The Use of Estrogens and Progestins and the Risk of Breast Cancer in Postmenopausal Women
Graham A. Colditz, M.B., B.S., Susan E. Hankinson, Sc.D., David J. Hunter, M.B., B.S., Walter C. Willett, M.D., JoAnn E. Manson, M.D., Meir J. Stampfer, M.D., Charles Hennekens, M.D., Bernard Rosner, Ph.D., and Frank E. Speizer, M.D.
Background The effect of adding progestins to estrogen therapyon the risk of breast cancer in postmenopausal women is controversial.
Methods To quantify the relation between the use of hormonesand the risk of breast cancer in postmenopausal women, we extendedour follow-up of the participants in the Nurses' Health Studyto 1992. The women were asked to complete questionnaires everytwo years to update information on their menopausal status,use of estrogen and progestin preparations, and any diagnosisof breast cancer. During 725,550 person-years of follow-up,we documented 1935 cases of newly diagnosed invasive breastcancer.
Results The risk of breast cancer was significantly increasedamong women who were currently using estrogen alone (relativerisk, 1.32; 95 percent confidence interval, 1.14 to 1.54) orestrogen plus progestin (relative risk, 1.41; 95 percent confidenceinterval, 1.15 to 1.74), as compared with postmenopausal womenwho had never used hormones. Women currently taking hormoneswho had used such therapy for 5 to 9 years had an adjusted relativerisk of breast cancer of 1.46 (95 percent confidence interval,1.22 to 1.74), as did those currently using hormones who haddone so for a total of 10 or more years (relative risk, 1.46;95 percent confidence interval, 1.20 to 1.76). The increasedrisk of breast cancer associated with five or more years ofpostmenopausal hormone therapy was greater among older women(relative risk for women 60 to 64 years old, 1.71; 95 percentconfidence interval, 1.34 to 2.18). The relative risk of deathdue to breast cancer was 1.45 (95 percent confidence interval,1.01 to 2.09) among women who had taken estrogen for five ormore years.
Conclusions The addition of progestins to estrogen therapy doesnot reduce the risk of breast cancer among postmenopausal women.The substantial increase in the risk of breast cancer amongolder women who take hormones suggests that the trade-offs betweenrisks and benefits should be carefully assessed.
Endogenous gonadal hormones have an important role in causingbreast cancer. Early age at menarche and late menopause increasethe risk of breast cancer.1,2 The number and timing of deliveriesalso affect this risk.3 Furthermore, among postmenopausal women,obesity is positively associated with serum concentrations ofendogenous estrogen4 and with moderate elevations in both theincidence of breast cancer and mortality from the disease.5,6
Hormone therapy also increases the risk of breast cancer inpostmenopausal women. Meta-analyses and reviews7 have assessedthe relation between the duration of postmenopausal hormonetherapy and the risk of breast cancer, but questions remain.Unresolved issues include the risks associated with estrogenplus progestins,8 the risks with progestins alone, and the variationin risk according to age.9 To address these issues, we extendedthe analysis of the participants in the Nurses' Health Studythrough 1992, adding 50 percent more prospective data to thosein our previous report.10
Methods
The Nurses' Health Study was established in 1976, when 121,700female registered nurses 30 to 55 years of age completed a mailedquestionnaire that included items about known or suspected riskfactors for cancer and cardiovascular diseases. Base-line informationincluded details of risk factors for breast cancer,11,12 theuse of oral contraceptives, and the postmenopausal use of hormones.Every two years, we mail follow-up questionnaires to the womenand ask them to update the information on risk factors, includingwhether they currently take hormones, the duration of hormoneuse, and the type of hormone preparation used (starting in 1978).We used the information on each questionnaire to define thewomen's status with respect to hormone therapy for the subsequenttwo-year period.
Identification of Cases of Breast Cancer
On each questionnaire, we asked whether breast cancer had beendiagnosed and, if so, the date of diagnosis. We routinely searchedthe National Death Index for deaths among women who did notrespond to the questionnaires. We asked all women who reportedbreast cancer (or the next of kin, for those who had died) forpermission to review the relevant hospital records and confirmthe diagnosis. Pathology reports, obtained for 93 percent ofthe cases, confirmed breast cancer in all but 10 women who reportedit. Although hospital records could not be obtained for 7 percentof the cases, we based our analysis on all cases of newly diagnosedbreast cancer, because the degree of accuracy of the participants'reports was extremely high among those for whom records wereobtained. We omitted the small number of cases of carcinomain situ (n = 157) from the primary analysis.
