Abstract
Background:
Healthcare disparities in Appalachia are well documented. However, no previous studies have examined possible differences in the utilization of breast reconstruction (BR) in Appalachia. This study aims to determine if a disparity in BR utilization exists in women from Appalachia Kentucky.
Methods:
A retrospective, population-based cohort study was conducted from January 1st, 2006 to December 31st, 2015. The Kentucky Cancer Registry was queried in order to identify population-level data for female patients diagnosed with breast cancer and treated with mastectomy. A multivariate logistic regression model controlling for patient, disease, and treatment characteristics was constructed in order to predict the likelihood of BR.
Results:
Bivariate testing showed differences (p < .0001) in BR utilization between Appalachian and non-Appalachian women in Kentucky (15.0% and 26.3%, respectively). Multivariate analysis showed that women from Appalachia (OR 0.54, CI(95) 0.48 – 0.61; p < .0001) were less likely to undergo BR than non-Appalachian women. Interestingly, the rate of BR increased over time in both Appalachian (r = 0.115; p < .0001) and non-Appalachian women (r = 0.148; p < .0001).
Conclusion:
Despite the benefits of BR, women from Appalachia undergo BR at lower rates and are less likely to receive BR than non-Appalachian Kentuckians. Although the rates of BR increased over time in both populations, access to comprehensive breast cancer care remains a challenge for women from Kentucky’s Appalachian Region.
Keywords: Breast Cancer, Breast Reconstruction, Appalachia, Health Disparity
Introduction
Breast cancer is the most common non-skin cancer among females, affecting nearly 1 in 8 women in the U.S. The National Cancer Institute estimates that 266,120 new diagnoses of invasive breast cancer will be made in 2018.1 Of those diagnosed, it is estimated that nearly 40% of those patients will require mastectomy.2 Breast reconstruction (BR) has been shown to be oncologically safe and is a valuable part of comprehensive breast cancer care.3 The benefits of BR are well documented and include significant improvements in surgical outcomes such as quality of life. Other psychosocial benefits include improved self-esteem, body image and sexuality, and reduced concerns of cancer recurrence.4–6 Despite this, less than half of patients requiring mastectomy are offered BR at the time of diagnosis and fewer than 20% of mastectomy patients choose to undergo reconstruction.7 Moreover, only 23% of women even understand the breadth of reconstructive options available.7
The Women’s Health Care and Cancer Rights Act (WHCRA) of 1998 mandated that insurance companies, Medicare, and Medicaid provide coverage for BR following mastectomy, which includes reconstruction of the contralateral or non-diseased breast in order to achieve symmetry. Despite the benefits of BR and legislative efforts aimed at improving healthcare coverage for BR, reconstruction rates remain low and range anywhere from 5 – 42% . Moreover, significant disparities in BR utilization, particularly in medically underserved populations including African American and Hispanic women,8 as well as women from rural areas have been reported.9 Clouding the interpretation of these findings is the fact that there is wide geographic variation in the reported rates of BR utilization.10
Appalachia is a geographic region that extends from southern New York to Mississippi. Nearly twenty-five million people reside in the Appalachian region, making up approximately 8% of the United States population,11 yet it remains understudied. In Kentucky, approximately 1.7 million (26%) people call Appalachia home. Cancer rates are higher in Appalachia compared to the rest of the country and within this region, Appalachian Kentucky has the highest overall cancer incidence. Furthermore, the Appalachian region has an elevated rate of unstaged cancer, suggesting that the area lacks access to cancer-focused health care.
The existing BR literature has largely focused on examining differences in the rate of BR utilization in the general population, the medically underserved, and rural populations. However, little is known about the utilization of BR specifically in Appalachia, which is concerning given the size and unique challenges facing this population. Thus, the overarching goal of this study is to determine if differences exist in post-mastectomy BR utilization along the Appalachian divide in Kentucky. We hypothesize that women from Appalachian Kentucky are less likely to receive BR than their non-Appalachian counterparts.
Methods
A retrospective, population-based cohort study was conducted using data from January 1st, 2006 to December 31st, 2015. This study was approved by the Institutional Review Board at the University of Kentucky.
