Risk Factors for Fatal Breast Cancer in African-American Women and White Women in a Large US Prospective Cohort

Marjorie L. McCullough, Heather Spencer Feigelson, W. Ryan Diver, Alpa V. Patel, Michael J. Thun and Eugenia E. Calle

From the Department of Epidemiology and Surveillance Research, American Cancer Society, Atlanta, GA

Correspondence to Dr. Marjorie McCullough, Department of Epidemiology and Surveillance Research, American Cancer Society, 1599 Clifton Road, NE, Atlanta, GA 30329-4251 (e-mail: marji.mccullough{at}cancer.org).

Received for publication March 28, 2005. Accepted for publication June 1, 2005.


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
African-American women have a higher lifetime risk of fatal breast cancer than do White women. Recent studies suggest that breast cancer risk factors may vary by race. The authors examined risk factors for fatal breast cancer in postmenopausal African-American women and White women in a large US prospective cohort. In 1982, 21,143 African-American women and 409,093 White women in the Cancer Prevention Study II completed a questionnaire on reproductive, medical, anthropometric, and demographic factors. During a 20-year follow-up, 257 deaths from breast cancer occurred among African-American women and 4,265 among Whites. Cox proportional hazards modeling was used to calculate multivariate-adjusted rate ratios, stratified by race. Higher body mass index, taller height, and physical inactivity were associated with increased breast cancer mortality rates in both groups. A college education was associated with higher mortality from breast cancer only in Africa-American women (hazard ratio = 1.62, 95% confidence interval: 1.13, 2.30; ptrend = 0.01, vs. less than a high school education). Most other risk factors were associated with breast cancer rates similarly in both groups. With few exceptions, established breast cancer risk factors were similarly associated with risk of death from breast cancer among African-American women and White women.

African Americans; body mass index; breast neoplasms; cohort studies; education; exercise; reproductive behavior; risk factors


Abbreviations: CI, confidence interval; HR, hazard ratio


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Breast cancer is the most commonly diagnosed cancer in both African-American women and White women in the United States (1Go), but prominent racial disparities are evident in both breast cancer incidence and mortality (2Go). African-American women have a lower lifetime risk of developing breast cancer but a higher lifetime risk of dying from breast cancer, compared with White women (3Go). Breast cancer death rates in African-American women surpassed those of White women beginning around 1980 (4Go) and, although death rates in both groups have been declining, the age-standardized rate in African-American women was 30 percent higher than in Whites in 2001 (2Go).

This disparity may have sociodemographic and/or biologic roots. Wojcik et al. (5Go) found that, among African-American women who were beneficiaries in the Department of Defense health-care system, death rates were closer to those of White women nationwide, suggesting that differences in access to care probably contribute to differences in survival. A recent report found that physicians treating African-American patients may be less well trained clinically and have less access to important clinical resources than do physicians treating White patients (6Go). African-American women also differ from White women in risk factor profiles (7Go), having a younger age at menarche, higher levels of obesity, and less physical activity. African-American women also present with later stage at diagnosis, more estrogen-receptor–negative tumors (8Go), and more aggressive tumors than do White women (9Go, 10Go), characteristics that have also been associated with lower socioeconomic status in both African-American women and White women (11Go). Poorer breast cancer prognosis among African-American women has also been linked to specific mutations (12Go) and cell-cycle defects (13Go).

Relatively few studies have examined risk factors for breast cancer separately in African-American women, and the literature addresses primarily the risk of breast cancer incidence rather than mortality. However, because known risk factors for incident breast cancer are also associated with breast cancer mortality (14Go–16Go), there should be considerable overlap. A 1996 review of the literature, based on five case-control studies, concluded that associations for both established and probable breast cancer risk factors are similar in African-American women and White women, and that lower survival among African-American women is likely due to later stage at diagnosis (17Go). In an analysis of data from the Multiethnic Cohort (18Go), breast cancer risk was similar in both African-American women and White women after control for known risk factors.

