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American Journal of Epidemiology Advance Access originally published online on August 9, 2007
American Journal of Epidemiology 2007 166(9):1035-1044; doi:10.1093/aje/kwm177
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American Journal of Epidemiology Published by the Johns Hopkins Bloomberg School of Public Health 2007.

ORIGINAL CONTRIBUTIONS

Factors Associated with Advanced Disease Stage at Diagnosis in a Population-based Study of Patients with Newly Diagnosed Breast Cancer

Karin M. E. Hahn1,2, Melissa L. Bondy2, Mano Selvan3, Mary Jo Lund4, Jonathan M. Liff5, Elaine W. Flagg6, Louise A. Brinton7, Peggy Porter8, J. William Eley4 and Ralph J. Coates9

1 Department of Breast Medical Oncology, The University of Texas M. D. Anderson Cancer Center, Houston, TX
2 Department of Epidemiology, The University of Texas M. D. Anderson Cancer Center, Houston, TX
3 Department of Quality Improvement, The University of Texas M. D. Anderson Cancer Center, Houston, TX
4 Winship Cancer Institute, Emory University, Atlanta, GA
5 Department of Epidemiology, Rollins School of Public Health, Emory University, Atlanta, GA
6 Division of HIV/AIDS Prevention, National Center for HIV, STD, and TB Prevention, Centers for Disease Control and Prevention, Atlanta, GA
7 Hormonal and Reproductive Epidemiology Branch, National Cancer Institute, Bethesda, MD
8 Division of Human Biology, Fred Hutchinson Cancer Research Center, Seattle, WA
9 Division of Cancer Prevention and Control, Centers for Disease Control and Prevention, Atlanta, GA

Correspondence to Dr. Karin M. E. Hahn, Departments of Breast Medical Oncology and Epidemiology, Unit 1354, The University of Texas M. D. Anderson Cancer Center, P.O. Box 301439, Houston, TX 77230-1439 (e-mail: khahn{at}mdanderson.org).

Received for publication January 16, 2007. Accepted for publication May 11, 2007.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Breast cancer is diagnosed at a younger age and a more advanced stage in African-American women than in White women. The authors investigated the effects of several factors, including race, on stage of breast cancer in women aged 20–54 years living in Atlanta, Georgia, and diagnosed between 1990 and 1992. A total of 251 African-American and 580 White women were interviewed and their medical records reviewed. By use of polytomous logistic regression, factors possibly influencing stage and racial differences in stage were studied. In African-American women, the odds of stage III/IV breast cancer at diagnosis were almost four times the odds in White women (odds ratio = 3.79, 95% confidence interval: 2.45, 5.89) and approximately two and one-half times for stage IIA or stage IIB disease (odds ratio = 2.57, 95% confidence interval: 1.66, 3.99; odds ratio = 1.94, 95% confidence interval: 1.31, 2.86, respectively). These racial differences appeared to be largely explained by insurance status, poverty, history of mammography, method of tumor detection, and obesity. Interventions targeting these factors could potentially lower the stage at diagnosis for African-American breast cancer patients and, in doing so, improve their survival and other outcomes.

body mass index; breast neoplasms; demography; ethnic groups; socioeconomic factors

Abbreviations: ER, estrogen receptor; PR, progesterone receptor


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
In the United States, African-American women diagnosed with breast cancer are more likely than White women to have regional/distant disease (43 percent vs. 33 percent, respectively) (1). This difference may help to explain why, although African-American women are less likely than White women to have breast cancer, they are more likely to die from their disease (1).

Although a number of studies have investigated which factor or factors are associated with the more advanced stage or the decreased survival observed among African-American women diagnosed with breast cancer, the explanation for this difference remains unclear (2–33). The majority of these studies utilized cancer registries, medical records, and/or other databases and, therefore, are limited by the lack of information that could have been obtained from the patients themselves. For example, in a recent meta-analysis of survival in African-American and White breast cancer patients in the United States that compared ethnicity with socioeconomic status, only three of the 20 studies examined relied on patients' self-reports for determining socioeconomic status (34).