Data Sources
The Kentucky Cancer Registry (KCR) served as the primary data source. KCR is part of the National Cancer Institute’s Surveillance, Epidemiology, and End Results (SEER) program as well as the Centers for Disease Control and Prevention’s National Program of Cancer Registries and has received the highest level of accreditation (Gold) from the North American Association of Central Cancer Registries for data quality. KCR was accessed in order to identify population-level data including patient demographics and case characteristics for adult female patients, ages 18–75 years diagnosed with breast cancer and treated with mastectomy over the study timeframe. Three types of data were collected: patient, disease, and treatment-related factors. Patient factors were age at diagnosis and race. Disease characteristics included AJCC stage as well as hormone receptor status. Treatment factors included mastectomy type, radiation status, BR status, and, if applicable, type of reconstruction.
A second data source, Plastic Surgeon Match ™, was accessed to identify the number of plastic surgeons by region. Plastic Surgeon Match ™ is made available online by the American Society of Plastic Surgeons (ASPS). In order to identify which plastic surgeons offered reconstructive services for breast cancer, the filters breast reconstruction, Transverse Rectus Abdominus Myocutaneous (TRAM) flap reconstruction, and free-flap breast reconstruction were applied.
Statistical Analysis
Patients were divided into mastectomy-only (n = 9,214) and mastectomy plus BR (n = 2,822) groups and stratified by Appalachian status. Appalachian status was determined by matching patient county of residence at time of diagnosis to Appalachian counties as defined by the Appalachian Regional Commission.12 Patient characteristics were compared according to Appalachian status. Age at diagnosis was dichotomized into a binary variable for greater than the median age of 61 years. Categorical variables were reported as frequencies (n) and column percentages (%) and compared using chi-square tests. Continuous variables were tested for normality using the Shapiro-Wilk test for normality and histograms. Normally distributed continuous variables were reported using means and standard deviations (SD) and compared using t-tests and ANOVAs. Chi-square tests were used to examine the association of BR with Appalachian status. Pearson’s correlation (r) was used to assess trends in BR over the study period.
A multivariate logistic regression model controlling for patient, disease, and treatment related factors was used to predict BR. The likelihood of undergoing BR was reported in odds ratios (OR) using a 95% confidence interval (CI). Model goodness-of-fit was tested using the Hosmer-Lemeshow goodness-of-fit test. Statistical significance was set at p ≤ 0.05. All statistical analyses were performed using R programming language, version 3.4.3 (Austria, Vienna; R Core Team).
Results
Overall, 12,036 patients underwent mastectomy and were included in the study. The primary outcome of this study was to determine if there were differences in BR utilization between Kentucky Appalachian and non-Appalachian women. Patient demographics and case characteristics are summarized in Table 1. The mean age of the patient population at time of diagnosis was 61 ± 13.5 years. As expected, the majority of patients were non-Appalachian (74.6%), and Appalachians made up 25.4% of the study population. Patients were primarily of white race (92.8%), followed by blacks (6.4%), and all other races (0.8%). Private insurance (46.3%) was the predominate payer type, followed closely by Medicaid (42.3%), and then Medicare (8.1%), uninsured (1.8%), Tricare/VA (1.0%), and unknown payer group (0.5%). AJCC stage 0-II accounted for 80.1% of patients, while 18.2% of patients presented in stage III stage or stage IV; AJCC staging was unknown in 1.8% of patients. A total of 17.9% of patients received adjuvant or neoadjuvant radiation therapy. Hormone receptor positivity for estrogen receptor and progesterone receptor was 73.7% and 62.9%, respectively. Total mastectomies (61.0%) were performed most frequently, followed by modified radical (36.5%), radical (0.4%), extended radical (0.03%), nipple-sparring (1.3%) mastectomies, and mastectomies not otherwise specified (0.7%).
Table 1.
