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ORIGINAL RESEARCH |
From the *Epidemic Intelligence Service, Division of Applied Public Health Training, Epidemiology Program Office; Division of Reproductive Health, National Center for Chronic Disease Prevention and Health Promotion; and Division of Cancer Prevention and Control, National Center for Chronic Disease Prevention and Health Promotion, Centers for Disease Control and Prevention, Atlanta, Georgia.
Address reprint requests to: Maura K. Whiteman, PhD, Centers for Disease Control and Prevention, 4770 Buford Highway NE, Mailstop K-34, Atlanta, Georgia 30341-3724; e-mail: acq5{at}cdc.gov.
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ABSTRACT |
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 ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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METHODS: We followed up 4,299 U.S. women enrolled between 1980 and 1982 at ages 20–54 years as incident breast cancer cases in a population-based, case-control study, the Cancer and Steroid Hormone Study. Vital status through 1997 for these cases was obtained by linking Cancer and Steroid Hormone Study data to Surveillance, Epidemiology, and End Results files. We estimated hazard ratios (HRs) and 95% confidence intervals (CIs) for death associated with selected reproductive factors using proportional hazards models.
RESULTS: During a median follow-up of 14.5 years, 1,847 deaths occurred. Women aged 20–45 years whose last birth occurred 12 months or less (age-adjusted HR = 1.62, 95% CI 1.10–2.37) and 13–48 months before breast cancer diagnosis (age-adjusted HR = 1.35, 95% CI 1.05–1.75) were at an increased risk for death compared with nulliparous women. After adjusting for additional factors including tumor stage, women whose last birth occurred 12 months or less before diagnosis remained at an increased risk for death (HR = 1.51, 95% CI 1.02–2.23). Fifteen-year survival was 38%, 51%, and 60% among women aged 20–45 years whose last birth was 12 months or less, 13–48 months, and more than 48 months before diagnosis, respectively, compared with 65% among nulliparous women. Mortality risk was not associated with age at first birth, parity, or breastfeeding duration among women aged 20–45 years or among women aged 46–54 years.
CONCLUSION: A recent birth may be an adverse prognostic indicator among women diagnosed with breast cancer at ages 20–45 years.
LEVEL OF EVIDENCE: II-2
Reproductive factors, including nulliparity and late age at first full-term pregnancy, are among the established risk factors for developing breast cancer,6 although less is known about the role of these and other reproductive factors in mortality after diagnosis. It is possible that reproductive risk factors for incident breast cancer promote the development of specific types of breast cancer with different prognostic consequences. Although some studies have examined the associations between reproductive factors and breast cancer mortality, their results are variable, with some suggesting an increased risk for mortality with ever having a birth,7,8 recent birth,7–12 older age at first birth,7 younger age at first birth,13 and higher parity.10 We explored the associations between mortality up to 17 years after breast cancer diagnosis and reproductive factors, including ever being pregnant, number of pregnancies, ever having a birth, age at first birth, parity, time since last birth, and lifetime duration of breastfeeding. To examine these associations, we linked data for breast cancer cases from the Cancer and Steroid Hormone Study, a population-based, case-control study, to survival information from the Surveillance, Epidemiology, and End Results Program. The Cancer and Steroid Hormone Study has contributed significantly to our understanding of hormonal and reproductive risk factors for developing breast cancer;14–17 in this report we have used data from that study to examine reproductive risk factors for mortality after primary breast cancer diagnosis.
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MATERIALS AND METHODS |
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ABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Breast cancer cases from the Cancer and Steroid Hormone Study were women aged 20–54 years who were diagnosed with primary breast cancer between December 1, 1980, and December 31, 1982, while residing in 1 of the 8 study locations. Of the 5,884 women identified as meeting the case definition, 4,730 participated in the Cancer and Steroid Hormone Study (80.4%). Reasons for nonparticipation included inability to locate the woman or to conduct an interview within 6 months (8.1%), refusal (4.1%), debilitating illness (3.6%), physician refusal (2.9%), or death (0.9%).
In the Cancer and Steroid Hormone Study, trained interviewers administered a questionnaire to each study participant in her home within 6 months of breast cancer diagnosis. The average time between diagnosis and interview was 2.5 months. Information was collected on reproductive and contraceptive histories, medical and family histories, use of medical services, and personal characteristics and habits. For each pregnancy, the following information was recorded: outcome of the pregnancy (single live birth, multiple birth, stillbirth, spontaneous miscarriage, tubal or ectopic pregnancy), duration of pregnancy, month and year the pregnancy ended, and duration of breastfeeding following the pregnancy. A life calendar from menarche to menopause was constructed for each woman to assist in the recall of reproductive events in relation to major life events such as marriages, divorces, and deaths.
