The survival benefit was attenuated among long-term hormoneusers (relative risk for 10 or more years of current use, 0.80;95 percent confidence interval, 0.67 to 0.96) (Table 2). Thisattenuation was primarily attributable to a 43 percent increasein death due to breast cancer (relative risk, 1.43; 95 percentconfidence interval, 0.82 to 2.48) with long-term use (dataon hormone use and breast cancer have been detailed elsewhere13,18).Past hormone use, regardless of duration, was not related tomortality.
Table 2. Risk of Death from All Causes among Current Users as Compared with Those Who Never Used Postmenopausal Hormones, According to the Duration of Use, 1976 to 1994.
Among past users, women who had stopped using hormones lessthan three years in the past had a 22 percent decrease in therisk of death from all causes (Table 3) (relative risk, 0.78;95 percent confidence interval, 0.66 to 0.92); this decreasein risk was maintained for three to four years after the discontinuationof hormone use, but the risk was slightly elevated after fiveyears.
Table 3. Risk of Death from All Causes among Past Users as Compared with Those Who Never Used Postmenopausal Hormones, According to the Length of Time since the Last Use, 1976 to 1994.
We also examined the effect of estrogen, both alone and combinedwith progestin (information was available for 92 percent ofthe case subjects and 89 percent of the controls). The relativerisk of death for current users of estrogen with progestin was0.46 (95 percent confidence interval, 0.36 to 0.58); for usersof estrogen alone it was 0.69 (95 percent confidence interval,0.60 to 0.80).
Because the greatest apparent decrease in risk was for deathfrom coronary heart disease, we repeated the analysis withinstrata defined by cardiovascular-risk status (Table 4). Amongthe 69 percent of the women who had at least one major cardiovascularrisk factor (current smoking, high cholesterol levels, highblood pressure, diabetes, a parental history of premature myocardialinfarction, or body-mass index of 29 or higher), we observeda 49 percent decrease in deaths from all causes for currenthormone users as compared with those who had never used hormones(relative risk, 0.51; 95 percent confidence interval, 0.45 to0.57). There was substantially less benefit among the 13 percentof the women who were at low risk for coronary heart disease(those who had never smoked cigarettes; did not have high cholesterollevels, high blood pressure, or diabetes; had no parental historyof myocardial infarction; and had a body-mass index of lessthan 25) (relative risk, 0.89; 95 percent confidence interval,0.62 to 1.28).
Table 4. Risk of Death from All Causes among Current Users as Compared with Those Who Never Used Postmenopausal Hormones, According to Risk-Factor Group.
We also examined the relation between current hormone use andmortality from all causes among women with a family historyof breast cancer (mother or sister) (Table 4). In that group(11 percent of the population), the relative risk of all-causemortality was 0.65 (95 percent confidence interval, 0.47 to0.90) for current hormone users as compared with those who hadnever used hormones. We also explored the association betweencurrent use and mortality in the presence of several other riskfactors (Table 4). For women with a body-mass index of 29 ormore, the inverse relation between hormone use and mortality(relative risk, 0.54; 95 percent confidence interval, 0.41 to0.72) was similar to that in the whole population. Among currenthormone users 50 years of age or less, the relative risk ofdeath was 1.05 (95 percent confidence interval, 0.65 to 1.68)as compared with those who had never used hormones; for womenwho had used hormones for 10 or more years, the relative riskwas 1.16 (95 percent confidence interval, 0.39 to 3.47) (datanot shown). For those 60 years of age or older, the relativerisk was 0.58 (95 percent confidence interval, 0.49 to 0.68)for current hormone use; the relative risks were 0.49 (0.40to 0.59) for less than 10 years of use and 0.79 (0.63 to 0.99)for 10 or more years of use.
Discussion
In this large, prospective study, women who were currently takingpostmenopausal hormones (i.e., as reported on the last questionnairecompleted by the case subject before a diagnosis of fatal diseaseor death) had a lower mortality rate than women who had neverused hormones, particularly for death due to coronary heartdisease. This apparent benefit disappeared within five yearsafter stopping use. Women with coronary risk factors had thegreatest reduction in mortality with hormone use, and therewas little decrease for women at low risk of heart disease.