Patient demographics and case characteristics stratified by Appalachian status.
| All cases | Appalachian status | p | ||
|---|---|---|---|---|
| Non-Appalachia | Appalachia | |||
| Total cases, n (%) | 12,036 (100) | 8,978 (74.6) | 3,058 (25.4) | |
| Age at diagnosis Mean (SD) | 61.1 (13.5) | 61.0 (13.7) | 61.4 (12.7) | .1602 |
| Age > median (61 years), n (%) |
5,910 (49.1) | 4,347 (48.4) | 1,563 (51.1) | .0107 |
| Race, n (%) | ||||
| White | 11,165 (92.8) | 8,158 (90.9) | 3,007 (98.3) | |
| Black | 773 (6.4) | 734 (8.2) | 39 (1.3) | < .0001 |
| Other | 98 (0.8) | 86 (1.0) | 12 (0.4) | |
| AJCC stage, n (%) | ||||
| 0 | 1,655 (13.8) | 1,314 (14.6) | 341 (11.2) | |
| I | 3,952 (32.8) | 3,012 (33.5) | 940 (30.7) | |
| II | 4,029 (33.5) | 2,958 (32.9) | 1,071 (35.0) | < .0001 |
| III | 1,838 (15.3) | 1,309 (14.6) | 529 (17.3) | |
| IV | 349 (2.9) | 241 (2.7) | 108 (3.5) | |
| Unknown | 213 (1.8) | 144 (1.6) | 69 (2.3) | |
| Radiation status, yes/no, n(%) |
2,151 (17.9) | 1,612 (18.0) | 539 (17.6) | .7018 |
| Hormone receptor status, n (%) |
||||
| ER positivity | 8,874 (73.7) | 6,660 (74.2) | 2,214 (72.4) | .121 |
| PR positivity | 7,565 (62.9) | 5,662 (63.1) | 1,903 (62.2) | .382 |
| Mastectomy type, n (%) | ||||
| Nipple sparring | 158 (1.3) | 125 (1.39) | 33 (1.1) | |
| Total | 7,345 (61.0) | 5,644 (62.9) | 1,701 (55.6) | |
| Modified radical | 4,392 (36.5) | 3,115 (34.7) | 1,277 (41.8) | < .0001 |
| Radical | 52 (0.4) | 39 (0.4) | 13 (0.4) | |
| Extended radical | 4 (0.03) | 3 (0.03) | 1 (0.03) | |
| NOS | 85 (0.7) | 52 (0.6) | 33 (1.1) | |
| Mastectomy
laterality, n (%) |
||||
| Unilateral | 8,952 (74.4) | 6,568 (73.2) | 2,384 (78.0) | <.0001 |
| Bilateral | 3,084 (25.6) | 2,410 (26.8) | 674 (22.0) | |
| Payer status, n (%) | ||||
| Private | 5,575 (46.3) | 4,433 (49.4) | 1,142 (37.3) | |
| Medicaid | 5,085 (42.2) | 3,691(41.1) | 1,394 (45.6) | |
| Medicare | 973 (8.1) | 580 (6.5) | 393 (12.9) | <.0001 |
| Uninsured | 222 (1.8) | 145 (1.6) | 77 (2.5) | |
| Tricare/VA | 117 (1.0) | 94 (1.0) | 23 (0.8) | |
| Unknown | 64 (0.5) | 35 (0.4) | 29 (0.9) | |
| Breast
reconstruction, n (%) |
2,822 (23.4) | 2,362 (26.3) | 460 (15.0) | <.0001 |
SD, Standard Deviation; VA, Department of Veterans Affairs; ER, estrogen receptor; PR, progesterone receptor; NOS, not otherwise specified.
When comparing non-Appalachians to Appalachians, differences were observed in median age, race, AJCC stage, mastectomy type, mastectomy laterality, and payer status. The predominant race in both populations was white, while Appalachians (98.9%) had a higher proportion of being white than non-Appalachians (90.9%) (p < 0.0001). Non-Appalachian patients presented in AJCC stage 0 or I at higher rates than Appalachians, who typically presented in stages II-IV (p < 0.0001). Differences (p < 0.0001) were also noted with regard to mastectomy type. Briefly, total mastectomies were the most common type of mastectomy performed in both Appalachians (55.6%) and non-Appalachians (62.9%). Modified radical mastectomies were performed at a higher frequency in Appalachians (41.8%) than non-Appalachians (34.7%). With respect to mastectomy laterality, unilateral mastectomy was more common in Appalachians (78.0%) than non-Appalachians (73.2%) as was bilateral mastectomy (26.8% versus 22.0%, respectively). Private insurance was the predominant payer type in non-Appalachians (49.4% versus 37.3%), while Medicaid was the major payer type in Appalachians (45.6% versus 41.1%) (p <0.0001).