Vital status information through December 31, 1997, was obtained by linking Cancer and Steroid Hormone Study interview data with Surveillance, Epidemiology, and End Results public access data files.19 We successfully linked 4,536 of the 4,730 Cancer and Steroid Hormone breast cancer cases (95.9%) to a Surveillance, Epidemiology, and End Results record using matching criteria of gender, cancer site, geographic location of the Surveillance, Epidemiology, and End Results registry, Surveillance, Epidemiology, and End Results identification number, year of birth, and diagnosis date (within 2 months). Surveillance, Epidemiology, and End Results also provided information regarding the stage of tumor at diagnosis (Surveillance, Epidemiology, and End Results historic stage: localized, regional, or distant disease), histologic type of tumor, and first course of treatment. Survival time in Surveillance, Epidemiology, and End Results was defined as the time in months from the date of diagnosis to the date of death or for those not known to have died, the time from the date of diagnosis to the date last known to be alive. Women diagnosed with in situ tumors (n = 228) or who were pregnant at the time of diagnosis or at the time of interview (n = 9) were excluded. Thus 4,299 women were included in this study.
We examined deaths due to any cause as well as deaths due to breast cancer (International Classification of Diseases, 9th Revision, codes 174.0–174.9) as outcomes. We conducted separate analyses for women aged 20–45 years and 46–54 years at diagnosis, because previous studies suggest the relationship between reproductive factors and breast cancer risk differ by age at diagnosis.20 Results were similar when analyses were stratified by menopausal status; thus, only age-stratified analyses are reported.
We used Kaplan-Meier methods21 to estimate 5-year, 10-year, and 15-year survival after breast cancer diagnosis. Hazards ratios (HRs) and 95% confidence intervals (CIs) derived from Cox proportional hazards models22 were used to estimate the relative risk for death associated with reproductive factors. All analyses were adjusted for age at diagnosis. Reproductive factors considered included ever being pregnant, number of pregnancies, ever having a birth, age at first birth, parity, time between most recent birth and diagnosis, and lifetime duration of breastfeeding. We examined the following as potential confounders: surgery, radiation therapy, history of benign breast disease, family history of breast cancer, race, smoking, body mass index (BMI), use of oral contraceptives, education, Surveillance, Epidemiology, and End Results registry, and number of comorbidities (diabetes, hypertension, blood clots, kidney disease, gallbladder disease, heart attack, rheumatoid arthritis, paralysis, stroke, and other cancers). Variables were included in the final model on the basis of prior literature or their independent association with mortality or the reproductive factor of interest. Because stage of disease at diagnosis may act as an intermediate factor rather than a confounder, it was entered separately into the model to assess the extent to which it would explain an association. The adequacy of the Cox proportional hazards assumptions for the included variables was checked by log (–log [survival]) curves as well as interaction terms with follow-up time. The log (–log [survival]) curves were approximately parallel, and the interaction terms with follow-up time were nonsignificant, thereby confirming the assumption of proportionality of hazards.
Trends were assessed among parous women for selected reproductive factors by entering the categorical variable of interest as a single term with equally spaced category scores into the proportional hazards model. To assess whether the effect of reproductive factors on survival differed between subgroups of women, we examined tumor stage, family history of breast cancer, history of benign breast disease, BMI, oral contraceptive use, and race as potential effect modifiers. Statistical significance of effect modifiers at the P < .05 level was determined by the log likelihood ratio test between a full model containing the relevant interaction terms and a reduced model without the interaction terms.
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RESULTS |
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ABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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During a median follow-up of 14.5 years, 1,847 deaths occurred in the study population, 846 in women aged 20–45 years at diagnosis and 1,001 in women aged 46–54 years at diagnosis. Of the 1,847 deaths, 1,475 (79.9%) were recorded as deaths due to breast cancer. Of the 372 deaths in the study population not coded as due to breast cancer, more than 30% did not have cause of death available. Analyses with all-cause mortality and breast cancer mortality yielded similar results; only those with all-cause mortality are shown.
There was no increase in the age-adjusted risk of mortality associated with ever being pregnant, number of pregnancies, ever having a birth, age at first birth, parity, or duration of breastfeeding among both women aged 20–45 years and women aged 46–54 years at diagnosis (Table 2). Compared with nulliparous women, women aged 20–45 years whose last birth occurred 12 months or less before diagnosis were at an increased risk of dying (age-adjusted HR = 1.62, 95% CI 1.10–2.37) and women whose last birth occurred 13–48 months before diagnosis were at a moderately increased risk (age-adjusted HR = 1.35, 95% CI 1.05–1.75). However, women whose last birth was more than 48 months before diagnosis were not at an increased risk (HR = 1.02, 95% CI 0.85–1.24).
