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Racial differences in follow-up of abnormal mammography findings among economically disadvantaged women
Article first published online: 26 OCT 2009
Copyright © 2009 American Cancer Society
Volume 115, Issue 24, pages 5788–5797, 15 December 2009
How to Cite
Adams, S. A., Smith, E. R., Hardin, J., Prabhu-Das, I., Fulton, J. and Hebert, J. R. (2009), Racial differences in follow-up of abnormal mammography findings among economically disadvantaged women. Cancer, 115: 5788–5797. doi: 10.1002/cncr.24633
Fax: (803) 576-5624
- Issue published online: 2 DEC 2009
- Article first published online: 26 OCT 2009
- Manuscript Accepted: 5 FEB 2009
- Manuscript Revised: 9 JAN 2009
- Manuscript Received: 14 OCT 2008
- health status disparities;
- African Americans;
- medically uninsured;
- breast neoplasms
In the United States, and particularly in South Carolina, African-American women suffer disproportionately higher mortality rates from breast cancer than European-American women. The timeliness of patient adherence to the follow-up of mammographic abnormalities may influence prognosis and survival. The objective of the current investigation was to examine racial differences in the completion and completion time of a diagnostic workup after the finding of a suspicious breast abnormality.
Study participants of the Best Chance Network, a statewide service program that provides free mammography screening to economically disadvantaged and medically underserved women, were included in the study. Racial differences in tumor characteristics and adherence to recommended workup were tested using chi-square tests and t tests. Logistic and Cox regression modeling was used to assess the relation between workup completion and other factors among African-American women and European-American women.
Completion of the workup was associated with the number of previous procedures and income, and no significant differences were noted by race. The amount of time to completion of the workup was influenced by previous procedures, income, and race. After accounting for completion time, African-American women were 12% less likely than European-American women to complete the recommended workup (hazard ratio, 0.88; P = .01).
The results from this study established a racial disparity in the time to completion of a diagnostic workup among Best Chance Network participants. These findings highlight the importance of understanding the factors associated with delays in and adherence to completing the recommended workup when breast abnormalities are detected in mammograms. Cancer 2009. © 2009 American Cancer Society.
It is well established that African-American women suffer disproportionately higher mortality rates from breast cancer than their European-American counterparts.1-3 Previous research has done little to explain why African-American women present at much younger ages with more aggressive disease4-7 and experience much higher breast cancer mortality rates than their European-American counterparts.4-9 Factors related to access to screening and treatment explain only part of the excess variability.2, 10-12 Many important gaps in our knowledge must be filled before we can devise the best strategies to reduce these racial disparities in breast cancer.
The disparities observed on the national level are even more striking when we focus on outcomes in South Carolina. In 2000, breast cancer incidence rates were lower than the national rates for South Carolinian women: 11% lower for European-American women and 8% lower for African-American women.1, 13 However, although mortality rates for European-American women in South Carolina were 7% lower than the national US mortality rate, they were 29% higher for African-American women in South Carolina.1, 13 Preliminary work in this South Carolina population has indicated that, even at the same stage and tumor size, breast cancers in African-American women tend to be more aggressive than those in European-American women.14
Numerous studies have demonstrated that early detection (from methods including mammography, breast self-examination, and clinical breast examination) is 1 of the best ways to improve the prognosis for a woman with breast cancer.9, 15-19 Not only may the prognosis for a woman with breast cancer be improved by early detection, but prognosis also may be influenced by the timeliness of a patient adhering to recommended follow-up when a breast abnormality is discovered.20 Patient adherence to follow-up recommendations most likely is multifaceted. Previous research has demonstrated that socioeconomic and demographic characteristics and certain attitudes or misconceptions about cancer are associated with delayed or incomplete follow-up.21-25 Such attitudes are common among low-income, minority, and underinsured or uninsured populations.17, 26 Furthermore, research has indicated that, compared with European-American women, African-American women experience significantly longer time intervals from an abnormal mammogram to diagnostic testing and are less likely to comply with recommended diagnostic follow-up examinations within 6 months of an abnormal mammogram.27-29
The South Carolina National Breast and Cervical Cancer Early Detection Program (NBCCEDP) offers an ideal opportunity to study the relation between race and mammography follow-up in an economically disadvantaged population. The NBCCEDP is a nationwide program that helps uninsured or underinsured women gain access to screening services for the early detection of breast cancer. The South Carolina NBCCEDP, commonly called the Best Chance Network (BCN), provides free mammography and cervical screenings to women ages 47 years to 64 years who do not have health insurance or for whom insurance pays for hospital care only and who are at or below 200% of federal poverty guidelines. Reflecting the demographics of South Carolina, the BCN enrolls a population that is approximately 60% African American, and the majority reside in a county that is classified as rural by the United States Census Bureau. The objective of this investigation was to examine the relation between race, compliance, and total time of follow-up of suspicious breast abnormalities among women participating in the BCN.