Breast Reconstruction Utilization
Overall, 2,822 (23.4%) patients underwent BR. Of those, non-Appalachians accounted for the majority of reconstructions when compared to Appalachians (83.7% versus 16.3%; p < 0.0001). BR characteristics stratified according to Appalachian status are listed in Table 2. The rate of BR among Appalachian and non-Appalachian women was 15.0% and 26.3%, respectively (p < 0.0001). Bilateral reconstruction (49.9%) was more common than unilateral reconstruction (44.5%) and 5.6% of reconstructions were not specified with respect to laterality. Implant-based reconstruction (39.6%) was the most common reconstruction type, followed by autologous tissue (22.0%), and combined (autologous plus implant-based) reconstruction (12.8%), while 25.6% of reconstructions were not specified. Differences in BR utilization (p < 0.001), reconstruction laterality (p < 0.003), and reconstruction type (p < 0.0001) were also noted between the cohorts.
Table 2.
Breast reconstruction stratified by Appalachian status.
| Categories | All cases | Appalachian status | p | |
|---|---|---|---|---|
| Non-Appalachia | Appalachia | |||
| Breast reconstruction, n (%) | 2,822 (100) | 2,362 (83.7) | 460(16.3) | < .0001 |
| Reconstruction laterality, n (%) | ||||
| Unilateral | 1,255 (44.5) | 1,082 (45.8) | 173 (37.6) | |
| Bilateral | 1,409 (49.9) | 1,155 (48.9) | 254 (55.2) | <.003 |
| NOS | 158 (5.6) | 125 (5.3) | 33 (7.1) | |
| Reconstruction type, n (%) | ||||
| Implant-based | 1,118 (39.6) | 965 (40.9) | 153 (33.3) | |
| Autologous tissue | 621 (22.0) | 533 (22.6) | 88 (19.1) | <.0001 |
| Combined | 361 (12.8) | 295 (12.5) | 66 (14.3) | |
| NOS | 722 (25.6) | 569 (24.1) | 153 (33.3) | |
Combined, autologous tissue and breast implant; NOS, Not otherwise specified.
Trends in Breast Reconstruction
Pearson’s correlation showed that BR utilization increased over time in Appalachian (r = 0.115; p < .0001) and non-Appalachian women (r = 0.148; p < .0001). More specifically, BR utilization increased from 8.8% to 22.7% in the Appalachian group, and increased from 14.7% to 35.9% in the non-Appalachian group over the study period (Figure 1).
Figure 1.
Trends in Breast Reconstruction Rates Over Time Stratified by Appalachian Status
Likelihood of Receiving Breast Reconstruction
In order to determine if differences existed in the likelihood of receiving BR between Appalachian and non-Appalachian women, a multivariate logistic regression model controlling for age, race, primary payer status, AJCC stage, and radiation status was constructed (Table 3). Multivariate analysis showed women from Appalachia (OR 0.54, CI 0.48 – 0.61; p < .0001) were approximately 46% less likely to undergo BR than non-Appalachian women. Age greater than the median (61 years) was found to decrease the likelihood of BR (OR 0.32, CI 0.28 – 0.37; p < 0.0001). When compared to women of white race, blacks (OR 0.78, CI 0.64 – 0.95; p < 0.01), and women of other races (OR 0.50, CI 1.06 – 2.56; p < 0.03) were less likely to undergo BR. When compared to having private insurance, having Medicare (OR 0.46, CI 0.38 – 0.54; p < 0.0001), Medicaid (OR 0.26, CI 0.22 – 0.31; p < 0.0001), or being uninsured (OR 0.21, CI 0.13 – 0. 32; p < 0.0001) were all found to be negative predictors of receiving BR.
Table 3.