The studies of ethnicity and breast cancer that included patient interviews have been focused primarily on the outcomes of overall or breast cancer-specific survival (2–5). In the Carolina Breast Cancer Study (2), premenopausal African-American women with breast cancer were more likely to have basal-like tumors (estrogen receptor (ER) negative, progesterone receptor (PR) negative, HER-2/neu negative, cytokeratin 5/6 positive, and/or HER-1 positive) than were postmenopausal African-American and non-African-American breast cancer patients. Carey et al. (2) proposed that the higher prevalence of basal-like tumors seen among premenopausal African-American women could contribute to their observed poorer prognosis. This analysis, however, focused primarily on pathologic predictors and did not adjust for other factors, demographic and/or socioeconomic, that could have influenced survival. In the Women's Health Initiative, there were no statistically significant racial differences in the stage of breast cancer diagnosed among participants (3). In this study, African-American women with breast cancer were more likely than White women to have tumors that were poorly differentiated, ER negative, and PR negative. After adjustment for age, body mass index, tumor stage, and study arm, the African-American participants in the Women's Health Initiative had a statistically significant increased risk of death after being diagnosed with breast cancer compared with the White women with breast cancer. In the Black/White Cancer Survival Study, nuclear grade and indicators of access to health care explained approximately half of the excess risk for advanced stage in African-American women diagnosed with breast cancer compared with White women (4).

Few studies have been able to address whether racial differences in breast cancer stage may be related to demographic characteristics, socioeconomic status, cultural factors, or the biologic characteristics of the tumors themselves. To further identify the factors that may contribute to an advanced stage at the time of diagnosis and that may explain racial differences in stage that have been reported, we conducted a population-based study of African-American and White women between the ages of 20 and 54 years with newly diagnosed invasive breast cancer.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Participants
The patients in this study were interviewed previously as part of a population-based case-control study of invasive and in situ breast cancer (35). After approval was obtained from the appropriate institutional review boards, the case-control study identified 950 African-American and White women aged 20–54 years, with unilateral invasive breast cancer diagnosed between May 1, 1990, and December 31, 1992. These women resided in Cobb, Fulton, or DeKalb counties in metropolitan Atlanta, Georgia. Case identification was through rapid ascertainment of hospital admission, surgery, and pathology records. The method of data collection has been described previously (35).

The interview response rate for the case-control study was 87.9 percent (835 of 950): 88.2 percent (584 of 662) for White women and 87.2 percent (251 of 288) for African-American women. For the current study, we excluded one woman who later self-reported being of another race, three women who were interviewed as control subjects and were subsequently diagnosed with breast cancer, and 13 women with bilateral breast cancer. Also excluded were two women for whom stage could not be determined. Thus, our study consisted of 829 women: 250 (30.2 percent) African American and 579 (69.8 percent) White.

Data collection
Data collection for the original case-control study included personal interviews, medical record review, and anthropometric measurements (35). The manner of data collection and the variables collected have been described previously (36).

Outcome variable
The disease stage at the time of diagnosis was defined by use of the criteria detailed in the American Joint Committee on Cancer staging manual. The third edition of the manual was in use for the entire period of case ascertainment, 1990–1992 (37). Stages IIA and IIB were analyzed separately, because 46 percent of patients with stage IIA disease had positive lymph nodes, but 94 percent of patients with stage IIB disease were lymph node positive. Thus, in our cohort, stages IIA and IIB appeared to represent different patient populations with different prognoses. Breast cancer patients with axillary lymph node involvement have a higher likelihood of recurrent disease when compared with node-negative breast cancer patients (38). Similar to the methods used in our study of delay in diagnosis and initiation of treatment, stages III and IV were combined because the numbers in each subset (IIIA, IIIB, and IV) were too small for meaningful analysis separately (36).

Predictors of stage
Our study used self-reported race. The numbers of Hispanic women (0.8 percent of African Americans and 1.0 percent of Whites) were too small for a separate analysis.

