This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Li, C. I. Articles by Daling, J. R. Search for Related Content PubMed PubMed Citation Articles by Li, C. I. Articles by Daling, J. R.

Differences in Breast Cancer Hormone Receptor Status and Histology by Race and Ethnicity among Women 50 Years of Age and Older¹

Fred Hutchinson Cancer Research Center, Division of Public Health Sciences, Seattle, Washington 98109-1024

	Abstract

Top Abstract Introduction Materials and Methods Results Discussion References

 
Numerous studies have demonstrated differences in certain biological breast cancer characteristics associated with survival, including hormone receptor status and histology, among women of different racial and ethnic groups. However, women classified as "Asian or Pacific Islanders" or "Hispanic whites" represent heterogeneous populations, and few studies have separately evaluated subgroups of these populations with respect to these breast tumor characteristics. Using data obtained from 11 cancer registries that participate in the Surveillance, Epidemiology, and End Results (SEER) Program, the tumor characteristics of 93,317 women in whom invasive breast cancer was diagnosed from 1992 to 1998 were compared by race and ethnicity using unconditional and polytomous logistic regression. The study consisted of 75,978 non-Hispanic whites, 6,915 African Americans, 203 Native Americans, 5,750 Asians/Pacific Islanders, and 4,471 Hispanic whites. Eight Asian/Pacific Islander and four Hispanic white subgroups were also analyzed separately. Relative to non-Hispanic whites, African Americans, Native Americans, Filipinos, Chinese, Koreans, Vietnamese, Indians/Pakistanis, Mexicans, South/Central Americans, and Puerto Ricans living in the United States had 1.4- to 3.1-fold elevated risks of presenting with estrogen receptor-negative/progesterone receptor-negative breast cancer. Numerous differences by histological type, including lobular, ductal/lobular, mucinous, comedocarcinoma, tubular, and medullary histologies, were also observed by race/ethnicity. Breast cancer tumor characteristics differ by race/ethnicity in the United States. Both biological and lifestyle factors likely contribute to these findings. Our results may explain, to some extent, the differences in breast cancer stage and survival observed by race/ethnicity. Understanding the factors underlying these differences may provide further insight into breast cancer etiology in different populations.

	Introduction

Top Abstract Introduction Materials and Methods Results Discussion References

 
African American (1, 2, 3, 4, 5, 6) , Hispanic (1 , 2 , 6, 7, 8, 9) , Native American (7 , 10) , Hawaiian, and Filipino (1 , 11 , 12) women living in the United States are more likely to be diagnosed with advanced stages of breast cancer and to have poorer survival after diagnosis compared with non-Hispanic whites. Alternatively, Japanese and Chinese women have been shown either to be no different with respect to breast cancer stage and survival (1) or to actually present with less advanced stages and to have better survival compared with non-Hispanic whites (11 , 12) . Various explanations for these findings have been postulated including differences in sociodemographic, cultural, and behavioral characteristics. With respect to African Americans, some studies have shown that differences in insurance coverage and socioeconomic status (13 , 14) do not explain the observed differences in stage, whereas other studies find that, after adjusting for factors such as socioeconomic status, income, stage, and breast cancer treatments, differences in survival are no longer observed (15, 16, 17) .

These stage and survival differences may also be related to the differential expression of breast tumor characteristics that have been independently shown to be related to mortality. Specifically, hormone receptor-negative breast tumors (18, 19, 20) are associated with poorer survival, whereas tumors that have a lobular histology are associated with better survival (21) . Previous studies suggested that African Americans are more likely to have ER³ -negative, PR-negative (5 , 22) , and medullary (4 , 6) breast tumors, and less likely to have tumors with a lobular histology (23) . Whether or not Hispanic women are more likely to have ER-negative and PR-negative breast tumors remains unclear with one study showing that they do (6) and two others showing that they do not (22 , 24) . Overall, there are few studies that have explored the relationship between race/ethnicity and breast tumor characteristics, and those that have, have been limited by studying women living in single geographic regions, by their sample sizes, and in their abilities to assess women in different racial/ethnic subgroups.

Using data from 11 population-based tumor registries in the United States, we assessed the relationship between race/ethnicity, using 17 separate categories, and risk of invasive breast carcinoma by hormone receptor status and histological type among women 50 years of age and older.

