Impact of Sociodemographic Factors, Hormone Receptor Status, and Tumor Grade on Ethnic Differences in Tumor Stage and Size for Breast Cancer in US Women
Barry A. Miller1,
Benjamin F. Hankey1 and
Terry L. Thomas2
1 Division of Cancer Control and Population Sciences, National Cancer Institute, Bethesda, MD.
2 Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD.
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ABSTRACT
|
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The importance of sociodemographic factors and tumor biomarkers in explaining ethnic differences in tumor stage and size at diagnosis was investigated in over 106,000 female breast cancer patients reported during 19921996 from 11 US population-based cancer registries. Japanese and non-Hispanic White women tended to be diagnosed at an earlier stage, with smaller diameter tumors and with a lower tumor grade than women from seven other ethnic groups. Statistical adjustment for individual- and group-level sociodemographic factors produced 5080% reductions in the odds ratios for distant (vs. localized) stage and larger (vs. <1 cm) tumor size among Black women and Hispanic women. These factors also helped to account for tumor stage and size variation among most other ethnic groups. Consideration of hormone receptor status and tumor grade had little effect on the ethnic patterns. Although small, elevated odds ratios remained for some groups, our results suggest that sociodemographic factors accounted for many of the observed ethnic differences in breast cancer stage and tumor size at the time of diagnosis. Because most of the sociodemographic variables were aggregate measures, it is possible that residual confounding by socioeconomic position could explain the persistence of slightly elevated odds ratios in some ethnic groups.
breast neoplasms; case-control studies; ethnic groups; neoplasm staging; SEER Program; socioeconomic factors
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INTRODUCTION
|
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Observed ethnic variation in the stage at diagnosis for female breast cancer has led to investigations of the potential role of sociodemographic factors and tumor biology (1


5
). The three largest studies to evaluate these factors included only White women and Black women, and findings were conflicting with regard to ethnic differences in tumor biomarkers after adjustment for socioeconomic position (1
, 2
, 5
). Other investigators reported no significant ethnic differences in tumor characteristics for Hispanic women (3
) and Asian women (4
) relative to Whites, but study sizes were too small to draw firm conclusions. Two of the three larger studies were hospital based (2
, 5
), and one of these accrued study subjects from participants in clinical trials (2
), so findings may not be generalizable. This report assesses the importance of sociodemographic factors and tumor biology in explaining ethnic differences in tumor stage and tumor size at diagnosis in a large, population-based series of female patients diagnosed with invasive breast cancer.
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MATERIALS AND METHODS
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Study population
The study population included women newly diagnosed with an invasive, primary breast cancer between January 1, 1992, and December 31, 1996, in 11 population-based cancer registries within the Surveillance, Epidemiology, and End Results Program of the National Cancer Institute. These registries cover about 14 percent of the total US population and include the states of Connecticut, Hawaii, Iowa, New Mexico, and Utah, as well as the metropolitan areas of Atlanta, Georgia; Detroit, Michigan; Los Angeles, California; San Francisco-Oakland, California; San Jose-Monterey, California; and Seattle, Washington. Because it was of interest to examine ethnic patterns, the study was limited to diagnoses among the 10 largest population groups in these areas (Hispanic and the following non-Hispanic groups: White, Black, Japanese, Filipino, Chinese, Hawaiian, Korean, Vietnamese, and American Indian). This resulted in a potential study group of 107,096 breast cancer patients. Cases identified from only an autopsy record or death certificate comprised less than 1 percent of the intended study population (n = 599) and were excluded since they lack useful information on tumor characteristics at the time of diagnosis. There were no notable differences between the excluded group and the study group with respect to ethnic category or registry.
Study measures
Specific tumor characteristics at the time of diagnosis (summary stage, size, grade, estrogen receptor and progesterone receptor status) and a limited set of demographic variables (age, ethnicity, sex, marital status, place of birth, county and census tract of residence) were collected on individual study subjects, largely from hospital and pathology laboratory records. Breast tumors that are positive for estrogen receptor or progesterone receptor are correlated with favorable prognostic features, including evidence of tumor cell differentiation and a lower rate of cell proliferation (6


10
). Another marker of tumor biology, histologic grade, classifies the degree of cellular differentiation in cancer tissue and is a morphologic indicator of tumor aggressiveness (6
). Histologic grade correlates with breast cancer patient survival, with high grade cancers having the lowest survival probabilities (11
). This relation persists despite inter-observer and intraobserver variation among the pathologists who are assigning the tumor grade (11
), and even after the lymph node status of patients is taken into account (12
, 13
). Therefore, hormone receptor status and tumor grade were included in our study as indicators of tumor biology.