ER and PR status was obtained from the cancer registry and medical record abstraction. The data from the two sources were compared, and when there was a conflict or data were not available from either source, an extensive review of pathology reports and other medical records was conducted. ER or PR values that were borderline or equivocal were classified as positive. Histologic grade was classified on the basis of the highest grade recorded; for example, if the grade was recorded as II/III or moderate to poorly differentiated, the grade was classified as III. Other predictors of stage in this analysis have been described previously (36).

Statistical methods
A set of predictor variables, which included tumor histologic grade, ER/PR status, race, age, menopausal status, marital status, comorbidity status, smoking status, family history, education, insurance, poverty index, 5-year mammography history, method of detection, breast self-examination practice, body mass index, bra cup size, and diagnosis delay, was selected on the basis of previously published research and current medical knowledge of variables that have been shown to influence stage at diagnosis (1–33). By performing a univariate analysis, we examined the effect of each of these factors on breast cancer stage at the time of diagnosis, with stage I as the reference stage (table 1) (39). All calculated p values were two sided.


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  		TABLE 1. Predictors of a later stage of breast cancer at diagnosis among women living in Atlanta, Georgia, and diagnosed between 1990 and 1992*

 
We then examined the distribution of this same set of predictors of stage by race to determine whether African-American women differed from White women in factors that could predict a higher stage at the time of diagnosis. We applied chi-square tests to evaluate the statistical significance of the associations between race and these variables.

Each of the predictors associated with either race or stage (p ≤ 0.20) in our analysis was modeled to determine its effect on relations between race and stage at the time of diagnosis. Factors that changed the odds ratio for the relations between race and stage by at least 10 percent were considered to be potential contributors to racial differences in stage. Each of these variables was entered individually along with race and age into the polytomous logistic regression model for stage, a multinomial response variable (table 2) (40).


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  		TABLE 2. Factors affecting the calculated odds of a higher stage of breast cancer for African-American women relative to White women living in Atlanta, Georgia, and diagnosed between 1990 and 1992

 
To determine which factors were most strongly predictive of a higher stage when adjusted for other predictors, we performed multiple logistic regression for those variables that predicted advanced stage disease in bivariate analysis (p ≤ 0.20) (40). In the first model, we considered all the variables (table 3). Because tumor grade and ER/PR status may partially be outcomes of stage at diagnosis, as well as being factors that influence stage, we conducted a second multinomial logistic regression analysis using those factors not related to specific tumor characteristics, that is, histologic grade and ER/PR status.


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  		TABLE 3. Factors affecting higher stage at breast cancer diagnosis (n = 814*) among women living in Atlanta, Georgia, and diagnosed between 1990 and 1992{dagger}

 

   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
Among African-American women with breast cancer in our study, approximately 25 percent had stage I disease; 29 percent, stage IIA; 21 percent, stage IIB; and 25 percent, stage III/IV at diagnosis. Of the White women with breast cancer, however, almost 46 percent had stage I disease; 27 percent, stage IIA; 15 percent, stage IIB; and 12 percent, stage IV. The majority of the study participants, both White and African American, were less than 50 years of age, were premenopausal, were married or living as married, did not have a college degree, were privately insured, had no comorbidities, had no family history of breast cancer, and were former or never smokers (data not shown).

There were several differences between African-American and White women in our study population in terms of the distribution of these predictors of stage (data not shown). African-American women were more likely to be younger at the time of diagnosis, to have more comorbidities, to have a higher body mass index, to lack a college education, to be poor, to be uninsured, to practice breast self-examination, to self-detect their tumors, to not have had a mammogram, and to have had a delay in diagnosis. African-American women were also more likely to have high-grade and ER/PR-negative tumors at diagnosis. In our study, there were no significant differences between African-American and White women in menopausal status, marital status, family history, or bra cup size.

