• breast cancer;
  • disparity;
  • survival;
  • radiation;
  • rural;
  • minority;
  • elderly


  1. Top of page
  2. Abstract


Definitive local therapy of early stage breast cancer includes adjuvant radiotherapy after breast-conserving surgery (BCS). The authors analyzed factors that influence the receipt of radiotherapy therapy and their resultant impact on outcome.


Using data from the Kentucky Cancer Registry, the authors analyzed the rate of adjuvant radiotherapy for 11,914 women who underwent BCS as a primary surgical treatment for stage 0, I, or II breast cancer between 1998 and 2007. The authors assessed the probability of receiving radiotherapy by using multivariate logistic regression and measured impact on outcome by using Cox survival analysis.


Overall, 66.2% of women received adjuvant radiotherapy for BCS over a 10-year period (annual rate range, 60.9%-70.1%). On multivariate analysis, the rate of receiving radiotherapy was drastically lower for women aged older than 70 years (vs younger) and rural Appalachian (vs non-Appalachian) populations. The rate was modestly lower for African American (vs white) women, those with in situ (vs invasive) disease, and uninsured (vs insured) patients. Lack of radiotherapy was associated with an increased hazard ratio for death of 1.67 (95% CI, 1.508-1.851) on Cox survival analysis when age, stage, tumor size, grade, hormone receptors, smoking, and insurance were factored into the analysis. The 10-year overall survival for patients who received adjuvant radiotherapy versus BCS alone was 79.7% versus 67.6% (P < .0001).


Despite widespread knowledge of the benefit of RT after BCS, the rate of undertreatment remains high, with significant disparities for elderly, rural, minority, and uninsured women. Multidisciplinary management strategies, including accelerated and hypofractionated radiation regimens, are needed to eliminate disparities and improve outcomes. Cancer 2011. © 2010 American Cancer Society.

Appropriate primary local management of preinvasive and early stage breast cancers involves the choice of breast conserving surgery (BCS) followed by radiotherapy (RT) verses mastectomy. Long-term data from multiple randomized studies demonstrates equivalence across all major disease-control endpoints for these 2 approaches; thus, BCS with adjuvant RT is preferred by the overwhelming majority of eligible patients.1-2 As a result, mastectomy rates across the United States have steadily declined over the last few decades.3 Although recent, less mature studies have suggested that BCS alone may be an appropriate choice for well-selected elderly and ductal carcinoma in situ (DCIS) patients, the addition of RT after BCS is recommended for nearly all patients for superior local control and long-term overall survival.4-6

As mastectomy rates have decreased over time, the challenge has been to ensure adequate therapy with consistent delivery of RT after BCS, especially among vulnerable populations who may lack access to oncology services.7-8 In the United States, reports on rates of application of RT after BCS contain estimations that vary widely (range, 65%-95%) according to study type and makeup of the analyzed cohort.7-17 Larger national cross-sectional studies drawn from Surveillance, Epidemiology, and End Results (SEER) and/or Medicare databases tend to show relatively lower rates of RT use (range, 65%-85%).7-12 On the other hand, comparatively smaller studies that involve data extracted from prospective trials,17 audits of comprehensive cancer canters,16, 18 and patient self-reports15 typically show higher RT use (range, 80%-95%). One consistent quality of most of the aforementioned studies is the ability to identify subpopulations of patients underserved by RT access and regular application. These disparities are varied, and may be dramatic, and are most often associated with age, race, and geographic region.8-9, 12, 15-20 In some studies, inadequate treatment has been linked to poorer disease-control endpoints and even overall survival in these patients.14, 21-25

During the last decade, major cancer centers in large cities have paved the way for significant growth and spread of multidisciplinary breast cancer care with the integration of systemic therapies and access to specialized RT procedures. In the United States, approximately 80% of the population lives in or near a major metropolitan canter; thus, the aforementioned studies are heavily influenced by the inclusion of significant numbers of urban patients.26 In fact, subset analyses of nearly all national database studies on this subject indicate that the lowest relative rates of RT use after BCS exist in more sparsely populated regions, especially the South and/or Southeast.8-10, 12, 17

The Commonwealth of Kentucky does not encompass a city listed among the top 25 incorporated entities (according to the United States Census Bureau) nor a top 40 metropolitan statistical area (as defined by the United States Office of Management and Budget). In addition, Kentucky does not contain a National Cancer Institute (NCI)-designated cancer center. The purposes of this study are to quantify the rate of RT use after BCS for preinvasive and early stage breast cancer in this underserved southern state and to identify disparities and barriers to adequate care.