Sociodemographic variables for census tracts in the 1990 decennial census were linked to individual patient records, and each case was assigned the characteristics of the census tract where she resided at the time of her diagnosis (14
). These variables were selected a priori on the basis of theoretical relevance (15
17
) and empirical evidence of their utility in assessing the impact of socioeconomic position on a variety of health outcomes (16
, 18


















38
). They included the percentage of persons aged
25 years who did not have a high school diploma, the percentage of employed persons aged
16 years in "working class" jobs (23
), the percentage of persons aged
16 years who were unemployed, the percentage of households that owned their home, the percentage of households not owning a car, the percentage of persons living below the poverty level, median family income, the percentage of families headed by women with incomes below the poverty level and one or more children at home but with no husband living at home, and an indicator of whether the census tract is entirely urban (14
) versus all other.
Statistical analysis
Unconditional logistic regression models were used to estimate the relative importance of ethnicity in explaining the stage of disease and tumor size at the time of diagnosis after adjustment for selected sociodemographic variables and for indicators of tumor biology: tumor grade (well/moderately differentiated, poor/undifferentiated, unknown) and hormone receptor status (estrogen receptor or progesterone receptor positive vs. all other). Patient survival data were used to help in classifying cases that were missing hormone receptor or tumor grade information. Five-year cumulative relative survival was highest, at 89 percent, in the group with either positive estrogen receptor or positive progesterone receptor status and lowest, at 75 percent, in the group that was negative for both estrogen receptor and progesterone receptor. Those with all other combinations of receptor status had a survival rate close to that of the receptor-negative patients (78 percent), so they were grouped with the receptor-negative patients for the logistic regression analysis. Patients for whom tumor grade information was missing had a 5-year cumulative relative survival rate of 84 percent. This is midway between the survival rates for the low grade (94 percent) and high grade (75 percent) patients and similar to the survival rate for patients in grades 14 combined (86 percent), suggesting that the unknown tumor grade group was a mixture of high grade and low grade patients.
Other variables included in the regression analysis were age at diagnosis (continuous); Surveillance, Epidemiology, and End Results Program area; marital status at the time of diagnosis (married vs. unmarried or unknown); and interaction terms between ethnic group and the sociodemographic variables. Two sociodemographic variables (percentage unemployed, percentage living below the poverty level) were highly correlated with other sociodemographic variables, so they were excluded from the models. Odds ratios represent the odds that breast cancer patients in each ethnic group had a given category of tumor (later stage or larger diameter) relative to the odds for White women and are presented with 95 percent profile likelihood confidence intervals. Three outcomes were examined: patients diagnosed with 1) distant stage tumors versus localized tumors, 2) regional tumors versus localized tumors, and 3) tumors
1.0 cm in diameter versus tumors <1.0 cm.
Because study cases within a census tract may be more similar to each other than to cases in different census tracts with respect to some unmeasured characteristics, standard errors associated with regression coefficients may be underestimated in a traditional logistic regression analysis (39
, 40
). To account for this correlated data structure, we recalculated standard errors for the odds ratios using the Taylor linearization standard error estimation method in the SUDAAN logistic procedure for clustered data (41
, 42
). Most of the standard errors estimated by this method were within 12 percent of those from the standard logistic regression analysis, and all were within 8 percent, so results are presented from the standard analysis only.