We observed no increasing benefit of hormones with increasingduration of use; in contrast, the apparent benefits were attenuatedafter 10 or more years of current hormone use. Whereas lowerrates of cardiovascular mortality were maintained for long-termusers, the risk of breast cancer mortality in this populationwas elevated by 43 percent after 10 years of taking hormones.Thus, with additional years of use, expected mortality advantageswere, in part, offset by the risk of breast cancer; this wastrue even for the oldest women in the cohort (those 60 to 73years of age).
Information on hormone use was self-reported, perhaps leadingto some misclassification. However, we believe the reports tobe accurate, because participants were registered nurses witha demonstrated interest in medical research. Because the informationwas gathered prospectively, any misclassification is likelyto have been random and to have resulted in underestimationof the true association between hormone use and mortality. Inaddition, the causes of death were carefully documented.
The presence of a "healthy user" bias has been discussed inobservational studies of postmenopausal hormones and mortality.18Sturgeon et al.8 examined data from a prospective study that,like ours, regularly updated information on the use of hormones.They reported a higher mortality rate among women who had recentlystopped taking estrogen than among those who had never takenor were currently taking estrogen. Sturgeon et al. hypothesizedthat women discontinue hormone use when symptoms of a fataldisease develop, so that healthy women are classified as currenthormone users and diseased women as recent-past hormone users.The design of the present study addresses this problem by identifyinghormone status among the case subjects on the last biennialquestionnaire completed by each one before the diagnosis ofthe fatal disease rather than at death when relevant. Defininghormone use in this way, rather than in the way it was definedby Sturgeon et al., we found a decrease in the risk of totalmortality from any cause among recent-past hormone users.
Posthuma et al.11 reviewed studies of postmenopausal hormoneuse that reported data on cancer (primarily mortality from cancer).They found lower risks of cancer among hormone users and suggestedthat the decrease must reflect the selection of healthy womenfor estrogen therapy. Part of the decrease may be due to a causalrelation between hormones and some cancers (e.g., recent studies,including our own, have found a strong inverse association betweenhormone use and colon cancer19,20). In addition, most of thestudies reviewed considered hormone use before death ratherthan before diagnosis, leading to the bias described above,which we attempted to avoid; notably, for three leading causesof death from cancer whose incidence is unrelated to estrogenuse, we found no association with hormone use (ovarian: relativerisk, 0.94; pancreatic: relative risk, 1.00; and brain: relativerisk, 0.97).
General population surveys21,22 have found that women who takehormones are leaner and more likely to have screening tests.However, because variations in socioeconomic status and accessto health care are smaller among the registered nurses in thestudy than in the general population,18 the corresponding healthdifferences between the women who choose estrogen and thosewho do not are likely to be smaller than in the general population.The magnitude of such differences in the overall risk profilein our study can be gauged by comparing the crude relative risk(0.58) with the multivariate relative risk (0.63); the modestattenuation in apparent benefit after adjustment for many riskfactors shows that the degree of confounding is not large. Furthermore,most studies neither adjust for as many factors nor update informationon confounding variables; thus, confounding in this study wasmore rigorously controlled.
Nonetheless, a potential "healthy user" effect cannot be completelyeliminated in an observational study. Hormone users are morelikely to have certain diseases diagnosed in earlier stagesthan nonusers and will be less likely to die of their diseases.In support of this concept, we found a relative risk of 0.65for the incidence of colorectal cancer,19 and a relative riskof 0.46 for mortality from colorectal cancer among current hormoneusers. Similarly, the relative risk of death from breast canceramong current users was 0.76, whereas the relative risks ofincident disease ranged from 1.09 to 1.47,23 depending on theduration of use. Furthermore, for breast cancer, postmenopausalestrogen probably acts as a late-stage growth promoter; withdrawalof the hormone (that is, stopping its use after a diagnosisof cancer) could be particularly beneficial in cases due toexogenous hormone use, perhaps rendering the cancer less malignant(and less likely to be fatal) than that which arises in nonusersof hormones.