MATERIALS AND METHODS
Because de-identified data that were collected for nonresearch purposes were used for the current investigation, an exemption of approval from the Institutional Review Board was granted by the University of South Carolina Office of Research.
Patients for this investigation were BCN participants. From its inception in 1992 to June 30, 2005, the BCN performed >50,000 mammography screenings. The BCN is implemented through the South Carolina Department of Health and Environmental Control and is funded by the Centers for Disease Control and Prevention. The program provides services for underserved women ages 47 years to 64 years who are at or below 200% of the federal poverty level and who do not have insurance or have insurance that covers only hospital care. The BCN provides screening services, such as mammograms and clinical breast examinations, diagnostic procedures, case management, and community education on breast cancer and early detection. Eligible women are recruited into the BCN through active in-reach efforts through primary care providers from federally qualified health centers; outreach through the American Cancer Society, South-Atlantic Division; and various media mechanisms. The BCN serves South Carolinian women through outreach workers across the entire state. The BCN is a network of public and private partnerships and comprises >250 healthcare providers, including federally funded primary care centers in the SC Primary Health Care Association; private physicians, including surgeons and gynecologists; and laboratories, university-sponsored clinics, free clinics, regional medical centers, and radiology facilities that provide screening and follow-up services. Community partners include over 800 volunteers, many of whom are members of local task forces that assist in referring women to screening sites. According to BCN protocol, all participants with a breast abnormality are provided case management services, which work with the participant to help her receive all diagnostic services within 60 days. Breast diagnostic workup is covered by the BCN program.
In accordance with the standard of care, films from all women undergoing screening mammography were classified according to the Breast Imaging Reporting and Data System (BI-RADS).30 The following coding definitions were used: 1 indicates negative; 2, benign; 3, probably benign; 4, suspicious for malignancy; and 5, highly suggestive of malignancy. Women were included in the analyses if they were African American or European American and if they had a BI-RADS rating of either 4 or 5 (n = 1630), indicating the need for further diagnostic procedures. The BCN protocol does not require diagnostic workup for a BI-RADS rating of 3. The recommended length of follow-up for this category is from 3 months to 6 months. Thus, women with this BI-RADS rating were excluded from the current analysis. The study sample consisted of 729 African-American women and 901 European-American women. A retrospective cohort study design was used to determine whether additional diagnostic procedures, including mammographic views, ultrasound, or biopsy, were undertaken. For women who had a pathologically diagnosed breast carcinoma, we retrieved additional information, such as tumor histology, behavior, stage, and size (n = 407). Among the women who underwent a breast biopsy, 187 were European American, and 220 were African American.
Women were considered to have complete follow-up if their recommended workup was recorded as complete by the BCN. In keeping with BCN guidelines, a complete workup indicates that the diagnostic testing is complete and that the final diagnosis (whether benign or malignant) and the date of final diagnosis are known. For women who were diagnosed with breast cancer, disease stage at diagnosis and tumor size also were recorded at the time of final diagnosis. An incomplete workup was defined as a curtailed planned workup, a pending workup, a refused workup, or if the woman was lost to follow-up. If a woman severed her relationship with the BCN program and had her diagnostic workup performed by another provider, then her workup was defined as refused. A woman was considered lost to follow-up if she died, if she moved before her workup started, or if tracking efforts were attempted but failed. The date at which this determination was made was used for our analyses.