	Materials and Methods

Top Abstract Introduction Materials and Methods Results Discussion References

 
Women 50 years of age and older with diagnoses of invasive breast cancer made between 1992 and 1998 were identified through 11 population-based cancer registries in the United States that participate in the National Cancer Institute’s SEER Program. The study was limited to women 50 years of age and older because hormone receptor status is known to differ by menopausal status (25) , and in the absence of information on menstrual history, 50 years of age has been shown to be a reasonable proxy for defining menopause (26) . The year 1992 was chosen as the starting point for this analysis because this was the year when two registries were added to the SEER program, those serving the urban areas surrounding Los Angeles and San Jose, California, both of which contain racially and ethnically diverse populations. The other SEER registries that were used include those serving the states of Connecticut, Hawaii, Iowa, New Mexico, and Utah and the urban areas surrounding Atlanta, Georgia; Detroit, Michigan; San Francisco-Oakland, California; and Seattle, Washington. The principal sources of data used by SEER are patients’ medical records. It is estimated that >95% of all incident cancer cases in the populations under surveillance are ascertained. Further operational details and methods used by the SEER program are provided elsewhere (27) .

A total of 95,523 women whose breast cancer diagnosis was their first primary cancer diagnosis of any type recorded at their registry were eligible for this study. Subjects were excluded if their cancer was diagnosed at autopsy (n = 33), if their race was classified as "other" (n = 159) or "unknown" (n = 611), or if their Hispanic ethnicity was classified as either "Spanish surname only" (meaning that the only evidence of a woman’s Hispanic origin was her surname or maiden name) or "unknown" (n = 1,360). In addition, to make our race/ethnicity categories mutually exclusive, 31 African American women, 1 Native American woman, and 11 Asians/Pacific Islanders who were also categorized as being Hispanic were excluded leaving a total of 93,317 subjects.

Our primary exposure of interest was race/ethnicity. Beginning in 1988, in addition to categorizing "race/ethnicity" as white, black, Native American/Alaskan Native, Chinese, Japanese, Filipino, and Hawaiian, SEER added categories for Koreans, Asian Indians/Pakistanis, and Vietnamese among others. Of the 5,750 Asian/Pacific Islanders included in this study, 127 were of less common Asian/Pacific Islander races, including Thai, Laotian, Tongan, and so forth; and 239 were classified as being other or NOS Asian/Pacific Islanders. These 366 women were grouped together and classified as other/NOS Asians/Pacific Islanders. In 1988, SEER also added information about "Spanish surname or origin" specifically coding whether individuals were Mexican, Puerto Rican, Cuban, South or Central American (except Brazil), other specified Spanish/Hispanic Origin (includes European), and Spanish/Hispanic NOS. We used these expanded categorizations in our analyses (although, because of the small number of Cubans (n = 117), we merged them with the 2,534 women of other/NOS Spanish/Hispanic origin). Given these categorizations, our study consisted of 75,978 non-Hispanic whites, 6,915 African Americans, 203 Native Americans, 5,750 Asians/Pacific Islanders, and 4,471 Hispanic whites.

In addition to age and year of diagnosis, SEER also provides information on: ER status, PR status, and histology. Moreover, information on the following tumor characteristics, which we evaluated as potential confounders or effect modifiers of the relationship between race/ethnicity and ER status, PR status, and histology, is available: American Joint Committee on Cancer (AJCC) stage, size, number of positive lymph nodes, number of lymph nodes examined, and tumor grade. In addition, surgical and radiation treatment information is available. Although information on marital status is provided, data regarding other sociodemographic factors such as income and health insurance status are not.