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RESULTS
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Ninety-nine percent of the 106,497 invasive breast cancer cases had evidence in their medical records of confirmation of their diagnosis by microscopic examination. The confirmation rate did not vary by ethnic group. The predominant histologic type of breast cancer was ductal adenocarcinoma, accounting for 73.4 percent of all cases. Other types included lobular carcinoma (13.2 percent), nonspecific adenocarcinoma (4 percent), mucinous carcinoma (2.5 percent), nonspecific carcinoma (2.2 percent), medullary carcinoma (1.3 percent), and inflammatory carcinoma (1.1 percent). There was limited ethnic variation in histologic type, with White patients tending to have a higher percentage of lobular carcinomas and a slightly lower percentage of ductal adenocarcinomas than most other groups. When patients with ductal adenocarcinoma and those with all other histologic types were analyzed in separate regression models, the patterns of association between the study factors and outcomes were similar. Thus, results are presented for all histologic types combined.
The ethnic patterns of tumor characteristics and sociodemograhic factors are summarized in table 1. Because of the large study size, all ethnic differences in study variables yielded statistically significant chi-squared tests at an alpha level of 0.05. Japanese patients and White patients tended to be diagnosed at an earlier stage, with smaller diameter tumors and with a lower tumor grade than other groups. The increased proportion of low grade tumors among Japanese women and White women persisted after stratification by tumor stage (not shown). Black patients and Hispanic patients were more likely than other groups to be diagnosed with metastatic disease, to have tumors
2 cm in diameter, and to have poorly differentiated tumors. American Indian patients and Hawaiian patients also had a larger percentage of distant stage breast cancers. Among patients with information on hormone receptor status, White women, Japanese women, and Hawaiian women had consistently higher percentages that were positive for estrogen receptor or progesterone receptor.
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TABLE 1. Distribution of selected characteristics by percentage among 106,497 US female breast cancer patients diagnosed during 19921996
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Tumor stage information was unavailable for a small portion (3 percent) of all study cases. The percentage of unstaged cases was slightly higher among Black women and Korean women. Black women also had the highest percentage of tumors of unknown size and unknown grade. Tumor grade was missing for 25 percent of all study patients. Those missing tumor grade were more likely to have distant stage disease (8 percent vs. 5 percent distant among those having tumor grade information) and to be aged
80 years at the time of diagnosis (16 percent vs. 11 percent). Information on hormone receptor status was not available for 23 percent of the study population, with Black women, Hispanic women, and Vietnamese women having the highest rates of missing data. Patients who lacked hormone receptor status information were more likely to have distant stage disease (10 percent vs. 4 percent distant among those with information on hormone receptor status) and to be aged
80 years at the time of diagnosis (16 percent vs. 11 percent). Forty percent of the patients without information on hormone receptor status were also missing tumor grade versus 21 percent of those with hormone receptor status.
Census tract sociodemographic information was linked to 96.1 percent of the study cases. Cases that were not linked generally had incomplete or nonspecific residence address information that precluded assigning them to a census tract. The age distribution of unlinked cases was similar to the distribution among those with complete information. The Hawaii cancer registry had the largest percentage of unlinked cases (14 percent), and as a result, the percentage of native Hawaiians missing sociodemographic data was higher than that for other ethnic groups.
There were notable ethnic differences in sociodemographic factors. Black women were the least likely group to be married at the time of diagnosis. Black patients, Hispanic patients, Vietnamese patients, and American Indian patients were similar with regard to many of the sociodemographic characteristics of the census tracts where they lived. They were much more likely than other groups to be living in less educated and poorer neighborhoods, as measured by the percentage of residents without a high school diploma and median family income. They also tended to live in areas where residents held "working class" jobs and where a high percentage of families were headed by women with incomes below the poverty level and one or more children at home but with no husband living at home. Korean patients, Vietnamese patients, Black patients, and Hispanic patients lived more frequently in areas with low home ownership. Black patients and American Indian patients lived in areas with low car ownership. Hispanic patients, Filipino patients, Chinese patients, Korean patients, and Vietnamese patients lived in census tracts with higher concentrations of foreign-born persons. Place of birth information for patients, when available, also indicated that the majority of patients in these five ethnic groups were born outside the United States.