Multivariate logistic regression model predicting breast reconstruction. n = 12,036.
| Variable | OR | 95% CI | p |
|---|---|---|---|
| Age > median (61 years) | .318 | .277 – .365 | < .0001 |
| Race | |||
| White (***) | *** | *** | *** |
| Black | .778 | .636 – .948 | .0137 |
| Other | .502 | 1.061 – 2.563 | .0255 |
| Primary payer | |||
| Private (***) | *** | *** | *** |
| Medicaid | .261 | .223 – .305 | < .0001 |
| Medicare | .457 | .382 – .544 | < .0001 |
| Uninsured | .205 | .126 – .317 | < .0001 |
| Tricare/VA | 1.104 | .741 – 1.635 | .6251 |
| Unknown | .363 | .163 – .721 | .0068 |
| AJCC pathologic stage | |||
| 0 (***) | *** | ||
| I | .644 | .562 – .739 | < .0001 |
| II | .429 | .372 – .494 | < .0001 |
| III | .206 | .166 – .255 | < .0001 |
| IV | .054 | .027 – .096 | < .0001 |
| Unknown | .312 | .201 – .471 | < .0001 |
| Radiation used | .767 | .656 – .895 | .0008 |
| Appalachian status | .540 | .478 – .610 | < .0001 |
AJCC, American Joint Committee on Cancer;
, referent category.
Reconstructive Plastic Surgeons by Region
The total number of reconstructive plastic surgeons located in Appalachia and non-Appalachia that offer reconstructive breast procedures was 1 and 20, respectively.
Discussion
This study compared post-mastectomy BR utilization among women from Appalachian and non-Appalachian Kentucky. Consistent with the stated hypothesis, a significant disparity in BR utilization was found. Appalachian women received significantly less BR operations and were less likely (46%) to receive BR compared to those that were non-Appalachian. Increasing age and advancing pathologic stage have been shown to decrease the likelihood of receiving BR. In our study, the Appalachian cohort was slightly older and presented at later AJCC stages which could have had an impact on BR utilization rates however, these factors were controlled for in our regression model. Consistent with prior studies,8,13,14 the regression model showed that increasing age, race, advancing AJCC stage, receipt of radiation, and having federally-funded health care (Medicaid, Medicare) decreased the likelihood of receiving BR. The disparity in BR utilization between Appalachian and non-Appalachian women is likely multifactorial in nature, and previously documented barriers to BR may play a role. In addition to those factors described above, plastic surgeon density, travel distance, socioeconomic status and general surgeon referral patterns are also predictive of BR.
In a statement from the American College of Surgeons Committee on Health Care Disparities regarding healthcare disparities and surgical outcomes, the College wrote: “there is no quality without access.”15 With regards to BR, access to BR services has been described as a “surrogate” marker for the quality of breast cancer care.16 Unfortunately, the Appalachian region of Kentucky is plagued with a deficit of specialty physicians, including surgeons. The supply of physicians per 100,000 is 59% lower than the national average and 60% lower than the average in non-Appalachian designated areas of Kentucky. To further investigate this, we followed the approach by Tseng et al.9 and examined the number of reconstructive plastic surgeons offering BR services throughout the state of Kentucky and found only one reconstructive plastic surgeon located in the Appalachian region. Conversely, the major metropolitan areas of the state including Louisville, Lexington, and Northern Kentucky (Cincinnati metropolitan area), which are non-Appalachian by definition, have a higher number of reconstructive plastic surgeons (n = 20) offering BR located in those areas.
General surgeon referral patterns to a reconstructive plastic surgeon have been shown to play a role in receiving BR as well. Alderman et al. found that general surgeons are more likely to refer their patients to a reconstructive plastic surgeon if they were affiliated with a high-volume (greater than 50 breast procedures performed per year) breast surgery center (OR 4.1; p < 0.01) or a large cancer institution (OR 2.4; p = 0.01) compared to surgeons that did not refer their patients at the time of surgical decision making.17 At the time of the breast cancer diagnosis, a patient will most likely be seen by a general surgeon or surgical oncologist as part of a multi-disciplinary team. Therefore, it is at the discretion of the general surgeon to describe the treatment and follow-up options for a patient post-mastectomy, including both a discussion of reconstruction options and referral to a reconstructive plastic surgeon. General surgeons in Appalachian areas are not in close proximity and may not be affiliated with high-volume breast surgery centers, which are instead found in more urban areas of the state and located a significant distance from where the initial consultation may occur. Complicating the matter, in many instances a reconstructive plastic surgeon may not be affiliated with a clinical practice or hospital located in the region, making delivery of BR increasingly challenging.