ORs were calculated as an estimate of the relative risk to evaluate the association between ER status, PR status, and histological type and different racial/ethnic groups. NonHispanic whites served as the reference group because they represented over 80% of our total study population. Using Stata 6.0 for Windows (Stata Corporation, College Station, TX) statistical software, unconditional logistic regression was performed to compute ORs and 95% CIs (28) and to evaluate the effects of confounding and modifying factors on the association between race/ethnicity and ER status and PR status. A factor was considered to be a confounder if it changed our estimates by more than 10%. None of the potential confounders or effect modifiers listed above were found to confound or modify the relationships that we assessed. In addition, histology was not a confounder of the relationships that we observed between hormone receptor status and race/ethnicity, and hormone receptor status was not a confounder of the relationship between histology and race/ethnicity. However, all analyses were adjusted for age at diagnosis (as a categorical variable), year at diagnosis (as a continuous variable), and SEER registry. Unconditional logistic regression was used to assess the association between race/ethnicity and ER status and PR status among women with a known hormone receptor status. Women whose hormone receptor status was classified as borderline, not assessed, or unknown were considered to have an unknown status. Polytomous logistic regression was used to evaluate the association between race/ethnicity and ER/PR status and histology. In these polytomous models the baseline categories used were ER-positive/PR-positive and ductal histology (defined using ICD-O code 8500), respectively. The other histologies that we assessed, were classified using ICD-O codes, as follows: lobular (8520), ductal-lobular (8522), mucinous (8480), comedocarcinoma (8501), adenocarcinoma (8140), tubular (8211 and 8201), and medullary (8510). These analyses were also adjusted for age at diagnosis, year at diagnosis, and SEER registry.

	Results

Top Abstract Introduction Materials and Methods Results Discussion References

 
Table 1 presents a comparison of various characteristics by race/ethnicity. Non-Hispanic white women tended to have later diagnosis ages compared with women of other races/ethnicities, although this may reflect the fact that the non-Hispanic white population is on average older than the other populations. African-American women most frequently came from the Atlanta, Detroit, and Los Angeles registries; Native Americans from New Mexico and Seattle/Puget Sound; Asian Americans/Pacific Islanders from Hawaii, Los Angeles, and San Francisco/Oakland; and Hispanic whites from Los Angeles and New Mexico. African Americans, Native Americans, and Hispanic whites were somewhat more likely to present with tumors that had a more advanced stage, were larger, and had more positive lymph nodes compared with non-Hispanic whites and Asians/Pacific Islanders. Of note, ER status was borderline, not assessed, or unknown for 19.3% of non-Hispanic whites, 28.5% of African Americans, 16.8% of Native Americans, 17.3% of Asians/Pacific Islanders, and 27.8% of Hispanic whites.

	Discussion

Top Abstract Introduction Materials and Methods Results Discussion References

Again, these studies were all limited in their ability to assess risk among different Asians/Pacific Islanders and Hispanic whites of different origins and in the geographic regions studied. Thus, in this study of women living in 11 geographic regions, we expand on what has been reported, i.e., that Native Americans, Filipinos, Chinese, Koreans, Vietnamese, Indians/Pakistanis, Mexicans, South/Central Americans, and Puerto Ricans (in addition to African Americans) living in the United States have elevated risks of being diagnosed with ER-negative/PR-negative tumors, which are tumors known to be associated with poorer survival (18, 19, 20) . Furthermore, we document differences with respect to histology, with African Americans, Native Americans, all Asian/Pacific Islander subtypes (except for Hawaiians and Indians/Pakistanis), and all Hispanic white subtypes (except for Puerto Ricans) having decreased risks of lobular carcinoma, which is a histological subtype that may be associated with a better prognosis (21) , than the most common histological type of breast cancer, ductal carcinoma. Overall, compared with non-Hispanic whites, differences were seen in at least five of the seven histological subtypes analyzed for African Americans, Filipinos, Chinese, Mexicans, and South/Central Americans.

A potential limitation of this study is that our exposure of interest, race/ethnicity, was determined via medical record reviews. However, information on race was classified as other or unknown, and ethnicity was classified as Spanish surname only or unknown, whether Spanish/Hispanic or not, for only 2130 women, representing 2.3% of the eligible study population. With respect to Asians/Pacific Islanders, only 239 women, representing 4.2% of this population, were classified as being of a NOS Asian/Pacific Islander race. An inability to categorize Hispanic whites into subgroups was a more important problem, because 2534 women, representing 56.7% of this population, were classified as being of an other or NOS Spanish/Hispanic origin. This inability to subcategorize the majority of Hispanic whites could bias our results with respect to these subgroups either toward or away from the null. Additionally, because we evaluated 17 different racial/ethnic groups and, hence, a large number of associations, some of the statistically significant relationships that we identified could have been attributable to chance.