Results from multiple logistic regression models, used to assess the importance of study variables in explaining ethnic differences in tumor stage and size at the time of diagnosis, appear in tables 24. Patients for whom medical record information was insufficient to assign a tumor stage (3 percent) were excluded from regression analyses of tumor stage, and those lacking information on tumor size (9 percent) were excluded from the tumor size analysis. Unstaged cases were evenly distributed across age groups with the exception of women diagnosed at age
90 years (16 percent missing stage). This age group, however, accounted for only 1.6 percent of the study group. Cases missing tumor size were also evenly distributed by age group, with the exception of women aged
90 years (18.5 percent lacking tumor size). Additional subjects (3.7 percent) were excluded from regression models when they could not be linked to census tract sociodemographic information. Interaction terms between ethnicity and the group-level sociodemographic variables were not significant, based on a likelihood ratio test, so they were not included in the final models.
Odds ratios for distant stage disease, adjusted for age at diagnosis, were significantly elevated among Black women, Hispanic women, and American Indian women relative to White women (table 2). Odds ratios were significantly reduced for Japanese women and were not significantly different from 1.0 for other groups. The addition of geographic variables (registry where diagnosed, urban/nonurban residence) had little effect on the odds ratios. When sociodemographic factors were incorporated into the model, the excess odds for Hispanic women were reduced by 80 percent (from 1.5 to 1.1), the excess odds for Black women were lowered by 50 percent (from 2.0 to 1.5), and the excess odds for American Indian women were also reduced. Inclusion of tumor grade and hormone receptor status in the final model further reduced the odds ratio for Black women (from 1.5 to 1.3) but did not have a notable effect on the odds ratios for other ethnic groups.
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TABLE 2. Adjusted odds ratios and 95% confidence intervals for distant stage breast cancer versus localized stage among specific US racial/ethnic groups, 19921996
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The analysis of regional stage disease versus localized disease (table 3) indicated that ethnic differences are not as great as in the distant versus localized comparison. The odds ratios for Black women and Hispanic women are again elevated relative to those for White women, though at somewhat lower levels than those for distant stage disease. The odds ratio for Japanese women is significantly lower than that for White women, while odds ratios for the other groups are not significantly different from 1.0. The addition of geographic area and sociodemographic factors reduced the odds ratios for Black women, Hispanic women, and American Indian women, but no further reduction occurred after the inclusion of biologic characteristics of the tumors. The lower odds ratio for Japanese women remained unchanged after the addition of each group of potential confounding factors.
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TABLE 3. Adjusted odds ratios and 95% confidence intervals for regional stage breast cancer versus localized stage among specific US racial/ethnic groups, 19921996
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The odds ratios for larger tumor size at the time of diagnosis by ethnic group are shown in table 4. In the initial model, odds ratios adjusted for age at diagnosis are significantly high for Black women, Hispanic women, Filipino women, Chinese women, and Korean women relative to those for White women. Sociodemographic factors reduced odds ratios for most ethnic groups, but the addition of tumor grade and hormone receptor status to the model had little effect. The odds ratios for Black women, Hispanic women, Filipino women, and Korean women remained significantly elevated after statistical adjustment for all study factors. The odds ratio for Japanese women was significantly reduced and remained unchanged after each set of study variables was added to the model.
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TABLE 4. Adjusted odds ratios and 95% confidence intervals for breast cancer tumor size equal to or greater than 1 cm in diameter versus less than 1 cm among specific US racial/ethnic groups, 19921996
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Additional regression models that excluded patients who lacked hormone receptor information were examined, but the odds ratios for ethnic group and sociodemographic variables were unchanged, though the confidence intervals increased slightly. Regression models in which cases that lacked tumor grade information were either combined with those having low grade tumors or excluded from the analysis also yielded results similar to those presented.
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DISCUSSION
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In this large, population-based study of breast cancer patients, we have noted a variety of ethnic patterns in tumor characteristics and sociodemographic factors. Our finding that White women and Japanese women tend to be diagnosed at an earlier stage than other groups has been documented in earlier studies in Hawaii (43
, 44
). The poorer stage distribution in Black women, Hispanic women, and American Indian women has also been noted by others (1
, 20
, 45










57
).