Population for Analysis
We excluded from the analysis all women who had reported breastcancer or other cancer (except nonmelanoma skin cancer) on the1976 questionnaire and all premenopausal women. We classifieda woman as postmenopausal from the time she returned a questionnaireon which she reported natural menopause or hysterectomy withbilateral oophorectomy. We classified women who reported hysterectomywithout bilateral oophorectomy as postmenopausal when they reachedthe age at which natural menopause had occurred in 90 percentof the cohort (54 years for current cigarette smokers and 56years for nonsmokers).
As reported on the 1976 questionnaire, 23,965 women were postmenopausal;these women entered follow-up in the period from 1976 to 1978.The women's reported menopausal status was updated every twoyears, and the study population was expanded to include womenin whom menopause occurred. By 1990, the beginning of the finaltwo-year follow-up period for this analysis, 69,586 women wereclassified as postmenopausal. Follow-up of the cohort for theidentification of nonfatal breast cancer by means of questionnairesand telephone interviews was 95 percent complete. For fatalbreast cancer, follow-up was more than 98 percent complete.13
Statistical Analysis
For each participant, follow-up time was allocated accordingto the 1976 exposure variables, which were updated at the beginningof each two-year period on the basis of the information providedby the women on follow-up questionnaires. Follow-up terminatedwith the date of diagnosis of breast cancer, the date of death,or June 1, 1992. Women who reported a diagnosis of cancer otherthan nonmelanoma skin cancer on any questionnaire were excludedfrom subsequent follow-up. If no questionnaire was returnedfor a follow-up cycle and the woman had previously reportedcurrent postmenopausal hormone use, her hormone-use status wasclassified as missing in the updated analysis.
As a measure of association, we used the relative risk, definedas the incidence of breast cancer among women who had takenhormones after menopause divided by the incidence among womenwho had never used such therapy. We conducted stratified analysesto control for risk factors and to assess the possible influenceof other risk factors for breast cancer on the effect of postmenopausalhormone use. We used proportional-hazards models to adjust formultiple risk factors simultaneously.14
To assess the relation between postmenopausal hormone therapyand mortality due to breast cancer, we identified all deathsdue to breast cancer from 1976 through June 1, 1992, among womenwho were postmenopausal at the time of the diagnosis (n = 359).For each woman who died of breast cancer, we matched 10 womenselected at random from among the women who were free from breastcancer, according to the year of birth and the age at menopause.We defined hormone use for these case patients and their controlsas that reported on the questionnaire completed immediatelybefore the diagnosis of breast cancer. To estimate the relativerisk of breast cancer according to current and past postmenopausalhormone therapy, we used the odds ratio from a logistic regressionin which we controlled for the year of birth and the age atmenopause. This approach accounted for changes in estrogen useover time and avoided bias due to the discontinuation of hormoneuse by women who had received a diagnosis of breast cancer.
Results
During 725,550 person-years of follow-up, we identified 1935cases of invasive breast cancer among postmenopausal women.Even though progestin use increased in this cohort, it did notadd to the risk of breast cancer associated with the use ofestrogen alone. Before 1986, few women took progestin. In 1986,18 percent of postmenopausal women taking hormones used progestin;this proportion rose to 30 percent in 1990. Most women (73 percent)used conjugated estrogens; 77 percent of those who used estrogenomitted taking the drug for one week each month in 1986, and66 percent did so in 1988. Almost all women receiving progestintook it for 14 or fewer days per month; the most common doseof medroxyprogesterone was 10 mg per day (used by 58 percentof the women who took this drug).
From 1978 to 1992, we observed a significant elevation in therisk of breast cancer among women using conjugated estrogensalone (adjusted relative risk, 1.32; 95 percent confidence interval,1.14 to 1.54), estrogen plus progestin (adjusted relative risk,1.41; 95 percent confidence interval, 1.15 to 1.74), and progestinsalone (adjusted relative risk, 2.24; 95 percent confidence interval,1.26 to 3.98) (Table 1). These relative risks did not differsignificantly from each other. For each age at menopause, therelative risk of breast cancer was at least as high for womentaking estrogen plus progestin as for those taking conjugatedestrogens alone. The small number of cases among women takingestrogen plus progestin precluded detailed analysis of the riskaccording to duration of use and age. However, the similar relativerisks for estrogen alone and for estrogen plus progestin suggestthat these types of hormone use could be combined in analysesof the duration of therapy.
Table 1. Type of Hormone Currently Used by Postmenopausal Women and Relative Risk of Breast Cancer in the Nurses' Health Study, 1978 to 1992.