Eight case-control analyses (19Go–26Go) published after the 1996 review are less consistent; two of these observed no association between body mass index and postmenopausal breast cancer risk in African-American women (19Go, 26Go). Only one published prospective study has examined breast cancer risk factors among African-American women (27Go). After 4 years of follow-up in the Black Women's Health Study, African-American women over age 45 years who had their first child after age 30 years were not at higher breast cancer risk compared with those whose age at first birth was less than 20 years, but high parity (among parous women) was associated with lower risk. Conversely, later age at first birth and higher parity were associated with higher breast cancer risk among African-American women aged less than 45 years (27Go).

The purpose of this study was to evaluate the relation between anthropometric, reproductive, and lifestyle breast cancer risk factors and fatal breast cancer among African-American women in a prospective cohort study. We focused our analysis on postmenopausal breast cancer because of the small number of premenopausal African-American women in the cohort. We included analyses of the same risk factors in White women in this cohort for comparison purposes.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Study cohort and follow-up
Women in the analysis were drawn from the 676,253 women of the American Cancer Society's Cancer Prevention Study II, a prospective mortality study of approximately 1.2 million US men and women begun in 1982 (28Go). Participants were recruited and enrolled by American Cancer Society volunteers in all 50 US states, the District of Columbia, and Puerto Rico and were followed for vital status through December 31, 2002, as previously described (29Go). Subjects completed a confidential four-page questionnaire in 1982 that included questions on demographic characteristics, height and weight, personal and family history of cancer and other diseases, reproductive history, estrogen replacement therapy, medication and vitamin use, physical activity, and a brief section on diet. We considered women to be "White" or "African American" if they selected "White" or "Black," respectively, from the following options: "White, Black, Oriental, Hispanic, and other." The Emory University School of Medicine Institutional Review Board approves all aspects of Cancer Prevention Study II.

We excluded participants from this analysis if they reported prevalent cancer other than nonmelanoma skin cancer at baseline (African-American women: n = 1,809; White women: n = 54,319); if they described themselves as "Hispanic," "Oriental," or "other"; or if information on race was missing (n = 14,718), if menopausal status was missing (African-American women: n = 1,710; White women: n = 12,767), or if the women were pre- or perimenopausal (African-American women: n = 8,550; White women: n = 151,169). The final analytical cohort consisted of 21,143 African-American women and 409,093 White women, among whom 257 and 4,265 deaths from breast cancer occurred, respectively.

The vital status of study participants was determined from the month of enrollment through December 31, 2002, using two approaches. American Cancer Society volunteers made personal inquiries in September 1984, 1986, and 1988 to determine whether their enrollees were alive or dead and to record the date and place of all deaths. Death certificates were then obtained from state health departments to verify the underlying cause of death. Automated linkage using the National Death Index was used to extend follow-up through December 31, 2002, and to identify deaths among 13,219 women (2 percent) lost to follow-up between 1982 and 1988. Details of the utility of the National Death Index for the ascertainment of participants in this study are given elsewhere (29Go). Death certificates or multiple cause-of-death codes were obtained for 98.5 percent of all women known to have died. The underlying cause of death from breast cancer was coded according to the International Classification of Diseases using Ninth Revision codes 174.0–175.9 through 1998 and Tenth Revision codes C50–50.9 through the year 2002 follow-up (30Go, 31Go).

Statistical analyses
Race-specific rates of breast cancer mortality were calculated by 5-year age intervals. In addition, age-standardized (to the entire study population), race-specific rates were calculated by risk factor and calendar year of follow-up. We examined several established risk factors for breast cancer separately among African-American women and White women, using Cox's proportional hazards modeling to calculate multivariate-adjusted hazard ratios (32Go). The time axis used was follow-up time since enrollment in 1982. Age adjustment was accomplished by stratifying on the exact year of age at enrollment within each Cox model.