  1. Top of page
  2. Abstract

This retrospective study was approved by the institutional review board at the University of Louisville School of Medicine. The study concept, design, and completion represent a collaborative effort between investigators at the University of Louisville's James Graham Brown Cancer Center (Louisville, Ky) and the Kentucky Cancer Registry at the University of Kentucky's Markey Cancer Center (Lexington, Ky). Data for female-only breast cancer cases diagnosed between 1998 and 2007 were obtained from the Kentucky Cancer Registry (KCR). The study included 11,914 women who met the following inclusion criteria: age at cancer diagnosis was 20 years or older, the cancer was the first primary cancer diagnosed, only AJCC stage 0 (ductal carcinoma in situ), I, and II cases were included, and BCS was given as part of the first course treatment. Cases abstracted from autopsy or death certificate only were excluded.

The KCR is a population-based registry and has been awarded the highest level of certification by the North American Association of Central Cancer Registries for an objective evaluation of completeness, accuracy, and timeliness every year since 1997. The KCR is also part of the Surveillance, Epidemiology, and End Results (SEER) program, which has the most accurate and complete population-based cancer registry in the world. The KCR also links its database annually with the National Death Index (NDI) to capture the most accurate survival information.

For purposes of this analysis, the treatment was categorized into 2 groups: BCS without RT or BCS with RT. BCS was defined as any surgery less than total mastectomy, including partial mastectomy (with or without nipple resection), segmental mastectomy, lumpectomy, tylectomy, quadrantectomy, or reexcision of the biopsy site for gross or microscopic residual disease. Women who received BCS plus confirmed RT were defined as having BCS with RT. The other patients who received BCS were defined as having BCS without RT.

Race, age at diagnosis, urban/rural status, and Appalachian status were primary demographic interests of the study. Urban/Rural status was based on the 2003 Urban-Rural Continuum codes with 1-3 defined as urban and 4-9 as rural. The county-level Appalachian status was based on definitions by the Appalachian Regional Commission. Other demographical and clinical variables included in the study were year at diagnosis, smoking history, insurance status, survival status at the end of the study, primary cancer sequence number, laterality, stage, nodes examined, estrogen receptor and progesterone receptor (ER/PR) status, tumor grade, histology, and tumor size.

The descriptive analysis for demographics and clinical factors was performed. We used chi-square tests to examine associations between treatment and the variables described above. Multivariate logistic regressions were fitted to evaluate the association between RT use and age at diagnosis/race/residence location while controlling for other covariates. The final model included only covariates with a significance level of .05 or less. Goodness of fit was also tested. Kaplan Meier plots and life tables by treatment were examined. Cox survival regression was also performed to assess how treatment and other factors impacted patient survival. All analyses were performed by using SAS statistical software version 9.1 (SAS Institute, Cary, NC). All statistical tests were 2-sided with a P ≤ .05 used to identify statistical significance.


  1. Top of page
  2. Abstract

The study cohort consisted of 11,914 patients who underwent BCS as their primary surgical treatment for stage 0, I, or II breast cancer from 1998-2007. The patient demographics, disease characteristics, and rates of RT receipt are shown in Table 1. The majority of patients were white, between the ages of 50 and 69 years, and nonsmokers. Most patients carried some type of medical insurance and resided in urban and non-Appalachian locations. For more than 90% of patients, ductal carcinoma in situ (DCIS) or early stage breast cancer was their only cancer diagnosis; all others were reported as “first” cancers. Cancers were most commonly stage I, well or moderately differentiated ductal histology, and hormone-receptor positive. Limited or no axillary surgery was performed for most of these preinvasive and early stage patients, and approximately two-thirds (66.2%) received RT. The majority of (86.2%) patients were alive at the time of this study.