Among women currently taking hormones, the relative risk ofbreast cancer was highest among the oldest women (relative risk,1.69 for women 65 to 69 years old, 1.42 for women 60 to 64 yearsold, 1.41 for those 55 to 59 years old, 1.46 for those 50 to54 years old, and close to 1.0 for women younger than 50). Therisk of breast cancer increased significantly only among womencurrently using hormone therapy who had used such therapy forfive or more years. The dose of estrogen among these women didnot differ from that received by women who had taken estrogenfor less than five years. In contrast, women who had formerlyused hormone therapy had no significant increase in risk ascompared with women who had never used hormone therapy; thiswas true even for women who had taken hormones for five or moreyears in the past (Table 2).
Table 2. Duration of Current and Past Postmenopausal Hormone Therapy and Relative Risk of Breast Cancer in the Nurses' Health Study, 1976 to 1992.
As compared with postmenopausal women who had never taken hormones,and after controlling for the age at menopause, the type ofmenopause, and family history, the relative risk of breast canceramong postmenopausal women who used hormones was 1.54 (95 percentconfidence interval, 1.19 to 2.00) for those 55 to 59 yearsof age who had taken hormones for five or more years. For women60 to 64 years of age, the relative risk was 1.71 (95 percentconfidence interval, 1.34 to 2.18). A shorter duration of usewas not consistently related to the risk of breast cancer (Figure 1).
Figure 1. Incidence and Relative Risk of Breast Cancer According to Age and the Duration of Current Postmenopausal Hormone Therapy.
Relative risks and 95 percent confidence intervals are shown on the top of the bars; relative risks are expressed in comparison with the risk among women in each age group who never received hormone therapy. Data have been adjusted for age at menopause, type of menopause, and family history of breast cancer in a proportional-hazards analysis.
The multivariate adjusted relative risk for five or more yearsof past use was 0.92 (95 percent confidence interval, 0.63 to1.35) among women 55 to 59 years old and 1.13 (95 percent confidenceinterval, 0.83 to 1.55) among those 60 to 64 years old whenthese women were compared with those who never took hormones.Women who stopped taking hormones after five or more years ofuse were at increased risk of breast cancer for a short periodafter stopping. For those who had stopped taking hormones lessthan two years earlier, the multivariate adjusted relative riskwas 1.44 (95 percent confidence interval, 0.99 to 2.08); forthose who had stopped two to four years earlier, the relativerisk was 0.80 (95 percent confidence interval, 0.55 to 1.16);and for those with five or more years since their most recentuse of hormones, the relative risk was 0.95 (95 percent confidenceinterval, 0.74 to 1.25).
On the basis of the 359 deaths due to breast cancer among womenwho were postmenopausal at the time of diagnosis, the overallrelative risk of death, adjusted for family history and historyof benign breast disease, was 1.14 (95 percent confidence interval,0.85 to 1.51) for women currently taking hormones and 0.80 (95percent confidence interval, 0.60 to 1.07) for those who usedhormones in the past. The relative risk for women currentlytaking hormones with less than five years of use at the timeof diagnosis was 0.99 (95 percent confidence interval, 0.66to 1.48), and for women with five or more years of use, therelative risk of death from breast cancer was 1.45 (95 percentconfidence interval, 1.01 to 2.09).
Discussion
In this prospective cohort study, we observed an elevated riskof invasive breast cancer among postmenopausal women who werecurrently taking estrogen alone or both estrogen and progestin.The increase in risk was most pronounced among women over theage of 55 and was largely limited to the women who had usedhormone therapy for five or more years. These data on womenin the United States thus confirm findings from Europe, wherecombination therapy with estrogen plus progestins has been associatedwith an increased risk of breast cancer.15,16,17 Because widespreaduse of progestins is a recent phenomenon, we were unable toexamine associations with risk according to the dose or durationof progestin use. Furthermore, we have no data to explain whywomen in this cohort take hormones after menopause or why theystop.
The addition of progestin to estrogen therapy has been growingmore common in the United States, but epidemiologic data onthe effects of combination therapy are limited.18 The initialreport by Gambrell et al.19 (based on 11 cases of breast canceramong women receiving estrogen plus progestin) suggested thatcombination therapy has a protective effect against breast cancer,but that study did not control for age or other confoundingfactors. Subsequent studies have found an elevated risk of breastcancer among Danish women who took sequential estrogen plusprogestin (62 cases; relative risk, 1.4) and among Swedish womenwith a history of long-term use of combined hormone therapy(10 cases; relative risk, 4.4). In a British study, the riskof breast cancer was similar among women taking estrogen aloneand among those taking estrogen plus progestin. Among threeU.S. case–control studies20,21,22 (a total of 48 casesin women who took hormones), two found an increased risk inassociation with combined therapy (as compared with no use ofhormones),20,22 and one found no association.21 The multivariateadjusted relative risk of breast cancer that we observed (1.41)is compatible with the confidence intervals in all previousstudies (except that of Gambrell et al.) and is based on 111cases in women taking estrogen plus progestin. These data clearlyindicate that the addition of progestin does not reduce therisk of breast cancer that is associated with estrogen use inpostmenopausal women. Ductal cells of the breast therefore responddifferently from the endometrium, where the addition of a progestincounters the adverse effect of estrogen. Hence, these data donot support the use of progestin by women who have undergonehysterectomy.