The following self-reported variables assessed in 1982 were modeled categorically: height (centimeters: <160, 160–165, >165–170, >170, missing); body mass index (weight (kg)/height (m)2: <25, 25–<30, 30–<35, ≥35, missing); exercise at work or play (none/slight, moderate, heavy, missing); education (less than high school, high school, some college/trade, college graduate and beyond, missing); age at menarche (years: <12, 12, 13, ≥14, missing); age at menopause (years: <45, 45–49, 50–54, ≥55, menopausal but unknown age); history of physican-diagnosed breast cysts (yes/no); history of breast cancer in a mother or sister (yes/no); alcohol use (nondrinker, <1 drink/day, ≥1 drink/day, unknown or missing); and estrogen replacement therapy (never, ever, unknown or missing). We examined age at first livebirth (years: <20, 20–24, 25–29, ≥30) and number of livebirths (n = 1, 2, 3, ≥4) among parous women only, and we controlled each variable for the other in multivariate models. In the remainder of the multivariate models that included nulliparous women, we controlled for parity using a binary variable (nulliparous/parous). Because of the high percentage of missing data for alcohol and because only 4 percent of African-American women reported consuming one or more drinks per day, we did not include the association with alcohol independently, but this variable remained as a covariate in multivariate models. We evaluated the potential for confounding by vegetable, fruit, whole grain, and red and processed meat consumption, as assessed on the baseline questionnaire as follows: "On average, how many days per week do you eat the following foods?". As control for these diet variables did not change the overall findings materially, the diet variables are not included in the final multivariate models. All reported p values are two sided.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
The median age of death from breast cancer in African-American women and White women was 72.6 and 73.7 years, respectively. Postmenopausal breast cancer death rates were higher in African-American women than in White women in every 5-year age group (figure 1). The overall age-standardized mortality rates in African-American women and White women in the cohort were 63.6 and 49.3 per 100,000 person-years, respectively.



View larger version (15K):
[in this window]
[in a new window]
 
FIGURE 1. Age- and race-specific death rates from breast cancer by 5-year age groups, Cancer Prevention Study II, 1982–2002. Vertical lines denote 95% confidence intervals. AA, African American.

 
Table 1 provides the distribution of risk factors and baseline characteristics by race in the cohort. There was no difference in height distribution between groups; however, African-American women were heavier than White women were. Sixty percent of White women, but only 33 percent of African-American women, had a body mass index of less than 25 at baseline. More African-American women (34 percent) than White women (16 percent) had less than a high school education; a slightly higher percentage of African-American women in the cohort had a college degree or beyond, compared with White women. Some reproductive characteristics also differed by race. African-American women were more likely to be nulliparous, to report four or more livebirths, or to have their first child at younger ages compared with White women. More White women reported a history of breast cysts and family history of breast cancer. Fewer African-American women reported drinking alcohol or using estrogen replacement therapy, but the percentage of missing data was higher in this group than among White women. African-American women also reported lower intakes of vegetables, citrus fruit, and whole grains; intakes of red and processed meat were similar by race.


View this table:
[in this window]
[in a new window]
 
TABLE 1. Distribution of baseline characteristics and risk factors by race, Cancer Prevention Study II cohort, 1982–2002

 
Most risk factors for fatal breast cancer showed similar patterns of association in African-American women and White women (table 2). For some variables, including height, body mass index, history of breast cyst, family history of breast cancer, and age at first livebirth, the association with breast cancer was statistically significant only among White women, reflecting their much larger sample size. For example, the point estimate associated with a height of greater than 170 cm was similar in African-American women (hazard ratio (HR) = 1.27, 95 percent confidence interval (CI): 0.84, 1.90; ptrend = 0.09) and White women (HR = 1.29, 95 percent CI: 1.17, 1.42; ptrend < 0.0001), but the association was statistically significant only in Whites. Body mass index was positively associated with fatal breast cancer in both African-American women and White women, but the association was weaker among African-American women. African-American women were at lower risk of breast cancer if they were physically active ("heavy" exercise vs. none or slight: HR = 0.70, 95 percent CI: 0.42, 1.16; ptrend = 0.04), a finding consistent with, but stronger than, that for White women (HR = 0.91, 95 percent CI: 0.79, 1.04; ptrend = 0.05), although the confidence intervals widely overlap. Ever having a child was associated with lower risk in both groups, but a linear reduction in risk with increasing number of livebirths among parous women was seen only in White women.