Table 1. Demographics of Overall BCS Population (1998-2007)
  • DCIS indicates ductal carcinoma in situ; ER, estrogen receptor; PR, progesterone receptor.

  • a

    “First primary cancer” refers to included patients who had breast cancer qualifying for this analysis, then a metachronous second other cancer diagnosed later.

Age at diagnosis, y  
Smoking history  
 Never smoked604950.8
Insurance status  
 Private insurance648654.4
Primary cancer sequence number1077890.5
 Only primary cancer11369.5
 First primary cancera  
 Stage I617151.8
 Stage II307625.8
ER/PR status  
 ER+ or PR+7436.2
Tumor grade  
 Well differentiated261021.9
 Moderately differentiated438536.8
 Poorly differentiated332127.9
 Ductal carcinomas856171.9
 Lobular carcinomas5114.3
Nodes examined  
 1-4 Nodes401233.7
 ≥4 Nodes430836.2
Adjuvant radiotherapy  
Survival status  

Figure 1 shows the rates of RT use as a function of time. The annual rate ranged from a zenith of 70.1% in 1998 to a nadir of 60.9% in 2001. Since that time, the rate has fluctuated; the most recently measured rate was 66.6% in 2007. Table 2 shows individual interactions of patient and disease characteristics with RT administration in a bivariate analysis. As to patient factors, the most significant predictors of not receiving RT, in order of magnitude, were age ≥70 years (P < .0001), Appalachian location (P < .0001), Medicare-insured status (P < .0001), rural county of residence (P < .0001), and patients with breast cancer as a first (rather than only) cancer diagnosis (P = .016). Race was not found to be significant on bivariate analysis (P = .487). In terms of disease specifics, patient were less likely to receive RT if they had in situ versus invasive disease, which was reflected in the variables of AJCC stage (stage 0, P < .0001), number of lymph nodes examined (none, P < .0001), and hormone-receptor status (unknown, P < .0001). Patients with unusual histologies—other than ductal or lobular variants—were also less likely to receive RT (P < .0001).

thumbnail image

Figure 1. The rate of adjuvant RT after BCS is depicted for all cases of stage 0, I, and II breast cancer from 1998-2007 in the Commonwealth of Kentucky.

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Table 2. Bivariate Analysis of Receipt of Radiotherapy According to Demographic Factors and Disease Characteristics
 Adjuvant Radiotherapy
Age at diagnosis, y    <.0001
Race    .4871
Smoking history    <.0001
 Never smoked192131.8412868.2 
Geographic location    <.0001
County of residence    <.0001
Insurance status    <.0001
 Not insured10434.419865.6 
Primary cancer sequence no.    .016
 Only primary cancer360233.4717666.6 
 First primary cancer42037.071663.0 
Laterality    .7202
AJCC Stage    <.0001
 Stage I180829.3436370.7 
 Stage II101533.0206167.0 
ER/PR status    <.0001
 ER+ or PR+23131.151268.9 
Tumor grade    <.0001
 Well differentiated88834.0172266.0 
 Moderately differentiated139731.9298868.1 
 Poorly differentiated102530.9229669.1 
Histology    <.0001
 Duct carcinomas276032.2580167.8 
 Lobular carcinomas16532.334667.7 
No. of lymph nodes examined    <.0001
 1-4 Nodes99524.8301675.2 
 ≥4 Nodes122828.5308071.5 

Table 3 shows the results of multivariate analyses including the entire list of variables in Tables 1 and 2. The most significant demographic factors associated with a lack of adjuvant RT administration were age ≥70 years (P < .0001), Appalachian residence (P < .0001), and lack of insurance (P = .0201). Race also was found to be significant when the rate of RT after BCS among the black population was compared with white and other races (P = .0108). As to disease specifics, RT was more likely to be administered for patients who had nodal evaluations (P < .0001), patients with less well-differentiated tumors (P < .0001), and known ER/PR status (P = .0004). Unlisted variables were not statistically significant in terms of impact on the administration of RT.