Another limitation of this study was our lack of information regarding other factors that may be associated with hormone receptor status and histology. Specifically, data on hormonal, reproductive, anthropometric, and lifestyle factors were unavailable. These factors could contribute to the differences that we observed, because nulliparity/late age at first live birth, early age at menarche, and higher body mass indices have been associated with an increased risk of developing an ER-positive tumor, but a decreased risk of developing an ER-negative tumor (18 , 31, 32, 33) . However, with respect to hormone receptor status, these factors may not play an important role because a study evaluating the risk of ER-positive tumors among whites and blacks found that blacks were still more likely than whites to have ER-negative tumors even after adjusting for age, reproductive factors, body mass index, use of alcohol and tobacco, socioeconomic status, and health care access and use (29) .

An additional concern is that hormone receptor assays and the classifications of tumor histologies were not conducted in a centralized location. This, and the fact that, relative to the other groups, African Americans and Hispanic whites had greater proportions of unknown data with respect to hormone receptors status, may bias our results. However, with respect to the first issue, it is unlikely that different practices across institutions could entirely account for our findings, particularly because the study is limited to a finite recent time period in which hormone receptor assays have been routinely used in the assessment of breast carcinomas and in which, histological classifications of breast tumors have not undergone major revisions. What is also reassuring is that our distributions of hormone receptor status and histology are quite comparable with other published results with respect to non-Hispanic white, African-American, and Hispanic white women (22) .

In summary, our findings suggest that relative to non-Hispanic white women, women of certain races/ethnicities living in the United States, including African Americans, Native Americans, Filipinos, Chinese, Koreans, Vietnamese, Indians/Pakistanis, Mexicans, South/Central Americans, and Puerto Ricans, have greater risks of presenting with breast cancers the characteristics of which are associated with a poorer prognosis. A combination of biological, genetic, environmental, and lifestyle differences across these populations are likely to account for these variations. Thus, rather than an independent risk factor for particular hormone receptor profiles and histologies, race/ethnicity is more likely to be a marker for other risk factors associated with such outcomes. Nevertheless, it may be important to explore how the impact of breast cancer risk factors vary by race/ethnicity because some of these factors have been independently associated with breast cancers with certain hormone receptor expression profiles and histologies. For example, the use of hormone replacement therapy (HRT) is associated with an increased risk of tumors with a lobular histology (34 , 35) . Although it is known that the use of HRT is more common among non-Hispanic whites than it is among African American women, whether or not this difference alone could explain our results is uncertain. In addition, as others have also suggested (6) , findings such as ours may partly explain the more advanced stages and poorer survival experienced by different racial/ethnic groups, including African Americans, Native Americans, Mexicans, and Puerto Ricans. Although both hormone receptor status and histology may be fairly crude measures of biological differences of breast tumors across races/ethnicities, important differences were identified here that will hopefully encourage the research of how other biological factors, including genetic and molecular markers, may further explain the observed variations in stage and survival across races/ethnicities and provide greater insight into breast cancer etiology in different populations.

	Footnotes

 
The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ Supported by Contract N01 CN 05230 from the National Cancer Institute, NIH.

² To whom requests for reprints should be addressed, at Fred Hutchinson Cancer Research Center, Division of Public Health Sciences; 1100 Fairview Avenue North, MP 381, P. O. Box 19024, Seattle, Washington 98109-1024. Phone: (206) 667-4630; Fax: (206) 667-5948, E-mail: cili{at}fhcrc.org

³ The abbreviations used are: ER, estrogen receptor; PR, progesterone receptor; SEER, Surveillance, Epidemiology, and End Results (survey); NOS, not otherwise specified; OR odds ratio; CI, confidence interval; ICD-O, International Classification of Diseases for Oncology.

Received 8/24/01; revised 3/22/02; accepted 4/ 3/02.

	References

Top Abstract Introduction Materials and Methods Results Discussion References

 