White patients and Japanese patients in our study were more likely than other groups to have well-differentiated breast tumors and to be positive for estrogen receptor or progesterone receptor. Ethnic differences in hormone receptor status have been documented in several studies (1
, 2
, 5
, 8
, 45
, 49
, 58


62
). Many of these were hospital-based studies or included only breast cancer patients in clinical trials. Few adjusted for potential confounding by sociodemographic factors (1
, 2
). Chen et al. (1
) noted that a Black/White difference in estrogen receptor status persisted among patients in three urban Surveillance, Epidemiology, and End Results registries after adjustment for socioeconomic position, body mass index, alcohol and tobacco use, reproductive experience, health care access, and usual source of care. Although we found ethnic variation in hormone receptor status and tumor grade in our study, the importance of these variables in explaining ethnic patterns of tumor stage and size, after adjustment for all other study variables, was limited primarily to the diagnosis of distant versus localized tumors.
In our study, sociodemographic factors accounted for 5080 percent reductions in the odds ratios for distant stage and larger size breast tumors among Black patients and Hispanic patients. Associations between sociodemographic factors and the severity of breast cancer have been reported by others (3
, 5
, 20
, 46
, 50
, 52
, 55
, 57
, 63
). Marital status, a strong predictor for tumor stage and size in our study, was linked to the extent of disease in a study of several cancer types in New Mexico (64
). It has been suggested that married persons tend to demonstrate better health behaviors, including less delay in seeking medical care after the occurrence of symptoms, than unmarried persons do. Married persons also tend to have higher socioeconomic status and greater social support (64
). Several investigators have emphasized the impact of sociodemographic factors on access to physician care or screening services (65
67
). Mammography use has been found to be positively associated with income, education, having health insurance coverage, having a usual source of care, and urban residence (68





75
). A number of surveys indicate that the use of mammography in the United States has risen over time (72
, 74
, 76
), though the majority of breast cancers are still first discovered by the patient either by breast self-examination or as an incidental finding (77
, 78
). Despite the general increase over time in the use of mammography for early detection, surveys indicate that sociodemographic differentials persist, with women in lower income and education groups having lower screening rates (68
, 71
, 72
, 76
, 79
).
A tumor size of
1 cm served as an indirect indicator of delayed detection in our study. Tumors of <1 cm are found primarily by screening mammography, whereas larger tumors are often detected by other methods such as symptoms, clinical breast examination, or breast self-examination (80
82
). Odds ratios for larger tumors remained elevated among Black women, Hispanic women, Filipino women, and Korean women in our analysis after adjustment for all other study variables. Recent analyses of breast tumor size and stage in Asian-American women and Hispanic women in a selected subset of Surveillance, Epidemiology, and End Results Program registries have suggested that larger tumor size at diagnosis is associated with birthplace outside the United States (83
, 84
). Birthplace information was missing, however, on a large percentage of the cases in these studies. Furthermore, birthplace information for cancer registry cases is frequently obtained only from a death certificate, thereby resulting in a study population that is overrepresented by deceased cases. Survey data on health behaviors among Chinese women, Filipino women, Korean women, and Vietnamese women living in California, however, have indicated that these ethnic groups are less likely to report ever having had a mammogram than are women in the general population (85



90
). Hispanic women have also been reported to be less likely to have undergone breast cancer screening than non-Hispanic White women (91
, 92
). This suggests the possibility that lower utilization of mammography in these ethnic groups may be leading to the diagnosis of more advanced tumors. Factors associated with lower screening rates among women in these studies included the lack of a physician recommendation for a mammogram, concern over cost, belief that a mammogram is needed only in the presence of symptoms, perceived inconvenience or difficulties in getting to the mammography facility, and embarrassment.
Odds ratios for distant and regional stage disease among Black women in our study relative to White women remained slightly elevated after adjusting for sociodemographic variables and tumor biology. Several other studies have found that sociodemographic effects alone do not account for all of the ethnic differences in tumor stage at diagnosis (47
, 52
, 63
, 93
95
). Even in situations where universal access to medical care is provided, ethnic disparities in breast cancer diagnosis or outcome persist (73
, 96
, 97
). Cultural factors such as beliefs, attitudes, and knowledge about cancer have been shown to vary by ethnicity and have been found to influence cancer screening and prevention behaviors (57
, 90
, 98




104
). Results from a recent case-control study of breast cancer patients diagnosed in an eastern North Carolina hospital indicated that psychosocial and cultural beliefs in conjunction with socioeconomic factors were sufficient to explain the difference in stage at diagnosis between Black women and White women (57
). The investigators concluded that cultural beliefs may have led to delayed presentation once a woman had developed a palpable breast abnormality. An earlier study of women in the same North Carolina communities found that personal knowledge and beliefs had little influence, however, on a woman's use of screening mammography (105
). The most important factor was whether mammography was recommended to the patient by a physician. Another study of breast cancer patients identified within a health maintenance organization setting in North Carolina also found that patient delay before reporting breast cancer symptoms to a physician was an important factor in explaining tumor stage at the time of diagnosis (106
).