Table 3. Multivariate Logistic Regression Modeling Breast Conservation Surgery (BCS) Without Adjuvant Radiotherapy (RT)
VariableHazard Ratio95% CIP
Age at diagnosis, y  <.0001
Race  .0108
Smoking history  <.0001
 Never smoked1.000 
Geographic location  <.0001
Insurance status  .0201
 Private insurance1.000 
ER/PR status  .0004
 Both positive1.000 
 One positive1.0290.854-1.240 
 Both negative1.1480.967-1.361 
Tumor Grade  <.0001
 Well differentiated1.000 
 Moderately differentiated0.9290.830-1.041 
 Poorly differentiated0.8250.727-0.937 
Nodes examined  <.0001
 1-4 Nodes0.3590.321-0.402 
 ≥4 Nodes0.4550.406-0.509 

Table 4 displays the multivariate Cox regression analysis for survival including all variables shown in Table 1. Unlisted variables were not statistically significant in terms of impact on survival. Advancing age and advancing stage both presented predictable and progressive decrements to overall survival (P < .0001). An increased hazard ratio for death was also seen for smokers (P < .0001), the uninsured, and those with government-subsidized insurance (P < .0001). Hormone-receptor negative and poorly differentiated cancers were also associated with inferior outcome (P < .0001). The receipt of BCS only was independently associated with an increased hazard ratio for death (P < .0001). To reduce the potential confounding effect from the older population, the same analysis was performed for the patients aged younger than 70 years. Similar results were also found for this nonelderly subpopulation, where the lack of RT was significantly associated with an increased hazard ratio of death (HR,1.26; P = .007; full tabular data not shown). Figure 2 is a graphic representation of survival curves for all patients who underwent BCS with or without RT. The 5- and 10-year overall survival for patients who received or did not receive RT were 92.3% versus 84.6% and 79.7% versus 67.6%, respectively (P < .0001). Table 5 breaks down survival data by age and stage related to the administration or lack thereof of RT after BCS. Across both groups, survival was predictably lower for older patients with higher-stage disease. Consistently lower survival was seen for all age and stage subgroups that did not receive RT compared with the corresponding subgroup that did receive RT.

thumbnail image

Figure 2. A Kaplan-Meier plot of overall survival is shown for cases of stage 0, I, and II breast cancer treated with BCS + RT (black) versus BCS alone (red) from 1998-2007 in the Commonwealth of Kentucky.

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Table 4. Cox Survival Analysis for Cases Undergoing Breast Conservation Surgery
VariableHazard Ratio95% CIP
  1. DCIS indicates ductal carcinoma in situ.

Age at diagnosis, y  <.0001
Smoking history  <.0001
 Never smoked1.000 
Insurance status  <.0001
 Private insurance1.000 
Stage  <.0001
 Stage 0 (DCIS)1.000 
 Stage I2.3141.901-2.817 
 Stage II3.4612.745-4.363 
ER/PR status  <.0001
 Both positive1.000 
 One positive1.3061.105-1.544 
 Both negative1.6011.368-1.873 
Tumor grade  <.0001
 Moderately differentiated1.1110.966-1.279 
 Poorly differentiated1.4441.235-1.689 
Adjuvant radiotherapy  <.0001
Table 5. Five- and 10-Year Survival Rates by Treatment and Stage at Diagnosis
AJCC StageBCS with RTBCS without RT
  1. AJCC indicates American Joint Commission on Cancer; BCS, breast-conserving surgery; RT, radiotherapy; SE, standard error of the mean; DCIS, ductal carcinoma in-situ.

DCIS (Total)96.1%0.00685.6%0.01793.0%0.00880.9%0.020
 Age <50 y99.1%0.00599.1%0.00599.2%0.00697.6%0.017
 Age 50-69 y97.8%0.00689.3%0.02196.3%0.00988.8%0.022
 Age ≥70 y87.1%0.02360.9%0.05081.7%0.02454.0%0.050
Stage I (Total)93.1%0.00481.6%0.01084.4%0.01064.4%0.020
 Age <50 y96.6%0.00792.1%0.01493.5%0.01684.6%0.044
 Age 50-69 y94.3%0.00686.0%0.01294.0%0.00984.8%0.023
 Age ≥70 y86.9%0.01262.3%0.02671.4%0.01837.8%0.031
Stage II (Total)88.0%0.00871.8%0.01675.3%0.01557.5%0.026
 Age <50 y90.8%0.01282.7%0.02088.6%0.02178.4%0.039
 Age 50-69 y88.8%0.01173.4%0.02284.4%0.01967.4%0.044
 Age ≥70 y80.1%0.02446.2%0.04652.2%0.03127.3%0.039


