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Breast Cancer Risk Estimates for Relatives of White and African American Women With Breast Cancer in the Women's Contraceptive and Reproductive Experiences Study

Michael S. Simon, Jeannette F. Korczak, Cecilia L. Yee, Kathleen E. Malone, Giske Ursin, Leslie Bernstein, Jill A. McDonald, Dennis Deapen, Brian L. Strom, Michael F. Press, Polly A. Marchbanks, Ronald T. Burkman, Linda K. Weiss, Ann G. Schwartz

From the Division of Hematology and Oncology; Population Studies and Prevention Program; Breast Cancer Program, Karmanos Cancer Institute at Wayne State University, Detroit, MI; Fred Hutchinson Cancer Research Center, Division of Public Health Sciences; University of Washington, School of Public Health and Community Medicine; Department of Epidemiology, Seattle, WA; Department of Preventive Medicine, Keck School of Medicine of the University of Southern California, Los Angeles, CA; Division of Reproductive Health, Centers for Disease Control and Prevention, Atlanta, GA; Center for Clinical Epidemiology and Biostatistics and Department of Biostatistics and Epidemiology, University of Pennsylvania, Philadelphia, PA; Department of Obstetrics and Gynecology, Baystate Medical Center, Springfield, MA; National Cancer Institute, Bethesda, MD; and the Department of Nutrition, University of Oslo, Oslo, Norway

Address reprint requests to Michael S. Simon, MD, MPH, Barbara Ann Karmanos Cancer Institute, Room 4221 HWCRC, 4100 John R, Detroit MI 48201; e-mail: Simonm{at}karmanos.org

	ABSTRACT

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PURPOSE: Family history is a well-recognized risk factor for breast cancer. Familial aggregation and segregation analyses have estimated breast cancer risk based on family history primarily for white women; such information is limited for African American (AA) women. The purpose of this report is to update breast cancer risk estimates associated with a family history of breast cancer for white and AA women.

METHODS: We used family cancer history from 2,676 white and 1,525 AA women with breast cancer (probands) in the population-based National Institute of Child Health and Human Development's Women's Contraceptive and Reproductive Experiences (CARE) Study to estimate age-specific breast cancer risks in their first degree adult female relatives. Cumulative hazard curves were calculated for relatives of all probands using Cox proportional hazards models, and were stratified by the proband's race and age at diagnosis and number of relatives affected.

RESULTS: Breast cancer risks for white and AA women with a family history of the disease are similar through age 49 years, but diverge afterwards, with higher risks by age 79 in white women than in AA women (17.5% [SE, 0.9%] v 12.2% [SE, 1.1%]; P < .001). These risks increase as the number of affected first degree relatives increases, reaching 25.2% (SE, 3.4%) and 16.9% (SE, 4.0%) in white and AA women with more than one affected relative, respectively (P = .3).

CONCLUSION: We found age-related racial differences in breast cancer risk in women with a family history of breast cancer and have updated risk estimates for white and AA women for clinical use.

	INTRODUCTION

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In 2005, it is estimated that there were 211,240 new cases and 40,410 deaths from breast cancer in the United States, making it the most common cancer and the second leading cause of cancer deaths among women.¹ Overall, breast cancer is more common among white than African American (AA) women, except for women diagnosed at younger ages,² although mortality rates are higher among AA women.^2-4 These statistics highlight the importance of providing race-specific risk information to women at increased risk for breast cancer.

According to data from the Surveillance, Epidemiology and End Results (SEER) program from the mid-1990s, the average lifetime risk of breast cancer is 12.6%.⁵ Using data from the Breast Cancer Detection Demonstration Project, Gail et al computed lifetime breast risk estimates based on age, family history, prior biopsies, and reproductive history initially only for white women,^6,7 then later expanded to include AA women.⁸ Using data from the Cancer and Steroid Hormone (CASH) Study, Claus et al⁹ estimated lifetime breast cancer risks for white and AA women with a family history of breast cancer. However, these risks were based on data obtained in the early 1980s from a population that consisted of female relatives of index cases diagnosed between the ages 20 years and 54 years of whom only 10% (n = 490) were AA. From a genetic analysis of the CASH data based on white participants,¹⁰ Claus et al published lifetime breast cancer risk estimates based on the number and types of affected relatives and ages at diagnosis of those relatives.¹¹ It is not known how generalizable these risks are to AA women.

To update breast cancer risk estimates for both white and AA women with a family history of the disease, we analyzed information on the breast cancer history of first degree female relatives (FDRs; ie, mothers, sisters, and daughters) collected from index cases in the National Institute of Child Health and Human Development's Women's Contraceptive and Reproductive Experiences (CARE) study.¹² This population-based case-control study was conducted among women between 35 years and 64 years of age and oversampled AA women to permit sufficient numbers to address race-specific questions.