1. Hsu J. L., Glaser S. L., West D. W. Racial/ethnic differences in breast cancer survival among San Francisco Bay Area women. J. Natl. Cancer Inst. (Bethesda), 89: 1311-1312, 1997.[Free Full Text]
2. Boyer-Chammard A., Taylor T. H., Anton-Culver H. Survival differences in breast cancer among racial/ethnic groups: a population-based study. Cancer Detect. Prev., 23: 463-473, 1999.[Medline]
3. Chevarley F., White E. Recent trends in breast cancer mortality among white and black US women. Am. J. Public Health, 87: 775-781, 1997.[Abstract/Free Full Text]
4. Joslyn S. A., West M. M. Racial differences in breast carcinoma survival. Cancer (Phila.), 88: 114-123, 2000.[Medline]
5. Elmore J. G., Moceri V. M., Carter D., Larson E. B. Breast carcinoma tumor characteristics in black and white women. Cancer (Phila.), 83: 2509-2515, 1998.[Medline]
6. Elledge R. M., Clark G. M., Chamness G. C., Osborne C. K. Tumor biologic factors and breast cancer prognosis among white. Hispanic, and black women in the United States. J. Natl. Cancer Inst. (Bethesda), 86: 705-712, 1994.[Abstract/Free Full Text]
7. Frost F., Tollestrup K., Hunt W. C., Gilliland F., Key C. R., Urbina C. E. Breast cancer survival among New Mexico Hispanic. American Indian, and non-Hispanic White women (1973–1992). Cancer Epidemiol. Biomark. Prev., 4: 861-866, 1996.[Abstract]
8. Zaloznik A. J. Breast cancer stage at diagnosis: Caucasians versus Hispanics. Breast Cancer Res. Treat., 42: 121-124, 1997.[Medline]
9. Bentley J. R., Delfino R. J., Taylor T. H., Howe S., Anton-Culver H. Differences in breast cancer stage at diagnosis between non-Hispanic white and Hispanic populations. San Diego County 1988–1993. Breast Cancer Res. Treat., 50: 1-9, 1998.[Medline]
10. Sugarman J. R., Dennis L. K., White E. Cancer survival among American Indians in western Washington state (United States). Cancer Causes Control, 5: 440-448, 1994.[Medline]
11. Meng L., Maskarinec G., Wilkens L. Ethnic differences and factors related to breast cancer survival in Hawaii. Int. J. Epidemiol., 26: 1151-1158, 1997.[Abstract/Free Full Text]
12. Meng L., Maskarinec G., Lee J. Ethnicity and conditional breast cancer survival in Hawaii. J. Clin. Epidemiol., 50: 1289-1296, 1997.[Medline]
13. Roetzheim R. G., Pal N., Tennant C., Voti L., Ayanian J. Z., Schwabe A., Krischer J. P. Effects of health insurance and race on early detection of cancer. J. Natl. Cancer Inst., 91: 1409-1415, 1999.[Abstract/Free Full Text]
14. Lannin D. R., Matthews H. F., Mitchell J., Swanson M. S., Swanson F. H., Edwards M. S. Influence of socioeconomic and cultural factors on racial differences in late-stage presentation of breast cancer. J. Am. Med. Assoc., 279: 1801-1807, 1998.[Abstract/Free Full Text]
15. Yood M. U., Johnson C. C., Blount A., Abrams J., Wolman E., McCarthy B. D., Raju U., Nathanson D. S., Worsham M., Wolman S. R. Race and differences in breast cancer survival in a managed care population. J. Natl. Cancer Inst. (Bethesda), 91: 1487-1491, 1999.[Abstract/Free Full Text]
16. Perkins P., Cooksley C. D., Cox J. D. Breast cancer: is ethnicity an independent prognostic factor for survival?. Cancer (Phila.), 78: 1241-1247, 1996.[Medline]
17. Ansell D., Whitman S., Lipton R., Cooper R. Race, income, and survival from breast cancer at two public hospitals. Cancer (Phila.), 72: 2974-2978, 1993.[Medline]
18. McGuire W. L., Clark G. M. Prognostic factors and treatment decisions in axillary-node-negative breast cancer. N. Engl. J. Med., 326: 1756-1761, 1992.[Medline]
19. Clahsen P. C., van de Velde C. J. H., Ducal. C, Pallud C., Mandard A. M., Delobelle-Deroide A., van den Broek L., van de Vijver M. J. The utility of mitotic index, oestrogen receptor and Ki-67 measurements in the creation of novel prognostic indices for node-negative breast cancer. Eur. J. Surg. Oncol., 25: 356-363, 1999.[Medline]