  1. Top of page
  2. Abstract

In the postmastectomy era, the standard of care for locoregional management of DCIS and early stage breast cancer is breast-conserving surgery (BCS) followed by a course of whole-breast radiotherapy (RT). As the breast-conservation approach has increased in popularity during the last 2 decades (since the defining 1991 NCI consensus conference2), greater cooperation has been required among surgeons and radiation oncologists to facilitate adequate therapy. Because BCS alone has been shown to be associated with an increased risk of locoregional recurrence and inferior long-term overall survival, the consistent and reliable delivery of RT is of vital importance.4 As opposed to the “one-stop” approach of mastectomy, a strategy of BCS plus RT places greater requirements on patients to coordinate therapies and adhere to treatment. The necessity exists not only for adequate access to RT but also for entrance into the adjuvant breast cancer system in general, which includes systemic hormonal therapy and cytotoxic therapy as well as active post-treatment surveillance. The greater complexity involved in multidisciplinary care, especially when oncology services are not consolidated into comprehensive cancer centers, leaves ample opportunity for therapeutic disparities to develop in vulnerable populations.8

During the past 2 decades, numerous studies have attempted to quantify the overall rates of and barriers to delivery of adjuvant RT in US women who undergo BCS for preinvasive and early stage breast cancer. Large SEER database studies, including those linked with Medicare records, have indicated an overall use of RT rate8-10, 12 averaging 73%-75%. These large national registry studies include hundreds of thousands of patients and are useful in providing a “snapshot” of therapeutic trends and provision of care, but they are frequently criticized for their tendency to underestimate these endpoints.27-28 Although the accuracy of registry data are inferior to actual reviews of medical records, registry data have substantial strength in estimating the application of hospital-based services, such as surgery and RT, especially in more recent studies.19, 27-28

Although smaller in scale, other approaches to estimating RT rates have attempted to overcome the perceived shortcomings of registry studies. Audits of comprehensive cancer centers serving large urban populations have shown higher RT rates of 84%-91%.16, 18 The highest estimated rate of RT (approximately 93%) was reported recently by Jagsi et al in a study that linked SEER data to patient self-reports in the metropolitan areas of Detroit and Los Angeles.15 All of the aforementioned studies, however, suffer from significant selection bias, which would tend to favor overestimation of RT rates. Indeed, Chagpar et al, in an audit of the RT rate in a the prospective, randomized North American Fareston versus Tamoxifen Adjuvant (NAFTA), found a rate of approximately 80%, similar to registry study estimates.17 Our analyses, which used SEER methodologies, showed an overall rate of RT (66.2%) that is significantly lower than that reported in similar studies performed over the same time period. However, the relatively low rate of RT use in Kentucky is similar to that found in studies reporting specific numbers (66%-72%) from the South/Southeast regions of the United States.8-10, 12, 17

Despite differences in overall RT rates estimated by the above-referenced studies, they are reliable in quantifying disparities in the application of RT among subpopulations of patients. Underuse of RT is consistently identified in elderly,8-9, 12, 17, 20 poor/uninsured16, 22-23, 29, and underserved racial-minority9-11, 18 populations. In addition, nationwide studies in the United States have regularly revealed geographic disparity, with the lowest rates of RT in the South and Southeast regions.8, 16-17 These more sparsely populated regions tend to have shortages of oncology resources, requiring patients to travel greater distances to receive adequate care.13, 20, 30-31 Our study largely confirms these previously published reports, showing significant disparities in the use of RT among elderly, African American, and uninsured populations. One of our largest differences, however, was identified among rural/Appalachian patients, a population largely unique to our state and region.