View this table:
[in this window]
[in a new window]
 
TABLE 2. Hazard ratios and 95% confidence intervals for fatal breast cancer in African-American women and White women, Cancer Prevention Study II cohort, 1982–2002

 
Breast cancer risk varied most notably by race for education. Higher educational attainment was associated with increased risk only among African-American women (for college education or higher relative to less than high school education: HR = 1.62, 95 percent CI: 1.13, 2.30; ptrend = 0.01). This association was unchanged when spousal education or geographic location was added to the multivariate models. Interestingly, the educational level of the spouse was not related to higher risk among African-American women (HR = 0.95, 95 percent CI: 0.54, 1.67) (not shown). College-educated women of both races were older when they had their first child, and they had fewer children overall, compared with less educated women. However, fewer college-educated, African-American women had three (14 percent) or four (14 percent) livebirths compared with White women (23 percent and 21 percent, respectively). Within race, the difference between the percentage of college-educated women and those with less than a high school education who had four or more children was more striking among African Americans (14 percent vs. 40 percent, respectively) than among Whites (21 percent vs. 29 percent, respectively). The positive association between education and breast cancer mortality among African-American women persisted after control for parity, whether as a binary variable or as a combined variable including age at first birth and number of children, or using separate terms among parous women only.

Older age at first livebirth was statistically significantly associated only with greater risk of fatal breast cancer among White women. The age-adjusted hazard ratio among African-American women was 1.44 (95 percent CI: 0.86, 2.41; ptrend = 0.09); however, after adjustment for other risk factors, particularly the number of livebirths and education, the association was attenuated (HR = 1.13, 95 percent CI: 0.65, 1.98; ptrend = 0.64). Later age at menarche was inversely associated with risk of breast cancer in White women (HR = 0.86, 95 percent CI: 0.78, 0.95; p = 0.002) but not African-American women (HR = 1.00, 95 percent CI: 0.69, 1.45), but confidence intervals were wide. Although age at menopause was similarly related to risk among both groups, there was a high percentage of missing data, especially among African-American women.

When we combined all women in the same age-adjusted model, the hazard ratio of fatal breast cancer among African-American women (as a main exposure) was 1.24 (95 percent CI: 1.10, 1.41; p = 0.0007), compared with White women. Adjustment for other measured breast cancer risk factors attenuated but did not eliminate the association (HR = 1.15, 95 percent CI: 1.01, 1.31; p = 0.03). However, race as an exposure did not meet the assumption for proportional hazards. Thus, emphasis should be placed on the stratified results. As illustrated in figure 2, breast cancer death rates were higher in African-American women than in White women in our cohort until the 1998–2002 time period, when mortality rates converged. The lower rates observed in both races in 1982–1987 reflect our exclusion of all preexisting cancers at baseline.



View larger version (15K):
[in this window]
[in a new window]
 
FIGURE 2. Age-standardized, race-specific death rates from breast cancer by calendar year, Cancer Prevention Study II, 1982–2002. Vertical lines denote 95% confidence intervals. AA, African American.

 

    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
In this large prospective US cohort, known risk factors for breast cancer incidence were generally related to breast cancer mortality similarly among White women and African-American women. Possible exceptions were a somewhat stronger association between body mass index and increased breast cancer risk in White women and a somewhat stronger inverse association between physical activity and breast cancer in African-American women. Completion of a college education was associated with a 60 percent higher risk of fatal breast cancer in African-American women relative to those with less than a high school education, even after controlling for reproductive risk factors, a finding not observed among White women. Parous women in both groups were at 20–30 percent lower risk compared with nulliparous women. However, contrary to findings in White women, older age at first livebirth was not significantly related to higher risk in African-American women, after controlling for number of births and education. Early age at menarche was positively associated with risk only among White women.