Total yearly family income, insurance status, and previous mammogram and breast symptoms were self-reported at the time of the woman's visit with the BCN. Breast symptoms included a lump, bloody nipple discharge, dimpling, ulceration, or inflammation of the skin. Diagnostic procedures included additional mammographic views, repeated clinical breast examinations or surgical consultations, breast ultrasound studies, breast biopsy or lumpectomies, fine-needle aspirations, and other procedures, such as stereotactic localization, magnetic resonance imaging, and metastatic workup (eg, a bone survey).
Tumor size, stage, and behavior were reported for women who had a diagnosis of breast cancer. Tumor size was categorized into the following groups: from 0 cm to 1 cm, from 1 cm to 2 cm, from 2 cm to 5 cm, >5 cm, and unknown. Tumor stage was reported according to the American Joint Committee on Cancer (AJCC).31 Tumor behavior was defined as either in situ or invasive.
Descriptive statistics, stratified by race, were calculated for all demographic and breast screening variables. Differences between African-American women and European-American women were analyzed using the chi-square test for categorical measures and the t test for continuous measures. All P values were 2-tailed, and significance was assessed at a Type I error rate of α = .05.
Logistic regression was conducted to model the relation between race and whether the recommended workup was completed. Other covariates that were included in these models were age, healthcare provider, number of procedures, income, and insurance type. Because there was a finite number of mammography providers, we had to consider the possibility of correlation among observations within the provider variable. After investigating several parametric structures for within-provider correlation, all testing indicated that the pooled model was the most appropriate approach where inference adjusted for possible within-provider correlation using the empirical (modified sandwich) variance estimator.32
Kaplan-Meier survival curves were compared using the log-rank test for equality. Cox proportional hazards modeling was the primary statistical method used for the analysis of follow-up time. Those women who had incomplete workups were categorized as censored observations. Two measures of time—the number of days between the first mammogram and the date that the status of the workup was finalized and the number of days between the first clinical breast examination and the date that the status was finalized—were analyzed in this investigation. For women who completed their workup, the date that the status was finalized corresponded to the date of a final diagnosis (either benign or malignant). A final diagnosis was documented only after the individual had completed all recommended diagnostic procedures, including additional mammographic views, ultrasound studies, and biopsy (if recommended). For those women who had an incomplete workup, the date corresponded to the date when their status (incomplete, refused, lost to follow-up, or pending) was assessed.
Like in our logistic models, we evaluated the possible correlation of repeated observations within each mammography provider for our estimated Cox models. Further testing indicated that the pooled (independence) Cox regression model was the most appropriate method.33 The proportional hazards assumption was tested, and the assumption was not violated for the main predictor variable of race (P = .11).
Study population characteristics are displayed in Table 1. The mean age of the women was 52 years and did not differ significantly between African-American women and European-American women. However, income levels varied by race: African-American women had a mean income of $1294 less than European-American women (P = .0003). African-American women were also less likely to have insurance compared with their European-American counterparts. The majority of women did not experience breast symptoms at the time of their appointment. African-American women were more likely to have an abnormal clinical breast examination than European-American women. In both groups of women, 91% had completed follow-up of abnormal breast findings. In addition, there was not a significant difference in the number of diagnostic procedures performed or in the number of previous mammograms performed between African-American women and European-American women.