	METHODS

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Study Population and Data
The population for this analysis consists of adult ( 20 years of age) FDRs of participants with breast cancer in the National Institute of Child Health and Human Development's Women's CARE study.¹² Briefly, the Women's CARE study was carried out at five sites in the United States, four of which were affiliated with the National Cancer Institute (NCI; Bethesda, MD) SEER Program (Atlanta, GA; Detroit, MI; Los Angeles, CA; and Seattle/Puget Sound, WA), and an additional site, Philadelphia, PA. The study was approved by institutional review boards at each site.

CARE participants (probands), whose relatives were included in the present analysis, were white and AA women born in the United States, age 35 years to 64 years, who were newly diagnosed with invasive breast cancer between July 1994 and April 1998. Probands were ascertained by reviewing pathology reports, and/or tumor registry abstracts from hospitals, clinics, and pathology laboratories. In Philadelphia, case ascertainment was conducted by field center staff; at the other sites it was conducted with the SEER registry using rapid-reporting techniques. Younger and AA cases were oversampled to approximate a uniform age distribution across racial groups. Oversampling was done in order to obtain a distribution of patients that was as uniform as possible across age groups by races. CARE probands included 4,575 of 5,982 eligible newly diagnosed breast cancer cases (76.5%).

Family cancer history for first degree relatives was obtained during in-person interviews of the probands. Data collected included history of any cancer, age at cancer diagnosis, and current age or age at death.¹³ Diagnoses of cancer in relatives were not validated. We used family history information only from probands for whom breast cancer was the first cancer diagnosed (excluded 283 who had a prior history of another cancer), whose family history included at least one biologic FDR (excluded 17 adopted probands who had no information on relatives), and whose family history questionnaires were rated by the interviewer as satisfactory quality (excluded 74 of unsatisfactory quality). Of the 4,575 CARE probands, data provided by 4,201 (2,676 white and 1,525 AA) were included in our analysis.

Statistical Methods
Using data from the FDRs of the probands, we conducted a survival analysis to estimate the lifetime probability of developing breast cancer, considering age at diagnosis of the proband, number of relatives with breast cancer, and race. We estimated age-specific breast cancer risks at 5- or 10-year reference ages using Cox proportional hazards models as implemented in SAS PROC PHREG, version 8.2 (2001, SAS Institute I, Cary, NC).¹⁴

While the probands did not contribute to the sample in the risk computation, they represent part of the family history of each relative. We excluded from the analysis any FDRs whose breast cancer status was unknown, unaffected relatives whose current age or age at death was unknown, and affected relatives whose age at breast cancer diagnosis was unknown (1% for white and 1.5% for AA). Though the relatives with unknown age at diagnosis were omitted from the analysis, (five white and 20 AA) they still contributed to the family history, similar to the probands.

The Cox proportional hazards model assumes that the hazard for any individual is a fixed proportion of the hazard for any other individual, without having to specify an underlying distribution for the baseline hazard function, and it also allows adjustment for the correlation between relatives within a family via the COVSANDWICH option.¹⁴ The observed event time for the affected relatives, is their age at diagnosis, whereas for unaffected relatives, the observed censored time is their age at the proband's interview date, if alive, or their age at death. Event times were coded in 5- or 10-year intervals, where some events, namely breast cancer diagnoses, fell within the same time interval (ie, they were tied). To facilitate the calculation of the partial likelihood functions in the hazard equation, which assumes only one event in each time interval, we used the Efron method to resolve ties. This estimation method satisfactorily approximates the more accurate, but computationally intensive, exact method.¹⁴

Initially, Cox proportional hazards regression was performed by pooling all FDRs with these covariates: proband's race (white v AA), number of FDRs, including the proband with breast cancer (> 1 v 1), and age at cancer onset of the proband (< 45 years or 45 years). All covariates were significant predictors (P < .001) with hazard ratios of 1.43, 1.73, and 1.49, respectively. Subsequent Cox proportional hazards regression analyses were performed after stratifying by one or more of the above covariates to obtain subgroup-specific breast cancer risks at 5- or 10-year reference ages. To determine whether pairs of corresponding cumulative risks for race, age at proband's diagnosis, and number of affected relatives in the same age intervals were statistically different at the = .05 level, we used large sample, two-sided Z-tests, and Welch-Satterthwaite t-tests, estimating the variance of the mean difference of the pair of cumulative probabilities under the assumption of unequal variances.¹⁵

In the manner described by Claus et al,¹¹ these age-specific risks can be used to calculate the conditional probability of breast cancer, z, up to a specific age, y, for a woman who has not yet been diagnosed with breast cancer as of her current age, x, for y > x. Using the cumulative probabilities of developing breast cancer up to the age intervals that include x and y, namely R(x) and R(y), respectively, the conditional risk of breast cancer to age y for that woman is given by equation 1:

	RESULTS

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The distribution of FDRs of CARE probands according to their number of FDRs with breast cancer (including the proband), is similar for white and AA women, with approximately 90% of relatives having only one affected FDR (namely the proband; Table 1). Overall, cumulative risks of breast cancer for women with at least one affected FDR are higher for white than AA women, with lifetime ( 80 years) risks reaching 22.4% (SE, 1.2%) and 14.5% (SE,1.5%), respectively (P = .0002; Table 2 and Fig 1). These risk estimates are similar for white and AA women before age 40; however after age 40, the cumulative risks diverge by race, with greater breast cancer risk seen among white than AA women.

View larger version (14K): [in this window] [in a new window]   Fig 1. Cumulative risk of breast cancer in first degree female relatives of the Women's Contraceptive and Reproductive Experiences probands, by race and number of affected first degree female relatives.

Cumulative breast cancer risks in the FDRs stratified by age at diagnosis and race of the proband and the number of affected FDRs, are presented in 10-year, rather than 5-year age intervals because fewer data are available, especially for the analysis of relatives of CARE probands diagnosed before age 45 years, where only 73 AA and 151 white FDRs were reported to have breast cancer (Table 3). As before, cumulative risks are generally higher for white than AA women. (Table 3 and Figs 2 and 3). For relatives of probands diagnosed at 45 years or older, the cumulative breast cancer risks to ages 70 or older are 17.1% (SE, 0.9%) and 10.3% (SE, 1.0%) for white and AA women, respectively (P < .0001). For relatives of probands diagnosed before age 45, the corresponding risks are 18.5% (SE, 1.9%) and 13.9% (SE, 2.3%) for white and AA women, respectively (P = .12).

View larger version (12K): [in this window] [in a new window]   Fig 2. Cumulative risk of breast cancer in first degree female relatives of the Women's Contraceptive and Reproductive Experiences probands diagnosed at 45 years of age or older, by race and number of affected first degree female relatives.

View larger version (13K): [in this window] [in a new window]   Fig 3. Cumulative risk of breast cancer in first degree female relatives of the Women's Contraceptive and Reproductive Experiences probands diagnosed before 45 years of age, by race and number of affected first degree female relatives.

Equation 1 can be applied to the cumulative risk of breast cancer listed in Tables 2 and 3 to determine the chance that a woman, who has not yet been diagnosed with breast cancer, will be diagnosed at some specified future age, given information about her race and family history. The results of these calculations are presented in Table 4 for unaffected FDRs of white and AA probands, without consideration of age at diagnosis of the proband or number of affected relatives in the family (Table 2, column 4). For example, for white women the risks range from 2.3% to 17.9% that an unaffected woman who is currently 50 to 54 will be diagnosed with breast cancer between the ages of 55 and 59 and at 80 years and older, respectively. Corresponding risks for AA women range from 1.0% to 10.7%. In contrast, if the proband was diagnosed before 45 and the family has more than one affected relative, equation 1 and the cumulative risks in Table 3, column 6 can be used to estimate that an unaffected white woman who is currently age 50 to 59 has a risk of 30.4% of developing breast cancer at 70 years and older (data not shown). For a similarly unaffected AA this risk is 12.4%.

	DISCUSSION

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The increases in breast cancer risk over time shown here may be partially a real increase in incidence or may also be due to increased detection associated with increased mammography screening. The older age distribution of CARE versus CASH probands likely provided a larger proportion of older relatives and therefore may reflect a more precise estimate of lifetime breast cancer risk. In addition, the larger sample size of AA probands in the CARE (1,525) versus the CASH study (490) provides better estimates of risk among AA women with family history of breast cancer than previously reported.^9,16

The results of our analysis show that lifetime breast cancer risks are higher for white than AA women with a family history of breast cancer with divergences in risk beginning after age 40. For younger ages, risks are comparable or slightly higher for AA than white women. These findings parallel those of Claus et al^9,16 and are also consistent with SEER data.² Possible explanations for this observed racial crossover in breast cancer rates includes age related differences in childbearing and/or other risk factor patterns^17,18 and other socio-cultural influences.¹⁹ As expected, breast cancer risk tends to be higher for women with more than one versus one affected FDR for both AA and white women. Also as expected, breast cancer risk is higher for FDRs of probands diagnosed before, rather than at or older than, age 45 years. However, these differences were only statistically significant for white women, probably because of smaller numbers of AA women in the different strata.