Body mass has been consistently associated with higher breast cancer risk in postmenopausal White women (33Go), but results from case-control studies of African-American women are inconsistent (19Go, 34Go). We observed higher risk of fatal breast cancer with increasing body mass index at baseline in both groups, but the association was stronger in White women, possibly because of the comparatively smaller sample size for African-American women.

Several explanations may account for the weaker associations between fatal breast cancer risk and body mass index in African-American women compared with White women in our study. First, African-American women with a body mass index of less than 25 (who comprised the referent group) had higher rates of fatal breast cancer compared with White women of normal weight (64 vs. 45 per 100,000) (table 1), possibly because of factors affecting medical care or the racial differences in circulating estrogen levels (35Go). Higher serum estrone concentrations have been observed in African-American women compared with White women, even after controlling for obesity (36Go). The increase in circulating estrogen levels with higher levels of obesity may not produce a linear increase in breast cancer risk in African-American women as has been reported in Whites (37Go). Second, African-American women have more estrogen receptor-negative tumors (9Go). Estrogen-mediated risk factors, including estrone synthesis in adipose tissue (38Go), may be less important for estrogen receptor-negative tumors (39Go). Finally, African-American women in our study were heavier than White women were and may also have had a higher body mass index during the premenopausal period when higher body mass is associated with lower subsequent risk of breast cancer (40Go).

The inverse association with physical activity in African-American women (23Go), along with the suggestion that physical activity was slightly more strongly related to lower breast cancer mortality among African-American women than White women (22Go), is consistent with limited data. In addition to its role in energy balance, physical activity is thought to lower breast cancer risk by influencing circulating hormone levels (22Go).

Educational attainment was the strongest risk factor observed in African-American women. Those who were college educated had a 60 percent higher risk of fatal breast cancer than did those with less than a high school education, a finding not observed among White women in our cohort. Two previous case-control studies reported higher breast cancer incidence associated with higher education (24Go, 41Go), even after controlling for age at first birth and number of births (24Go), while two others observed no association (26Go, 34Go). Interestingly, spousal education was not related to risk in our study.

Because our study was of breast cancer mortality, one may hypothesize that higher education would predict lower mortality, not greater, if it reflected better access to screening and health care. Our findings may also be due to unmeasured confounders among college-educated women (17Go) or residual confounding. For example, women in our study with higher education were taller and experienced menarche at an earlier age, regardless of race. Thus, higher education may capture a combination of reproductive and other risk factors that acts as a stronger predictor of risk than do individual factors. Nevertheless, this finding varied by race.

Reproductive factors affect breast cancer risk partly by modulating lifetime exposure to the mitogenic effects of estrogen. We observed a 20–30 percent statistically significant lower risk of fatal breast cancer in parous compared with nulliparous women of both races. However, among parous women, age at first birth and number of livebirths—both clearly related to risk among White women—were not clearly related to risk of postmenopausal breast cancer among African-American women. Later age at first birth was not related to increased breast cancer risk in African-American women, but having four or more births (vs. a single birth) was related to lower risk, controlling for age at first birth. This finding is similar to a recent report from the Black Women's Health Study cohort of breast cancer incidence (27Go). In that study, among African-American women over the age of 45 years, age at first birth was not related to risk, but the number of births was inversely related to risk; opposite patterns were observed in women aged less than 45 years of age (27Go). Previous case-control studies have been equivocal, with some reporting increased breast cancer risk with later age at first birth in African-American women (34Go, 42Go–44Go), while others observed no association (21Go, 24Go, 26Go, 27Go). Likewise, having multiple births has been inversely associated with risk in three case-control studies of postmenopausal breast cancer in African-American women (21Go, 26Go, 34Go) but not in another (45Go). Although later age at menopause was similarly related to risk in both groups, later age at menarche was associated with lower risk only in White women, a finding not inconsistent with the literature (24Go, 34Go, 45Go).