However, these phenomena are more plausible for cancer thanfor cardiovascular disease; for coronary heart disease, therelative risks of fatal and nonfatal disease are more similar(0.47 for mortality due to coronary disease and 0.58 for nonfatalcoronary events). Thus, a better disease prognosis or otherhealth characteristics in estrogen users can explain only partof the 37 percent decrease in mortality we observed among currenthormone users, much of which was attributable to a 53 percentdecrease in mortality due to heart disease.
The few other studies of mortality report an inverse associationwith postmenopausal hormone use, with most estimates of relativerisk ranging from 0.4 to 0.8,3,4,5,6,7,8,9 although only twostudies excluded prevalent cases of cancer and cardiovasculardisease at base line.6,9 Since women with disease at base lineare more likely to die during the study period and less likelyto take hormones, their inclusion would exaggerate the protectionprovided by hormone use. Finally, most previous studies havenot updated the information on hormone use. Because the benefitappears to be concentrated among current and recent users,2,12failure to update data will tend to result in underestimationof the value of current use. Further evidence bearing on therelation between hormone use and mortality will emerge in thenext decade from the Women's Health Initiative, a large, randomizedtrial.
In the population we studied, the largest reduction was formortality due to coronary disease and for mortality due to anycause among women with cardiovascular risk factors. However,our study population ranged in age from 30 to 73, with similarnumbers of deaths due to heart disease and breast cancer; inthe general population, heart disease is more prevalent. Thebalance of risks and benefits for mortality will be determinedlargely by the decreased risk of heart disease and the long-termincrease in breast cancer among women taking hormones and thuswill vary according to the distribution of causes of death inthe population under study.
Nonetheless, we know many ways to lower the risk of coronarydisease, but few to lower the risk of breast cancer. Furthermore,in the Nurses' Health Study, women taking hormones appear tobe at a greater risk for the development of breast cancer13than for death from the disease. The decision to use hormoneswill be based on many factors besides mortality, including qualityof life and the possibility of living with breast cancer. Onaverage, the survival benefits appear to outweigh the risks,but the risks and benefits vary depending on existing risk factorsand the duration of hormone use and must be carefully consideredfor each woman.
Supported by research grants (CA 40356 and HL 34594) from theNational Institutes of Health.
Source Information
From Channing Laboratory (F.G., M.J.S., G.A.C., W.C.W., J.E.M., B.R., C.F., S.E.H., D.J.H., F.E.S.) and the Division of Preventive Medicine (J.E.M., C.H.H.), the Departments of Medicine and of Ambulatory Care and Prevention (C.H.H.), Brigham and Women's Hospital and Harvard Medical School; and the Departments of Epidemiology (F.G., M.J.S., G.A.C., W.C.W., J.E.M., S.E.H., D.J.H., C.H.H.), Nutrition (M.J.S., W.C.W.), and Biostatistics (M.J., B.R.), Harvard School of Public Health — all in Boston.
Address reprint requests to Dr. Grodstein, Channing Laboratory, 181 Longwood Ave., Boston, MA 02115.
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Postmenopausal Hormone Therapy and Mortality
Whooley M. A., Grady D., Cummings S. R., Green J., Wintfeld N., Atkins C. D., Grodstein F., Stampfer M. J., Willett W. C.
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N Engl J Med 1997;
337:1389-1391, Nov 6, 1997.
Correspondence
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Decensi, A., Bonanni, B., Baglietto, L., Guerrieri-Gonzaga, A., Ramazzotto, F., Johansson, H., Robertson, C., Marinucci, I., Mariette, F., Sandri, M. T., Daldoss, C., Bianco, V., Buttarelli, M., Cazzaniga, M., Franchi, D., Cassano, E., Omodei, U.
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Goldstein, L. B., Adams, R., Becker, K., Furberg, C. D., Gorelick, P. B., Hademenos, G., Hill, M., Howard, G., Howard, V. J., Jacobs, B., Levine, S. R., Mosca, L., Sacco, R. L., Sherman, D. G., Wolf, P. A., del Zoppo, G. J.
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