As depicted in table 1, the odds of stage III/IV disease for African-American women were almost four times the odds for White women, and the odds of stage IIA or IIB disease were approximately from two to two and one-half times those of White women. Stage IIA disease was associated with being younger, having unknown insurance status, not having had a mammogram in the past 5 years, self-detecting the cancer, having the cancer detected by clinical breast examination, and having tumors that were moderate to poorly differentiated (table 1). For those diagnosed with stage IIB disease, they were more likely to be younger, poor, and overweight/obese, without a college degree; to have government-funded health insurance or unknown insurance status; to not have had mammography in the past 5 years; to self-detect their tumors; to have moderate to poorly differentiated tumors; and to have ER/PR-negative tumors. Women diagnosed with stage III/IV disease were more likely to be poor, to be overweight/obese, to have a larger bra cup size, to be without a college degree, to have comorbidities, to be without insurance or to have unknown insurance status, to have no mammography in the past 5 years, to detect the breast tumor through either clinical or self-breast examination, and to have tumors that were moderately to poorly differentiated and tumors that were ER and PR negative.

Adjustment for the factors associated with stage or with race reduced the odds of late-stage disease among African-American women (table 2). Individual adjustment for insurance status, poverty index, mammography history, method of detection, and body mass index reduced the odds of African-American women's subsequent diagnosis with later-stage disease. Adjustments for each of the other factors that we examined (table 1) did not reduce the odds of a more advanced stage of diagnosis by more than 10 percent. Adjustment for insurance status, poverty index, mammography history, method of detection, and body mass index reduced the excess odds of stage IIA disease by more than 50 percent and the excess odds of the later stages by much more then 50 percent, with the 95 percent confidence interval for each stage overlapping 1.0. This suggested that these five factors explained most of the racial differences in stage in this cohort. None of these factors could be clearly identified as the major contributor to racial differences in stage, as each factor had different effects on the odds that African-American women were diagnosed with later-stage breast cancer. Although adjustment for tumor histologic grade and ER/PR status reduced the odds of later-stage disease among African-American women, adjustment for these factors in addition to nontumor variables did not further significantly reduce the calculated odds of late-stage disease in African-American women beyond the reduction found by adjustment for the nontumor variables.

Examining the relations of all of the predictors of stage in a single model showed that the factors that were most clearly predictive of late-stage disease were being poor, self-detecting the tumor, having a higher body mass index, and having a poorly differentiated tumor (table 3). Although tumor ER and PR status appeared to influence stage, this may have been affected by the tumors of unknown receptor status. However, the percentages of White and African-American patients who were missing data on receptor status were small and almost equally balanced at 5.2 percent and 5.6 percent, respectively. Race and the other predictors examined in this analysis were unrelated or less clearly related to stage.

Because such tumor-specific variables as histologic grade and ER/PR status may partially be an outcome of stage rather than just a predictor of stage, we examined the effect of all the nontumor-specific predictors of stage in another model. The results of this analysis were similar to those when the tumor-specific variables were included (data not shown). In this model, method of detection, that is, self-detection of a tumor, and body mass index had the greatest effect on a higher stage at the time of diagnosis, although poverty may have had some effect (p = 0.062).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
We found that African-American women were more likely to be diagnosed with more advanced breast cancer, a finding similar to those of other studies and reflecting data from the Surveillance, Epidemiology, and End Results (SEER) Program cancer registry (1, 4, 9, 11, 12, 14). We found that these racial differences in stage were explained largely by insurance status, poverty, mammography screening history, method of breast cancer detection, and obesity (as shown by body mass index).

We found that a lack of health insurance explained some of the observed differences in stage at diagnosis when African-American and White women were compared. Several studies have directly or indirectly addressed the effect of health insurance on stage at the time of breast cancer diagnosis (3, 6, 7, 18, 19, 24, 25). Most of these studies appeared to suggest that racial differences in breast cancer stage were not significant in systems where there was equal access to care through either private or governmental health-care coverage. However, health insurance alone is unlikely to be the only answer, because the findings of our study and those of the Black/White Study suggest that the problem is probably multifactorial (6).