20. Mauri F. A., Maisonneuve P., Caffo O., Veronese S., Aldovini D., Ferrero S., Cozzaglio F., Dalla Palma P., Galligioni E., Barbareschi M. Prognostic value of estrogen receptor status can be improved by combined evaluation of p53. Bcl2 and PgR expression: an immunohistochemical study on breast carcinoma with long-term follow-up. Int. J. Oncology, 15: 1137-1147, 1999.[Medline]
21. Du Toit R. S., Locker A. P., Ellis I. O., Elston C. W., Nicholson R. I., Robertson J. F. R., Blamey R. W. An evaluation of differences in prognosis, recurrence patterns and receptor status between invasive lobular and other invasive carcinomas of the breast. Eur. J. Surg. Oncol., 17: 251-257, 1991.[Medline]
22. Gapstur S. M., Dupuis J., Gann P., Collila S., Winchester D. P. Hormone receptor status of breast tumors in black. Hispanic, and non-Hispanic white women: an analysis of 13,239 cases. Cancer (Phila.), 77: 1465-1471, 1996.[Medline]
23. Klonoff-Cohen H. S., Schaffroth L. B., Edelstein S. L., Molgaard C., Saltzstein S. L. Breast cancer histology in Caucasians, African Americans, Hispanics, Asians, and Pacific Islanders. Ethnicity Health, 3: 189-198, 1998.[Medline]
24. Weiss S. E., Tartter P. I., Ahmed S., Brower S. T., Brusco C., Bossolt K., Amberson J. B., Bratton J. Ethnic differences in risk and prognostic factors for breast cancer. Cancer (Phila.), 76: 268-274, 1995.[Medline]
25. Anderson W. F., Chu K. C., Chatterjee N., Brawley O., Brinton L. A. Tumor variants by hormone receptor expression in white patients with node-negative breast cancer from the Surveillance, Epidemiology, and End Results database. J. Clin. Oncol., 19: 18-27, 2001.[Abstract/Free Full Text]
26. Morabia A., Flandre P. Misclassification bias related to definition of menopausal status in case-control studies of breast cancer. Int. J. Epidemiol., 21: 222-228, 1992.[Abstract/Free Full Text]
27. Young, J. L., Jr., Percy, C., and Asire, A. J. (eds). Surveillance, Epidemiology, and End Results: incidence and mortality, 1973–77. Natl. Cancer Inst. Monogr., 57: 1–1082, 1981.
28. Breslow N. E., Day N. E. . The Analysis of Case-Control Studies, IARC Lyon, France 1980.
29. Chen V. W., Correa P., Kurman R. J., Wu X-C., Eley J. W., Austin D., Muss H., Hunter C. P., Redmond C., Sobhan M., Coates R., Reynolds P., Herman A. A., Edwards B. K. Histological characteristics of breast carcinoma in blacks and whites. Cancer Epidemiol. Biomark. Prev., 3: 127-135, 1994.[Abstract]
30. Pegoraro R. J., Karnan V., Nirmul D., Joubet S. M. Estrogen and progesterone receptors in breast cancer among women of different racial groups. Cancer Res., 46: 2117-2120, 1986.
31. Potter J. D., Cerhan J. R., Sellers T. A., McGovern P. G., Drinkard C., Kushi L. R., Folsom A. R. Progesterone and estrogen receptors and mammary neoplasia in the Iowa Women’s Health Study: how many kinds of breast cancer are there?. Cancer Epidemiol. Biomark. Prev., 3: 319-326, 1995.
32. Enger S. M., Ross R. K., Paganini-Hill A., Carpenter C. L., Bernstein L. Body size, physical activity, and breast cancer hormone receptor status: results from two case-control studies. Cancer Epidemiol. Biomark. Prev., 9: 681-687, 2000.[Abstract/Free Full Text]
33. Huang W. Y., Newman B., Millikan R. C., Schell M. J., Hulka B. S., Moorman P. G. Hormone-related factors and risk of breast cancer in relation to estrogen receptor and progesterone receptor status. Am. J. Epidemiol., 151: 703-714, 2000.[Abstract/Free Full Text]
34. Li C. I., Weiss N. S., Stanford J. L., Daling J. R. Hormone replacement therapy in relation to risk of lobular and ductal breast cancer in middle-aged women. Cancer (Phila.), 88: 2570-2577, 2000.[Medline]
35. Chen C-L., Weiss N. S., Newcomb P., Barlow W., White E. Hormone replacement therapy in relation to breast cancer. J. Am. Med. Assoc., 287: 734-742, 2002.[Abstract/Free Full Text]