Most epidemiologic studies of breast cancer risk factors pertain almost exclusively to White women; risk factors are assumed to be similar across racial groups. In the Cancer Prevention Study II cohort, being African American is associated with higher risk of death from breast cancer after controlling for other measured risk factors (rate ratio = 1.15; p = 0.03). Even though our analysis controlled for most established breast cancer risk factors, we could not control for tumor characteristics associated with poor prognosis (8Go), screening behavior, or quality of health care.

Breast cancer mortality rates in African-American women in our cohort decreased over time and approached rates of White women by the end of follow-up in 2002. This is promising, because it suggests that the disparity in death rates by race in our cohort has diminished over time. The explanation for this phenomenon is unclear. It may be a chance finding, as the confidence interval around the death rate in African-American women for the most recent calendar period is wide, or it may reflect a shift toward greater screening and earlier diagnosis in our African-American women over time.

The strengths of this study include its prospective design and information on several important breast cancer risk factors. The follow-up of African-American women for breast cancer death is larger (in person-years) than in any other cohort. The limitations of our study were that we did not have information on breast cancer incidence, which would have allowed us to distinguish factors associated with incidence from those associated with survival. We had no information on access to health care, mammography screening, or treatment. Risk factors were assessed only at baseline in 1982; thus, misclassification of time-dependent risk factors, such as physical activity, body mass index, and hormone replacement therapy use, over the 20-year follow-up may attenuate associations.

In conclusion, established breast cancer risk factors associated with energy balance and estrogen metabolism generally influenced the risk of postmenopausal breast cancer similarly in both African-American women and White women. Our observation of an elevated risk of fatal breast cancer among African-American women with higher education deserves further study. Education may represent a combination of lifestyle factors closely tied with reproductive patterns that we are unable to fully control in our study. Our findings support health messages aimed at improving modifiable risk factor profiles in both African-American women and White women, including maintenance of ideal body weight and increased physical activity to reduce risk of breast cancer mortality.


    ACKNOWLEDGMENTS
 
Conflict of interest: none declared.