Estrogens increase serum hormone concentrations to approximatethose in premenopausal women,23,24,25,26 and 1.25 mg of conjugatedestrogens has a greater effect than 0.625 mg.26 There is evidencethat progestins, when added to estrogen, may enhance the proliferationof epithelial cells in the breast.27
One potential source of bias in our study is the differencesin the rates of participation in mammographic screening. Weaddressed this problem in several ways. First, because mammographydetects a larger proportion of in situ breast cancers than othermethods, we excluded such cases from this analysis. As expected,current use of hormones was somewhat more strongly associatedwith in situ disease (age-adjusted relative risk, 1.95), a findingthat is consistent with the slightly higher frequency of screeningmammography among postmenopausal women taking hormones. However,the age-standardized rate of screening mammography was onlyabout 14 percent higher among women currently using hormonesand 8 percent higher among past users of hormones than amongpostmenopausal women who never used hormones. Furthermore, from1988 to 1992, only 9 percent of women who never used hormones,6 percent of past users, and 3 percent of those currently usinghormones did not undergo at least one mammogram. This differenceis proportionately much smaller than the increase in risk forcurrent users of hormones, and the large majority of women hadbeen screened previously. Thus, it is unlikely that differencesin the frequency of mammographic studies can explain the elevationin the risk of breast cancer among current postmenopausal recipientsof hormone therapy. Moreover, postmenopausal women who receivedhormone therapy in the past and those who had been taking suchhormones for less than five years were not at increased riskfor breast cancer despite a higher rate of screening mammography.Finally, the higher risk of death due to breast cancer amongwomen who had taken hormone therapy for five or more years atthe time of diagnosis adds further weight to the causal association,because analyses based on mortality overcome problems of leadtime and selective detection of tumors.28
In this analysis, we confirmed our earlier finding of a greaterincrease in the risk of breast cancer among older women takinghormones after menopause. This finding is consistent with datafrom several case–control studies that suggested an increasedrisk among older women, independent of the duration of hormoneuse.21,29,30 This effect was stronger among women with fiveor more years of current use of hormones. The lack of associationbetween current estrogen therapy and breast cancer among youngerwomen may be due at least in part to the short time since menopause.Our data and those from several case–control studies suggestthat the use of hormones at older ages after menopause may havea particularly deleterious effect on the risk of breast cancer.
These findings suggest that women over 55 years of age shouldcarefully consider the risks and benefits of estrogen therapy,especially if they have used estrogen for five or more years.It is not clear that benefits outweigh risks for all women,particularly women with few risk factors for heart disease.Furthermore, short-term estrogen therapy — for up to sevenyears — in the decade after menopause cannot be expectedto protect against osteoporotic fractures many years later.31,32Our data indicate that the addition of progestins to postmenopausalestrogen therapy does not reduce the risk of breast cancer.Estrogen alone, estrogen plus progestin, and progestins aloneall appear to raise the risk of breast cancer. The significantincrease in the risks of breast cancer and of death due to breastcancer among postmenopausal women over 55 who are currentlytaking hormones and who have used this therapy for five or moreyears suggests that the risks and benefits of hormone therapyamong older women should be carefully assessed.
Supported by a grant (CA 40956) from the National Institutesof Health. The work of Dr. Colditz was supported in part bya grant (FRA-396) from the American Cancer Society.
Source Information
From the Channing Laboratory, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School (G.A.C., S.E.H., D.J.H., W.C.W., J.E.M., M.J.S., C.H., B.R., F.E.S.), and the Departments of Epidemiology (G.A.C., S.E.H., D.J.H., W.C.W., M.J.S.), Biostatistics (B.R.), and Nutrition (W.C.W., M.J.S.), Harvard School of Public Health — all in Boston. Presented in part at the meeting of the American Association for the Advancement of Science, San Francisco, February 22, 1994.
Address reprint requests to Dr. Colditz at Harvard Medical School, Channing Laboratory, 180 Longwood Ave., Boston, MA 02115.
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Breast Cancer and Hormone-Replacement Therapy
Brunoski T., Powell L. H., Blackman J. A., Bush T. L., Joseph K.S., Dupont W. D., Wigg D.R., Bluming A. Z., Colditz G. A., Willett W. C., Speizer F. E.
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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;
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Writing Group for the Women's Health Initiative In,
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A correction has been published: N Engl J Med 1995;333(20):1355.