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Among women aged 20–45 years at diagnosis, survival at 5, 10, and 15 years was poorest among those whose last birth occurred 12 months or less before diagnosis and increased in a generally linear manner with increasing time since last birth (Figure 1). At 15 years, survival was 38% (95% CI 25–52%) among women whose last birth occurred 12 months or less before diagnosis, 51% (95% CI 44–58%) among women whose last birth was 13–48 months before diagnosis, 60% (95% CI 55–65%) among women whose last birth was more than 48 months before diagnosis, and 65% (95% CI 60–70%) among nulliparous women.
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Adjustment for surgery, radiation therapy, race, oral contraceptive use, education, BMI, and history of benign breast disease did not substantially change the age-adjusted estimates of the association between time since last birth and mortality among women aged 20–45 years at diagnosis (Table 3). Women aged 20–45 years with more recent births were more likely to be diagnosed with distant or regional stage tumors than were nulliparous women; 61.4%, 54.6%, and 51.8% of women aged 20–45 years whose last birth was 12 months or less, 13–48 months, and more than 48 months before diagnosis, respectively, were diagnosed with distant or regional tumors, compared with 42.6% of nulliparous women. Inclusion of stage in the model attenuated the association between time since last birth and mortality somewhat, although women aged 20–45 years whose last birth was 12 months or less before diagnosis remained at an increased risk of dying compared with nulliparous women (HR = 1.51, 95% CI 1.02–2.23) (Table 3). Women whose last birth occurred 13–48 months before diagnosis were at a moderately increased risk, although the increase in risk was no longer statistically significant (HR = 1.25, 95% CI 0.95–1.64). There remained a pattern suggesting an increased risk for death with less time since most recent birth (P trend in parous women less than .05).
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In additional analyses restricted to parous women, breastfeeding at the time of last birth did not alter our findings of an increased risk for death among women aged 20–45 years with recent births. Age at first birth was examined as a potential confounder among multiparous women (for primiparous women the effect of time since last pregnancy cannot be assessed independently of age at first birth14) and did not influence our results. Finally, our findings regarding the association between recent birth and mortality after breast cancer diagnosis were unchanged in a subgroup analysis limited to women with ductal tumors.
Our findings regarding recent birth and mortality risk among women aged 20–45 years did not differ significantly according to family history of breast cancer, history of benign breast disease, BMI, oral contraceptive use, or race. Although the association between time since last birth and mortality also did not differ significantly by stage of tumor at diagnosis (P = .15), the association was stronger among women with distant or regional tumors than among women with local tumors (Table 4).
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To assess whether a detection delay may explain the increased risk for death among women aged 20–45 years with a more recent birth, we assessed mode of cancer detection, frequency of breast exams, and frequency of mammography according to time since last birth. Before their first breast problem, 33% of women whose last birth was 12 months or less before diagnosis reported having a breast examination more than once a month (self-examination, or examination by a doctor or nurse) compared with 32% and 28% of women whose last birth was 13–48 months and more than 48 months before diagnosis, respectively, and 30% of nulliparous women (P > .05). Mode of cancer detection and frequency of mammography also did not differ significantly according to time since last birth.
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DISCUSSION |
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Our finding of an increased risk for mortality after breast cancer diagnosis among women with a recent birth is consistent with most,7–12 but not all,23,24 prior studies. In a study by Eweritz et al,23 a recent birth was defined as occurring less than 5 years before diagnosis, which may have precluded the detection of an increased risk among women with births 1–2 years before diagnosis. Another study reported no increase in the risk of distant metastasis with a recent birth before breast cancer diagnosis.23 In our study—as well as in some,7,12 but not all,11 previous studies—the survival disadvantage among women with a recent birth is not fully explained by stage of tumor at diagnosis.
Consistent with most past studies, we found no increase in mortality risk after breast cancer diagnosis with other reproductive factors, including ever being pregnant, number of pregnancies, ever having a birth, age at first birth,11 parity,7,11,13,23 or lifetime duration of breastfeeding among both women aged 20–45 years and aged 46–54 years at diagnosis. Although other studies have noted an increased risk associated with ever having a birth,7,8 some studies attribute such findings to the increased risk among women with a recent birth.7 Although longer lifetime duration of breastfeeding may decrease the risk for incident breast cancer,25 no other studies have assessed its effect on survival after breast cancer diagnosis. Our study, along with most past research, does not support an association between these other reproductive factors and survival after breast cancer diagnosis.