    References
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

  1. Jemal A, Murray T, Ward E, et al. Cancer statistics, 2005. CA Cancer J Clin 2005;55:10–30.[Abstract/Free Full Text]
  2. American Cancer Society. Cancer facts & figures for African Americans 2005–2006. Atlanta, GA: American Cancer Society, 2005.
  3. Ries LAG, Eisner MP, Kosary CL, et al. SEER cancer statistics review. Bethesda, MD: National Cancer Institute, 2004.
  4. American Cancer Society. Breast cancer facts & figures 2003–2004. Atlanta, GA: American Cancer Society, 2003.
  5. Wojcik BE, Spinks MK, Optenberg SA. Breast carcinoma survival analysis for African American and white women in an equal-access health care system. Cancer 1998;82:1310–18.[CrossRef][ISI][Medline]
  6. Bach PB, Pham HH, Schrag D, et al. Primary care physicians who treat blacks and whites. N Engl J Med 2004;351:575–84.[Abstract/Free Full Text]
  7. Bernstein L, Teal CR, Joslyn S, et al. Ethnicity-related variation in breast cancer risk factors. Cancer 2003;97:222–9.[CrossRef][Medline]
  8. Chlebowski RT, Chen Z, Anderson GL, et al. Ethnicity and breast cancer: factors influencing differences in incidence and outcome. J Natl Cancer Inst 2005;97:439–48.[Abstract/Free Full Text]
  9. Coates RJ, Bransfield DD, Wesley M, et al. Differences between black and white women with breast cancer in time from symptom recognition to medical consultation. J Natl Cancer Inst 1992;84:938–50.[Abstract]
  10. American Cancer Society. Cancer facts & figures for African Americans 2003–2004. Atlanta, GA: American Cancer Society, 2003.
  11. Wells BL, Horm JW. Stage at diagnosis in breast cancer: race and socioeconomic factors. Am J Public Health 1992;82:1383–5.[Abstract]
  12. Jones BA, Kasl SV, Howe CL, et al. African-American/white differences in breast carcinoma: p53 alterations and other tumor characteristics. Cancer 2004;101:1293–301.[CrossRef][ISI][Medline]
  13. Porter PL, Lund MJ, Lin MG, et al. Racial differences in the expression of cell cycle-regulatory proteins in breast cancer. Cancer 2004;100:2533–42.[CrossRef][ISI][Medline]
  14. Feigelson HS, Calle EE, Robertson AS, et al. Alcohol consumption increases the risk of fatal breast cancer. Cancer Causes Control 2001;12:895–902.[CrossRef][ISI][Medline]
  15. Petrelli JM, Calle EE, Rodriguez C, et al. Body mass index, height, and postmenopausal breast cancer mortality in a prospective cohort of US women. Cancer Causes Control 2002;13:325–32.[CrossRef][ISI][Medline]
  16. Calle EE, Martin LM, Thun MJ, et al. Family history, age, and risk of fatal breast cancer. Am J Epidemiol 1993;138:675–81.[Abstract]
  17. Trock BJ. Breast cancer in African American women: epidemiology and tumor biology. Breast Cancer Res Treat 1996;40:11–24.[CrossRef][ISI][Medline]
  18. Pike MC, Kolonel LN, Henderson BE, et al. Breast cancer in a multiethnic cohort in Hawaii and Los Angeles: risk factor-adjusted incidence in Japanese equals and in Hawaiians exceeds that in whites. Cancer Epidemiol Biomarkers Prev 2002;11:795–800.[Abstract/Free Full Text]
  19. Hall IJ, Newman B, Millikan RC, et al. Body size and breast cancer risk in Black women and White women. Am J Epidemiol 2000;151:754–64.[Abstract]
  20. Palmer JR, Rao RS, Adams-Campbell LL, et al. Height and breast cancer risk: results from the Black Women's Health Study (United States). Cancer Causes Control 2001;12:343–8.[CrossRef][ISI][Medline]
  21. Ursin G, Bernstein L, Wang Y, et al. Reproductive factors and risk of breast carcinoma in a study of white and African-American women. Cancer 2004;101:353–62.[CrossRef][ISI][Medline]
  22. John EM, Horn-Ross PL, Koo J. Lifetime physical activity and breast cancer risk in a multiethnic population: the San Francisco Bay Area Breast Cancer Study. Cancer Epidemiol Biomarkers Prev 2003;12:1143–52.[Abstract/Free Full Text]
  23. Adams-Campbell LL, Rosenberg L, Sowmya Rao R, et al. Strenuous physical activity and breast cancer risk in African-American women. J Natl Med Assoc 2001;93:267–75.[ISI][Medline]
  24. Brinton LA, Benichou J, Gammon MD, et al. Ethnicity and variation in breast cancer incidence. Int J Cancer 1997;73:349–55.[CrossRef][ISI][Medline]