|% (No. of Patients) or Mean±SD|
|Demographic Characteristic||African Americans, n=729||European Americans, n=901||P*|
|Age at diagnosis, y||52±9.3||52±10.18||.46|
|Yes||20 (184)||24 (174)||.089|
|No||77 (695)||75 (545)|
|Unknown||3 (10)||1 (10)|
|Clinical breast examination result|
|Normal||51 (463)||45 (329)||.04|
|Abnormal||44 (396)||50 (363)|
|Not needed||5 (42)||5 (37)|
|Yes||52 (471)||48 (352)||.27|
|No||46 (413)||50 (362)|
|Unknown||2 (17)||2 (15)|
|Status of mammography final diagnosis|
|Workup complete||91 (817)||91 (662)||.93|
|Refused, pending, incomplete||9 (84)||9 (67)|
|None||78 (701)||73 (527)||.008|
|Hospitalization only||6 (51)||5 (37)|
|Unreported||16 (149)||22 (165)|
|No. of procedures|
|0||7 (48)||7 (64)||.28|
|1||48 (354)||44 (396)|
|2||29 (215)||33 (300)|
|3||12 (86)||13 (119)|
|>4||4 (26)||3 (22)|
|In situ||4 (40)||5 (38)||.73|
|Invasive||20 (180)||20 (149)|
|Breast cancer not diagnosed/unknown||76 (681)||75 (542)|
Clinical characteristics of the women who were diagnosed with breast cancer within the BCN are listed in Table 2. Among the women who were diagnosed with breast cancer, there was no difference between African-American women and European-American women with regard to tumor size, stage, or behavior. For both groups, there was a greater percentage of tumors >2 cm and <5 cm, and the tumors were more likely to be invasive than in situ.
|% (No. of Patients)|
|Clinical Characteristic||African Americans, n=220||European Americans, n=187||P*|
|Tumor size, cm|
|0-1||8 (18)||8 (15)||.54|
|>1 to 2||20 (43)||22 (42)|
|>2 to 5||30 (65)||29 (54)|
|>5||15 (33)||10 (18)|
|Unknown||27 (61)||31 (58)|
|In situ||18 (40)||20 (38)||.58|
|Invasive||82 (180)||80 (149)|
|Stage I/local||23 (50)||21 (39)||.90|
|Stage II, III/regional||44 (98)||48 (90)|
|Stage IV/distant||4 (9)||4 (8)|
|Unknown||29 (63)||27 (50)|
The relation between the various available covariates and the overall completion of recommended workup is displayed in Table 3. Regression analyses indicated that a complete workup was associated with the number of previous procedures and income but was not associated significantly with age, type of insurance, or race. Women who had 1 previous procedure were >3 times more likely to complete their recommended follow-up compared with women who did not have any previous procedures (95% confidence interval [CI], 1.71-6.27). For each doubling of income, the odds of completing the workup increased by 10% (95% CI, 1.03-1.19).
|No. of Patients|
|Variable||Incomplete Workup||Complete Workup||RR (CI)|
|No. of procedures|
|Hospital only insurance||59||343||0.51 (0.20-1.30)|
|African American||67||662||1.29 (0.65-2.55)|
Kaplan-Meier curves that compare the number of days between the first mammogram and the date of final status by race are depicted in Figure 1. The graph of the time estimates for race indicates that there was little difference between African-American women and European-American women, although the log-rank test for equality of survival functions was marginally significant (P = .056). The median workup time from the first mammogram to the final status was 34 days for African-American women and 28 days for European-American women.
Kaplan-Meier curves of the time (in days) between the first clinical breast examination and the date of final status are depicted in Figure 2. It is noteworthy that we observed a significant difference in the time to workup completion between African-American women and European-American women (median time, 44 days for African Americans and 40 days for European Americans; P = .02).