We considered biologic mechanisms through which a recent birth may increase risk for a poor prognosis after breast cancer diagnosis. In vitro experiments show that pregnancy hormones may stimulate tumor cell growth,26 which would increase the volume of a tumor diagnosed shortly after pregnancy; however, previous studies found that the poorer survival associated with recent birth is independent of tumor size and nodal status,7,9,10,12 suggesting enhanced growth alone does not explain the survival disadvantage. Because progression from initiation of breast cancer to clinical detection is estimated to take several years, the cancers detected in women with a recent birth were most likely present subclinically before pregnancy. Perhaps the most likely explanation for the poorer survival in women with a recent birth is that the biologic changes that accompany pregnancy alter the course of breast cancer by increasing not only generalized tumor growth but by promoting the selection and growth of more aggressive cells in an already existing, occult breast tumor. Others have reported that women with recent births, either less than 2 years7,12 or 12 months or less,9 before breast cancer diagnosis were more likely than nulliparous women to have tumors with unfavorable characteristics, including positive nodes,7,9,12 higher histologic grade,7,12 p53 positive,7 high mitotic count,7 and high S phase fraction.7 These observations support the assertion that tumors with poor prognostic characteristics may be selected for enhanced growth by pregnancy hormones. In a study conducted by Daling et al,7 however, the association between recent birth and mortality after breast cancer diagnosis remained significant and essentially unchanged after controlling for a broad panel of tumor markers, suggesting that as yet unknown tumor characteristics or factors other than tumor characteristics may contribute to the poor prognostic effect of a recent birth.
It is also possible that the poorer survival observed among women with a recent birth in this study could be explained by a diagnostic delay. Women who recently gave birth likely devote most of their attention to child care, which may prevent them from detecting breast cancer symptoms, reporting these symptoms to a health care provider, or having breast exams; however, because we found no difference in mode of cancer detection, frequency of breast exams, or frequency of mammography according to time since last birth, our data do not support the hypothesis of a detection delay in women with a recent birth. The increased density of breast tissue among younger women, particularly those who are lactating, may make tumors more difficult to detect clinically, leading to tumors being diagnosed at later stages. Tumor stage did not fully explain the poorer survival rate seen in women with a recent birth, however, suggesting that additional factors are involved.
Our study was subject to several limitations. First, there was limited information on tumor characteristics. Extent of disease (size, grade, and lymph node involvement) and receptor status was not available, because Surveillance, Epidemiology, and End Results Program did not collect this information at the time the Cancer and Steroid Hormone participants were diagnosed. Another limitation is the lack of information on adjuvant therapy, because women with recent births may be less likely to undergo adjuvant therapy, which may result in poorer survival rates. However, Kroman et al12 found that a recent birth had an adverse effect on survival among women who did and women who did not receive adjuvant treatment. An additional limitation of our study was the lack of information on possible prognostic or confounding factors occurring after breast cancer diagnosis. Finally, the upper age limit of our study population was 54, whereas the majority of breast cancers occur in older women.
The strengths of our study include the large sample-size, population-based case selection, detailed collection of reproductive history, and long period of follow-up. Unlike other studies, the present study had information regarding mode of cancer detection, frequency of breast exams, and frequency of mammography. This allowed us to assess more directly whether a detection delay due to lack of attention to care could explain the poorer survival rates observed among women with recent births.
Consistent with most previous reports, this study suggests that women aged 20–45 years diagnosed with breast cancer 12 months or less after giving birth are at a survival disadvantage. In future studies examining this association it will be useful to obtain information on symptom detection and medical care usage to assess the influence of detection delay as well as information on molecular tumor characteristics to assess whether tumors in women with recent births are more aggressive than tumors in other women. Additional research is needed to assess whether a recent birth could be an important consideration in evaluation, subsequent counseling, and treatment options in younger breast cancer patients. Although breast cancer is a rare disease in younger women (incidence in women aged younger than 50 years is 43 per 100,00027), they typically have a poorer prognosis than older women. The effect of a recent birth may, in part, explain this survival disadvantage in younger women with breast cancer.
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Footnotes |
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The Cancer and Steroid Hormone Study was supported by interagency agreement 3-Y01-HD-8-1037 between the Centers for Disease Control and Prevention and the National Institute of Child Health and Human Development, with additional support from the National Cancer Institute.
The authors thank Caroline Costello for her work on the data linkage and acknowledge the many contributors to the Cancer and Steroid Hormone Study, including George L. Rubin, Nancy C. Lee, Michele G. Mandel, Herbert B. Peterson, Raymond Greenberg, J. Wister Meigs, W. Douglas Thompson, G. Marie Swanson, Elaine Smith, Charles Key, Dorothy Pathak, Donald Austin, David Thomas, Joseph Lyon, Dee West, Fred Gorstein, Robert McDivitt, Stanley J. Robboy, Lonnie Burnett, Robert Hoover, Peter M. Layde, Howard W. Ory, James J. Schlesselman, David Schottenfeld, Bruce Stadel, Linda A. Webster, Colin White, Walter Bauer, William Christopherson, Deborah Gersell, Robert Kurman, Allen Paris, and Frank Vellios.
10.1097/01.AOG.0000128173.01611.ff
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