As presented in Table 4, when counseling an unaffected woman regarding her future risk of breast cancer, the clinician should consider her family history as well as the fact that she has lived to her current age without developing breast cancer. For example, for unaffected white women with one or more FDRs with breast cancer, the conditional lifetime risk of breast cancer decreases from 22.3% for a woman younger than age 30, to 6.0% for a woman in the 75 to 79 age group and who is cancer free (Table 4). Comparable risks for unaffected AA women in the same age intervals are lower and decrease from 14.5% to 2.7% (Table 4). The risk of breast cancer for an unaffected counselee can be further refined considering the number of her affected relatives and their age(s) at diagnosis, in addition to the counselee's current age, through the application of equation 1 to the data presented in Table 3.

One limitation of our analysis is the possibility of misreported or underreported family cancer history. Although the family history data were nearly complete for FDRs of probands of both races, we were not able to validate the diagnoses of cancer in the relatives. However, other studies have shown that the amount of misreporting is expected to be relatively low for breast cancer compared with other primary sites.^20,21 Because the CARE family history questionnaire did not specifically distinguish between in situ versus invasive cancer, it is also possible that probands overreported diagnoses of cancer in their relatives by including diagnoses of both in situ and invasive cancers. To assess whether the extent of misreporting may have differed between AA and white CARE participants, we compared invasive breast cancer rates for FDRs of CARE controls to population rates derived from the SEER program (1975 to 1998). Race-specific breast cancer risk estimates for FDRs of both white and AA CARE controls were only slightly less than the population-based risk estimates derived from SEER (data not shown). There were, however, no apparent racial differences between CARE and SEER results indicating that the degree of misreporting is likely to be similar for both racial groups.

In conclusion, the most accurate prediction of breast cancer risk is made from population-based studies which provide risk estimates based on reported family cancer history. Given the wide disparity in breast cancer risk and mortality between women of different racial and ethnic backgrounds, it is important for the clinician to provide racially- and/or ethnically-specific risk information. These updated estimates of breast cancer risk should be useful to health care professionals who provide counseling to women with a family history of breast cancer.

	Authors' Disclosures of Potential Conflicts of Interest

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The authors indicated no potential conflicts of interest.

	Author Contributions

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Conception and design: Michael S. Simon, Jeannette F. Korczak, Cecilia L. Yee, Kathleen E. Malone, Giske Ursin, Leslie Bernstein, Jill A. McDonald, Dennis Deapen, Polly A. Marchbanks, Linda K. Weiss Financial support: Ann G. Schwartz Administrative support: Jeannette F. Korczak, Leslie Bernstein, Jill A. McDonald, Dennis Deapen, Polly A. Marchbanks, Linda K. Weiss, Ann G. Schwartz Provision of study materials or patients: Michael S. Simon, Kathleen E. Malone, Giske Ursin, Leslie Bernstein, Jill A. McDonald, Dennis Deapen, Brian L. Strom, Ronald T. Burkman, Linda K. Weiss Collection and assembly of data: Michael S. Simon, Kathleen E. Malone, Giske Ursin, Leslie Bernstein, Jill A. McDonald, Dennis Deapen, Brian L. Strom, Linda K. Weiss Data analysis and interpretation: Michael S. Simon, Jeannette F. Korczak, Cecilia L. Yee, Kathleen E. Malone, Giske Ursin, Leslie Bernstein, Jill A. McDonald, Dennis Deapen, Brian L. Strom, Michael F. Press, Polly A. Marchbanks, Ronald T. Burkman, Ann G. Schwartz Manuscript writing: Michael S. Simon, Jeannette F. Korczak, Cecilia L. Yee, Kathleen E. Malone, Giske Ursin, Leslie Bernstein, Jill A. McDonald, Dennis Deapen, Brian L. Strom, Michael F. Press, Polly A. Marchbanks, Ronald T. Burkman, Linda K. Weiss, Ann G. Schwartz Final approval of manuscript: Michael S. Simon, Jeannette F. Korczak, Cecilia L. Yee, Kathleen E. Malone, Giske Ursin, Leslie Bernstein, Jill A. McDonald, Dennis Deapen, Brian L. Strom, Michael F. Press, Polly A. Marchbanks, Ronald T. Burkman, Linda K. Weiss, Ann G. Schwartz

 

	NOTES

 
Supported by the National Institute of Child Health and Human Development with additional support through National Cancer Institute (Bethesda, MD) contract CN65064, the Michigan Health Care Education and Research Foundation, and institutional funds from the Karmanos Cancer Institute Population Studies and Prevention Program.

Presented in part at the 40th Annual Meeting of the American Society of Clinical Oncology, New Orleans, LA, June 5-8, 2004.

Authors' disclosures of potential conflicts of interest and author contributions are found at the end of this article.

	REFERENCES

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Submitted September 1, 2005; accepted March 9, 2006.

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