The majority of studies that examined the impact of poverty on stage at breast cancer diagnosis used registry data, such as the Surveillance, Epidemiology, and End Results Program registry, that were then linked to census tract indicators of socioeconomic status (15, 20–23). In most of these studies, adjustment for these socioeconomic indicators explained the majority of the observed differences in stage between African-American and White breast cancer patients (15, 22). However, in the recent meta-analysis by Newman et al. (34), adjustment for socioeconomic status alone did not explain the poor outcome of African-American women diagnosed with breast cancer. As mentioned previously, only three of the 20 studies they examined relied on patient self-report for determining socioeconomic status. In our study, we also found that differences in the poverty (as measured by the Department of Health and Human Services Poverty Index) alone did not explain the racial differences in stage at diagnosis that we observed (41).

Several studies have examined the impact of screening mammography on the observed racial differences in breast cancer stage at diagnosis (4, 6, 31, 42). In a large prospective cohort of over 1 million women 40 years of age or older who had at least one mammogram between 1996 and 2002, African-American women were more likely than White women to have large, advanced-stage breast tumors (42). The observed differences in advanced stage at diagnosis in this cohort were attenuated or eliminated when stratified by screening history. However, African-American women whose last mammogram was 4 or more years from breast cancer diagnosis had more advanced tumors than did White women with the same screening history. In our study, mammography history significantly impacted on stage at diagnosis in age-adjusted polytomous logistic regression (table 2).

In our population, being overweight (body mass index: 25.0–29.9) or obese (body mass index: ≥30) increased the risk of later-stage disease. Similar results have been seen in other studies (4, 26–28). The increased body mass index may make it more difficult to radiographically image tumors and may affect the ability of the patient or physician to palpate the cancer. Estrone is produced in adipose tissue through the aromatization of androstenedione. Studies have shown that the growth of breast tumors is promoted by a local increase in estrogen levels (43–45). Although the mechanism is not completely clear, obesity and/or weight gain may play a role in the development or growth of breast cancer.

This study has several strengths: It was population based, response rates were good, and we were able to collect information on many factors that may influence the stage of breast cancer at the time of diagnosis. However, the study size was somewhat small, and this may have affected the power to detect the effect of some factors that could influence stage. Our findings may reflect temporal and regional differences in socioeconomic and cultural factors, and this may influence the generalizability of our results.

Our findings suggest that the observed differences between African-American and White women in breast cancer stage at diagnosis could be substantially reduced by addressing poverty and obesity, improving health insurance coverage, and increasing participation in recommended screening mammography. Poverty and lack of health insurance are ongoing problems for many African-American women as noted in many earlier studies examining factors influencing a later stage at breast cancer diagnosis. Education of the public and health-care professionals may need to be improved or reinforced so that all women, particularly women 40–54 years of age, are aware of the US Preventive Services Task Force's recommendations for mammography screening (46). The "Guide to Community Preventive Services" has recommendations on effective community and health-system interventions to increase mammography screening (47). Some specific interventions, resources, and tools are available on the Cancer Control PLANET website (48) for those communities, health plans, or agencies interested in improving or implementing preventive health services. The National Breast and Cervical Cancer Early Detection Program provides screening services to low-income, uninsured, and underserved women in the United States but reaches only a small percentage of those who are eligible (49). Finally, obesity, which increases the risk of many adverse health conditions including breast cancer, needs to be addressed through effective community interventions. Recommendations and resources for effective interventions to improve physical activity are also available from the Community Guide and Cancer Control PLANET (47, 48). The American Cancer Society has recently published guidelines on nutrition and physical activity for cancer prevention (50).

In summary, our study has identified several factors that if addressed could reduce the differences in advanced stage breast cancer diagnosis between African-American and White women and, by doing so, may ultimately affect the observed racial differences in breast cancer mortality. Although there are a number of effective programs that could reduce some of the elements responsible for the later stage at breast cancer diagnosis seen among African-American women as compared with White women, the availability or accessibility of these programs may need to be improved.


   ACKNOWLEDGMENTS
 
This work was supported by Public Health Services grants N01-CP-95604, N01-PC-35135, and R01-CA64292-01A2 from the National Cancer Institute and by grant U48 CCU0619515 from the Centers for Disease Control and Prevention.

The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention.

Conflict of interest: none declared.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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