Table 4 provides the Cox hazard analysis of factors that influenced the time to completion of the recommended workup. In that analysis, time was measured as the number of days between the first mammogram and the date that final status was determined. Cox analyses suggested that, after adjusting for age, income, number of previous procedures, and insurance, African-American women were 11% less likely to complete their workup than European-American women (P = .09). In addition, the results indicated that, for each previous procedure, women were 30% more likely to complete the workup (P < .0001). With each doubling of income, the likelihood of completing the recommended workup was 1.01 times higher (P = .017). Women with insurance were 1.11 times more likely to complete the recommended workup than women without insurance or women with hospitalization insurance only (P = .05). Age was not significantly associated with completing the workup.
|No. of Patients|
|Variable||Incomplete Workup||Complete Workup||HR (CI)|
|No. of procedures|
|Hospital only insurance||59||343||1.11 (0.99-1.24)|
|African American||67||662||0.89 (0.77-1.02)|
Table 5 contains results from the Cox analysis of factors that influenced the time to completion of the recommended workup when time was assessed from the date of the first clinical breast examination to the date that the status of the workup was finalized. Analyses indicated that, after adjusting for age, income, number of previous procedures, and insurance, African-American women were 12% less likely to complete their workup than European-American women (P = .01). In addition, these results indicate that women who had >1 previous procedure were 32% more likely to complete the workup (P < .0001) than women who had no previous procedures. Age, income, and insurance status were not associated significantly with completing the workup.
|No. of Patients|
|Variable||Incomplete Workup||Complete Workup||HR (CI)|
|No. of procedures|
|Hospital only insurance||59||343||1.07 (0.94-1.22)|
|African American||67||662||0.88 (0.79-0.97)|
Among economically disadvantaged women, race was not associated significantly with overall completion of mammographic workup. However, we did find evidence for racial disparities in the time between the first abnormal clinical breast examination and the determination of final status. After accounting for time, African-American women were significantly less likely to complete their mammographic workup than European-American women.
It is noteworthy that, when time was measured in the number of days between the mammogram and the date of final status, a significant effect of race no longer was evident. Because the clinical breast examination typically precedes the diagnostic mammogram, these findings suggest that the racial differences may occur early in the process. Although the exact protocol will vary according to the clinical site where the patient receives care, the clinical breast examination usually will be completed by a different provider than the provider of the mammographic services. Consequently, structural and environmental factors that could affect the time between the clinical breast examination and the mammogram are communication to the patient from the provider, lengthy scheduling delays, proximity of the mammography clinic to the patient (which could be especially pertinent in a rural setting), and availability of transportation.23, 34-38 Conceptualizing these factors in light of the racial differences that we observed suggests several interesting areas for further research.24, 38-40 Diagnostic delays also may be a result, in part, of deficits in the patient-provider relationship. It has been demonstrated that patient trust in the provider is correlated positively with willingness to seek care and to adhere to treatment recommendations.41 Furthermore, the lack of a usual provider is associated with inadequate follow-up after an abnormal mammogram.42 It has been noted that physician perceptions tended to be more negative regarding lower income and minority women compared with higher income and nonminority women.37, 41, 43 Therefore, African-American women may not adhere to recommendations concerning breast abnormalities because of a lack of trust with their healthcare provider or the lack of a consistent provider because of lower socioeconomic status. It is puzzling to observe that, even for a population in which all services are provided free of charge, income influences a woman's adherence to recommended follow-up. Although the BCN does provide all diagnostic services, up until 2000, there were no provisions for no-cost services once a woman was diagnosed with a breast malignancy. Consequently, this may have influenced a woman's decision to follow-up after a physician's recommendation because of her inability to pay or her fear about paying for additional medical services should she be diagnosed with breast cancer. This is consistent with literature indicating that numerous socioeconomic factors are associated with delayed follow-up of an abnormal mammogram or clinical breast examination, including low household income, other cost issues, and transportation problems.21-24, 34, 40, 44-51
Delayed follow-up of breast abnormalities could result in detecting the breast cancer at a later stage, thus influencing a woman's prognosis and mortality from the disease. Richards and colleagues observed in a meta-analysis that a delayed diagnosis of breast cancer of as little as 3 months was associated with lower survival compared with prompt follow-up.52 Likewise, those authors observed that delays of 3 months to 6 months clearly were associated with increased tumor size, advanced disease stage, and poorer long-term prognosis.