Our finding that Japanese patients tended to be diagnosed at an earlier stage and smaller tumor size than other groups has been reported by others (83
, 107

110
). It has been suggested that differences in the histopathologic features of breast cancers in Japanese women and White women may indicate underlying biologic differences in the tumors between these two groups (110
, 111
). Adjustment for tumor grade and hormone receptor status, in addition to socio-demographic factors, did not alter the reduced odds ratios among Japanese women for any of our study outcomes.
Evidence for a role of tumor grade or hormone receptor status in explaining ethnic differences in breast cancer stage and size at diagnosis was not compelling in our study. After adding these variables to the regression models, we found that odds ratios for Black women declined somewhat for distant stage disease but did not markedly change in any of the ethnic groups for regional stage disease or larger tumor size. These findings must be interpreted with caution because of the large percentage (about 20 percent) of study cases with missing information on either hormone receptor status or tumor grade.
Only limited risk factor information was available from cancer registry records on our study subjects. Individual information on factors such as body mass, alcohol and tobacco use, reproductive history, medical insurance status, usual source of health care, and screening behavior would have been helpful in evaluating the ethnic patterns of tumor stage and size at the time of diagnosis. Although the utility and advantages of using neighborhood-level sociodemographic data have been shown in a variety of studies assessing the impact of socioeconomic position on health outcomes (24
, 27
, 32
, 37
, 38
, 112
, 113
), the addition of individual-level sociodemographic information would have allowed a multilevel assessment of the importance of these factors in our study population. Using neighborhood-level sociodemographic data may also lead to residual confounding by socioeconomic position because the aggregated measures lack distributional information (114
116
). This residual confounding and/or the influence of other important unmeasured factors could explain the persistence of slightly elevated odds ratios for some ethnic groups in this study. Nevertheless, several investigators support the increased use of neighborhood-based measures of socioeconomic position in public health research and surveillance because they capture aspects of a person's living conditions that may be missing from individual measures (4
, 32
). Neighborhood-level measures may also provide a more stable estimate of the economic situation of persons than do some of the more volatile individual measures such as personal income.
Our results suggest that the sociodemographic factors measured in this study can account for a large portion of observed ethnic differences in breast cancer stage and tumor size at the time of diagnosis. It would be useful to confirm these findings in additional studies that include patient-level sociodemographic data as well as area-based measures. Since a socio-demographic disparity in mammography screening levels has been documented in several population surveys, methods for increasing compliance with recommended guidelines should be identified and implemented. Additional studies could focus on the relations between sociodemographic factors and the quality of mammography, whether mammography is received at regular intervals, and whether appropriate follow-up and treatment are given to identified cases. Further study is also needed to determine whether differential exposure to carcinogens, genetic susceptibility, or some other factors may lead to more aggressive forms of breast cancer.
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ACKNOWLEDGMENTS
|
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This study was based largely on doctoral dissertation research completed for the Department of Preventive Medicine and Biometrics of the Uniformed Services University of the Health Sciences in Bethesda, Maryland.
The authors thank Drs. David Cruess, Gary Gackstetter, and Tracy Sbrocco of the Uniformed Services University of the Health Sciences and Dr. Barry Graubard of the National Cancer Institute for their respective contributions. Technical support from the cancer registries participating in the Surveillance, Epidemiology, and End Results Program of the National Cancer Institute was greatly appreciated.
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NOTES
|
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Correspondence to Dr. Barry A. Miller, National Cancer Institute, Suite 504, 6116 Executive Boulevard, Bethesda, MD 20892 (e-mail: bm33q{at}nih.gov).
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Received for publication April 10, 2001.
Accepted for publication September 13, 2001.