  25. Kinney AY, Millikan RC, Lin YH, et al. Alcohol consumption and breast cancer among black and white women in North Carolina. Cancer Causes Control 2000;11:345–57.[CrossRef][ISI][Medline]
  26. Hall IJ, Moorman PG, Millikan RC, et al. Comparative analysis of breast cancer risk factors among African-American women and White women. Am J Epidemiol 2005;161:40–51.[Abstract/Free Full Text]
  27. Palmer JR, Wise LA, Horton NJ, et al. Dual effect of parity on breast cancer risk in African-American women. J Natl Cancer Inst 2003;95:478–83.[Abstract/Free Full Text]
  28. Thun MJ, Calle EE, Rodriguez C, et al. Epidemiological research at the American Cancer Society. Cancer Epidemiol Biomarkers Prev 2000;9:861–8.[Free Full Text]
  29. Calle EE, Terrell DD. Utility of the National Death Index for ascertainment of mortality among Cancer Prevention Study II participants. Am J Epidemiol 1993;137:235–41.[Abstract]
  30. World Health Organization. International classification of diseases, injuries, and causes of death. Based on recommendations of the 9th Revision conference, 1975, and adopted by the 29th World Health Assembly. Geneva, Switzerland: World Health Organization, 1977–1978.
  31. World Health Organization. International statistical classification of diseases and related health problems. Geneva, Switzerland: World Health Organization, 1992.
  32. Cox DR. Regression models and life-tables (with discussion). J R Stat Soc (B) 1972;34:187–220.[ISI]
  33. Calle EE, Kaaks R. Overweight, obesity and cancer: epidemiological evidence and proposed mechanisms. Nat Rev Cancer 2004;4:579–91.[CrossRef][ISI][Medline]
  34. Schatzkin A, Palmer JR, Rosenberg L, et al. Risk factors for breast cancer in black women. J Natl Cancer Inst 1987;78:213–17.[ISI][Medline]
  35. Taioli E, Garte SJ, Trachman J, et al. Ethnic differences in estrogen metabolism in healthy women. (Letter). J Natl Cancer Inst 1996;88:617.[Free Full Text]
  36. Richards RJ, Svec F, Bao W, et al. Steroid hormones during puberty: racial (black-white) differences in androstenedione and estradiol—the Bogalusa Heart Study. J Clin Endocrinol Metab 1992;75:624–31.[Abstract]
  37. Endogenous Hormones Breast Cancer Collaborative Group. Body mass index, serum sex hormones, and breast cancer risk in postmenopausal women. J Natl Cancer Inst 2003;95:1218–26.[Abstract/Free Full Text]
  38. Feigelson HS. Breast cancer: epidemiology and molecular endocrinology. In: Henderson BE, Ponder B, Ross RK, eds. Hormones, genes and cancer. New York, NY: Oxford University Press, 2003.
  39. Althuis MD, Fergenbaum JH, Garcia-Closas M, et al. Etiology of hormone receptor-defined breast cancer: a systematic review of the literature. Cancer Epidemiol Biomarkers Prev 2004;13:1558–68.[Abstract/Free Full Text]
  40. Potischman N, Swanson CA, Siiteri P, et al. Reversal of relation between body mass and endogenous estrogen concentrations with menopausal status. J Natl Cancer Inst 1996;88:756–8.[Free Full Text]
  41. Mayberry RM, Stoddard-Wright C. Breast cancer risk factors among Black women and White women: similarities and differences. Am J Epidemiol 1992;136:1445–56.[Abstract]
  42. MacMahon B, Cole P, Lin TM, et al. Age at first birth and breast cancer risk. Bull World Health Organ 1970;43:209–21.[ISI][Medline]
  43. Austin H, Cole P, Wynder E. Breast cancer in black American women. Int J Cancer 1979;24:541–4.[ISI][Medline]
  44. Mayberry RM. Age-specific patterns of association between breast cancer and risk factors in black women, ages 20 to 39 and 40 to 54. Ann Epidemiol 1994;4:205–13.[Medline]
  45. Laing AE, Demenais FM, Williams R, et al. Breast cancer risk factors in African American women: the Howard University Tumor Registry experience. J Natl Med Assoc 1993;85:931–9.[ISI][Medline]




This Article
Abstract
Full Text (PDF)
All Versions of this Article:
162/8/734    most recent
kwi278v1
Alert me when this article is cited
Alert me if a correction is posted
Services
Email this article to a friend
Similar articles in this journal
Similar articles in ISI Web of Science
Similar articles in PubMed
Alert me to new issues of the journal
Add to My Personal Archive
Download to citation manager
Disclaimer
Request Permissions
Google Scholar
Articles by McCullough, M. L.
Articles by Calle, E. E.
PubMed
PubMed Citation
Articles by McCullough, M. L.
Articles by Calle, E. E.