In a previous investigation, our research team examined the effect of delayed diagnosis on mortality in the BCN.53 In this investigation, 1 of the intervals examined was the time between the suspicious mammogram or clinical breast examination and the breast cancer diagnosis. It is noteworthy that we observed no significant association between the diagnosis interval and mortality and or no significant interaction between race and the diagnosis interval. Combined with our findings, this suggests that future studies should focus on the time between clinical breast examination and mammography.
Like any epidemiological investigation, our study had some limitations that are worth noting. Data elements from the NBCCEDP are dictated by the Centers for Disease Control and Prevention. Although we had a wealth of information with which to work, we did not have information on beliefs about screening, health literacy, patient-provider communication and relationship, or system failures. It would be useful to collect this information in future studies to provide a more comprehensive analysis of our findings. In addition, because of small cell sizes, we were forced to collapse the outcome variable “status of the workup” from 4 levels to 2 levels (refused, lost to follow-up, or pending were condensed to incomplete). This may have led to possible misclassification bias, because the factors associated with a refusal, loss to follow-up, or pending workup may be different. Nevertheless, such misclassification of the outcome would be expected to bias the findings toward the null value, thereby strengthening the claim of a true association based on the observed relationship between race and time between the first clinical breast examination and the date of final status.
The current research study has many strengths. The BCN targets rural, medically underserved women of South Carolina, serving a population that is approximately 70% African American. Hence, we were able to study a population that is chronically under represented in the scientific literature. In addition, because the BCN is a statewide program, we were able to follow women over time regardless of where they may have received treatment, thus minimizing losses to follow-up (eg, a woman would not be lost if she moved to another city). Because of the cohort design of the program and our study, we were able to account for past screening history in the investigation, which does appear to affect the time required to complete the diagnostic workup.
In conclusion, the current findings provide evidence for a racial disparity in the time to completion of a diagnostic workup among low-income women enrolled in the South Carolina NBCCEDP: the BCN. Given the target population of the BCN, we believe that these results are particularly applicable to economically disadvantaged African-American women who live in rural areas. The finding that no disparities existed in the overall completion of the workup also are an encouraging evaluation of the NBCCEDP, because it suggests that the program is making progress toward eliminating racial disparities in breast cancer and offers areas for strengthening the overall program (ie, decreasing the total time interval). Overall, these findings highlight the importance of understanding the factors associated with these delays. In addition, they suggest several areas for potential policy changes, such as additional support to the BCN program, to allow the expansion of services. Improving patient adherence to follow-up recommendations and decreasing the time lag between the detection of breast abnormalities and the date of completion may decrease breast cancer mortality rates.
Conflict of Interest Disclosures
Supported by the University of South Carolina, Office of Research and Health Sciences. We also acknowledge funding of the South Carolina Cancer Disparities Community Network through grant 1 U01 CA114601-01 from the National Cancer Institute (Community Networks Program).
- 1Breast cancer disparities in South Carolina: early detection, special programs, and descriptive epidemiology. J S C Med Assoc. 2006; 102: 231-239., , , et al.
- 10Mammograms and healthcare access among US Hispanic and non-Hispanic women 40 years and older. Fam Commun Health. 2006; 29: 80-88., , .
- 12Can racial differences in breast carcinoma survival be explained by access to medical care? Cancer. 2000; 88( suppl): 1268-1269., .
- 13South Carolina Cancer Facts and Figures 2001-2002. Charleston, SC: South Carolina Central Cancer Registry, Office of Public Health Statistics and Information Services, South Carolina Department of Health and Environmental Control; American Cancer Society, Southeast Division; 2001., , , .
- 19Outcomes of modern screening mammography. J Natl Cancer Inst Monogr. 1997; 22: 105-111., .
- 30American College of Radiology. Breast Imaging Reporting and Data System (BI-RADS) Atlas. Reston, Va: American College of Radiology; 2003.
- 31FlemingID, CooperJs, HensenDE, et al, eds. AJCC Cancer Staging Manual. 5th ed. Philadelphia, Pa: Lippincott-Raven; 1998.