This article has been cited by other articles:

				B. N. Polite, C. Cirrincione, G. F. Fleming, D. A. Berry, A. Seidman, H. Muss, L. Norton, C. Shapiro, K. Bakri, K. Marcom, et al. Racial Differences in Clinical Outcomes From Metastatic Breast Cancer: A Pooled Analysis of CALGB 9342 and 9840--Cancer and Leukemia Group B J. Clin. Oncol., June 1, 2008; 26(16): 2659 - 2665. [Abstract] [Full Text] [PDF]

				S. K. Quick, P. G. Shields, J. Nie, M. E. Platek, S. E. McCann, A. D. Hutson, M. Trevisan, D. Vito, R. Modali, T. A. Lehman, et al. Effect Modification by Catalase Genotype Suggests a Role for Oxidative Stress in the Association of Hormone Replacement Therapy with Postmenopausal Breast Cancer Risk Cancer Epidemiol. Biomarkers Prev., May 1, 2008; 17(5): 1082 - 1087. [Abstract] [Full Text] [PDF]

				K. M. E. Hahn, M. L. Bondy, M. Selvan, M. J. Lund, J. M. Liff, E. W. Flagg, L. A. Brinton, P. Porter, J. W. Eley, and R. J. Coates Factors Associated with Advanced Disease Stage at Diagnosis in a Population-based Study of Patients with Newly Diagnosed Breast Cancer Am. J. Epidemiol., November 1, 2007; 166(9): 1035 - 1044. [Abstract] [Full Text] [PDF]

				L. A. Newman, K. A. Griffith, I. Jatoi, M. S. Simon, J. P. Crowe, and G. A. Colditz Meta-Analysis of Survival in African American and White American Patients With Breast Cancer: Ethnicity Compared With Socioeconomic Status J. Clin. Oncol., March 20, 2006; 24(9): 1342 - 1349. [Abstract] [Full Text] [PDF]

				S. R. Gorla, N. Hou, S. Acharya, A. Rademaker, S. Khan, V. Staradub, and M. Morrow A Predictive Model for the Development of Hormone-Responsive Breast Cancer Ann. Surg. Oncol., January 1, 2005; 12(1): 48 - 56. [Abstract] [Full Text] [PDF]

				L. A. Newman Breast Cancer in African-American Women Oncologist, January 1, 2005; 10(1): 1 - 14. [Abstract] [Full Text] [PDF]

				E. Ziv, J. Tice, R. Smith-Bindman, J. Shepherd, S. Cummings, and K. Kerlikowske Mammographic Density and Estrogen Receptor Status of Breast Cancer Cancer Epidemiol. Biomarkers Prev., December 1, 2004; 13(12): 2090 - 2095. [Abstract] [Full Text] [PDF]

				F. M. Selaru, J. Yin, A. Olaru, Y. Mori, Y. Xu, S. H. Epstein, F. Sato, E. Deacu, S. Wang, A. Sterian, et al. An Unsupervised Approach to Identify Molecular Phenotypic Components Influencing Breast Cancer Features Cancer Res., March 1, 2004; 64(5): 1584 - 1588. [Abstract] [Full Text] [PDF]

				G. A. Colditz, B. A. Rosner, W. Y. Chen, M. D. Holmes, and S. E. Hankinson Risk Factors for Breast Cancer According to Estrogen and Progesterone Receptor Status J Natl Cancer Inst, February 4, 2004; 96(3): 218 - 228. [Abstract] [Full Text] [PDF]

				C. C. Benz, C. A. Clarke, and D. H. Moore II Geographic Excess of Estrogen Receptor-Positive Breast Cancer Cancer Epidemiol. Biomarkers Prev., December 1, 2003; 12(12): 1523 - 1527. [Abstract] [Full Text] [PDF]

				J. R. Daling, K. E. Malone, D. R. Doody, L. F. Voigt, L. Bernstein, P. A. Marchbanks, R. J. Coates, S. A. Norman, L. K. Weiss, G. Ursin, et al. Association of Regimens of Hormone Replacement Therapy to Prognostic Factors among Women Diagnosed with Breast Cancer Aged 50-64 Years Cancer Epidemiol. Biomarkers Prev., November 1, 2003; 12(11): 1175 - 1181. [Abstract] [Full Text]

This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Li, C. I. Articles by Daling, J. R. Search for Related Content PubMed PubMed Citation Articles by Li, C. I. Articles by Daling, J. R.