Multiple studies have shown that the lack of RT after BCS has real consequences for these vulnerable populations, where inadequate therapy is ultimately associated with inferior outcomes. A SEER study of more than 100,000 women with stage I-IIIA breast cancer who also qualified for both Medicare and Social Security Disability Insurance were found to be less likely to undergo RT (RR, 0.83; 95% CI, 0.77-0.90) and, subsequently, had a higher overall mortality rate (HR, 2.02; 95% CI, 1.88-2.16) and breast-cancer–specific mortality rate (HR, 1.31; 95% CI, 1.18-1.45).23 A SEER-Medicare study of 7791 patients by Gold et al also found that patients who have incomplete RT have a higher risk of overall mortality (HR, 1.32; 95% CI, 1.06-1.63).14 In a study of 1837 women aged 65 years or older treated within the National Cancer Institute Cancer Research Network, women lacking RT after BCS had a higher breast cancer-specific mortality (HR, 2.19; 95% CI, 1.51-3.18; P < .001).25 Similar numbers have been reported for studies conducted outside the United States.21, 24 Our report primarily confirms this pattern of poor overall survival outcome among women who do not receive RT after BCS (HR, 1.67; 95% CI, 1.508-1.851).

However, all of these associations between inadequate application of RT and inferior disease-specific or overall survival are likely confounded by multiple unfavorable variables. Nonreceipt of RT has been linked to higher levels of medical comorbidity and disability.18-19, 22 African Americans and Hispanics who do not receive RT after BCS are also less likely to receive other standard-of-care measures such as documentation of hormone-receptor status and surveillance mammography.11 Finally, omission of RT is also found to be associated with omission of appropriate systemic therapy, suggesting a linkage to adjuvant treatment administration.16, 32

Because omission of RT after BCS in well-selected elderly (aged ≥70 years) has recently been established,6 the most clinically significant disparity discovered on multivariate analysis was in the rural/Appalachian population (HR, 1.742; 95% CI, 1.584-1.915). Several factors exist in rural communities that contribute to healthcare disparities, including high percentages of uninsured patients, disproportionate elderly populations, higher levels of medical comorbidities, physician shortages, and lack of transportation options and assistance.33 Rural primary care physicians report taking an “active role” in the decision-making process for nearly one-third of their patients who receive a new diagnosis of cancer, but these physicians often have very low levels of awareness of current NCI guidelines, especially of RT after BCS guidelines.34 As a result, delivery of oncology services to rural patients typically does not improve over time, and in fact as evidence-based recommendations become more complicated with layering and tailoring of therapies, the rate of appropriate adjuvant treatment may actually decline.7, 35 Because approximately 20% of the US population lives in an area qualified as rural,26 disparities similar to that found in our study may have broad-based implications for the country as a whole.


Adjuvant RT after BCS is disproportionately omitted in elderly, rural, racial-minority, and uninsured populations, and there has been little improvement for these patients during the last decade. Our study is the largest of its kind specifically focused on an underserved Southern US population, and the largest clinically significant disparity was found among rural patients. This report is 1 of the largest studies to date to identify an independent association of lack of RT after BCS with an increased hazard ratio for death. All registry studies have limitations related to the lack of breadth and depth of information contained within a full medical record, and ours is no exception. Information that is absent from the SEER database that may confound these data includes the presence, type, and severity of medical comorbidities, referral patterns for and compliance with radiotherapy, and use of outpatient systemic therapies (chemotherapy and hormone therapy). Even so, our results suggest that lack of application of RT after BCS may be a reliable indicator of inadequate access to other adjuvant therapies and poor post-treatment surveillance. Incentive programs focused on multidisciplinary care as a quality endpoint must be targeted to these underserved populations. Cost-effective alternatives to conventionally fractionated RT must be investigated and widely implemented to improve treatment access for vulnerable patient populations.


  1. Top of page
  2. Abstract
  • 1
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    Anderson RT, Kimmick GG, Camacho F, et al. Health system correlates of receipt of radiation therapy after breast-conserving surgery: a study of low-income Medicaid-enrolled women. Am J Manag Care. 2008; 14: 644-652.
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