Choosing to undergo BR is first and foremost a choice, but women must be presented the opportunity to make that choice. In a separate study by Alderman et al., the authors found that only 33% of patients had a general surgeon discuss BR with them during the surgical decision-making process for their breast cancer.18 Why is this discussion not occurring? Provider reimbursement influencing general surgeon referral patterns may be one such explanation. For example, if a general surgeon refers a patient to a high-volume center which has access to a reconstructive plastic surgeon, the referring surgeon would likely lose the case, and the mastectomy along with the reconstruction would instead be performed at the high-volume center. Therefore, due to risk of loss of patient continuity and possible economic implications, a general surgeon in Appalachia may be less likely to encourage breast cancer and reconstructive services elsewhere.
Patients that receive BR are also more likely to live in urban areas and in areas with higher median incomes.14 While the present study did not examine socioeconomic factors such as median incomes, it is well-established that Appalachia is one of the most impoverished and lowest median income-accruing regions in the state and country,19 placing them at a disadvantage of receiving BR. Although, this seems counterintuitive since the WHCRA of 1998 mandates coverage for BR across all payer groups including Medicare and Medicaid.
A travel distance of greater than 20 miles has been also been shown to be a negative predictor of receiving BR (p < 0.05).13 While this study did not examine distance, many patients in our sample would be traveling this distance or greater if coming from an Appalachian county to larger urban areas, which have a greater number of reconstructive plastic surgeons. Collectively, these factors may have contributed to the lower rates of BR surgeries being performed following breast cancer resection in Appalachian patients.
One anticipated finding was that the rate of BR increased over time in both Appalachian and non-Appalachian groups. The noticeable increase in Appalachian reconstruction rates may be due in part to comprehensive legislative efforts. The Affordable Care Act of 2010 expanded health insurance coverage by increasing qualifications to Medicaid plans allowing more individuals access to health insurance. As a result, Kentucky’s Medicaid enrollment increased by 110% from 2013 to 2017, making it one of the most successful states in decreasing the number of uninsured individuals overall.20 Medicaid expansion may have resulted in an increased and sustained rate of BR for patients who had previously been unable to access to care.
Limitations
While this study has contributed valuable information concerning the disparity of BR utilization in Appalachia Kentucky, there are several limitations that should be considered when interpreting study results. First, the Appalachian region extends far beyond the geographic borders of Kentucky. Secondly, the retrospective nature of the study design limited the breadth of variables related to BR that could be examined. As such, we were unable to assess the timing of breast reconstruction, immediate versus delayed, or the location where the patient received BR. This study also did not take into account the relative importance Appalachians have towards BR which could affect the rate of BR. Future studies should seek to quantify BR utilization throughout the entire Appalachian region using state cancer registries, including those not represented in SEER. Additionally, prospective studies should examine if these patients undergo delayed BR more frequently as a result of lack of access to reconstruction, which is associated with increased complications relative to immediate reconstruction. Lastly, the feelings and importance that Appalachian women place on BR should be examined, as should the impact of the Affordable Care Act on increasing access to BR.
Conclusion
Despite the benefits of BR, Appalachian women undergo BR at lower rates and are less likely to receive BR than non-Appalachian women. Although the rates of BR increased in both populations over the study period, there remains a disparity in utilization of BR along the Appalachian divide. While this disparity is likely multifactorial in nature, access to and delivery of care remain a challenge for women with breast cancer in this region. Future efforts should seek to improve access to comprehensive breast cancer care for women in Appalachia, which should include increasing access to a reconstructive plastic surgeon.
Acknowledgments:
Data used in this publication were provided by the Kentucky Cancer Registry (KCR), Lexington, KY. The authors would like to thank Jaclyn McDowell, DrPH at KCR as well as Betsy Fink, BS.
Funding Sources: Ryan C. DeCoster, MD is supported by a National Institutes of Health (NIH), National Cancer Institute (CA160003) T32: Oncology Research Training for Surgeon-Scientists training grant. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH. This research was partially supported by the William S. Farish Endowed Chair in Plastic Surgery.
Footnotes
Disclosures: The authors have no associations or financial disclosures to report that create a conflict of interest with the information presented in this article.
Presented in part at the 8th annual Appalachian Translational Region Network Summit in Lexington, KY.
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