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The pervasive crisis of diminishing radiation therapy access for vulnerable populations in the United States—Part 4: Appalachian patients

Open AccessPublished:August 10, 2018DOI:https://doi.org/10.1016/j.adro.2018.08.001

      Abstract

      Purpose

      Compared with the rest of the United States, the population of Appalachia has lower education levels, higher rates of poverty, and limited access to health care. The presence of disparities in radiation therapy (RT) access for Appalachian patients with cancer has rarely been examined.

      Methods and materials

      The National Cancer Institute initiatives toward addressing disparities in treatment access for rural populations were examined. An extensive literature search was undertaken for studies investigating RT access disparities in Appalachian patients, beginning with the most common cancers in these patients (lung, colorectal, and cervical).

      Results

      Although the literature investigating RT access disparities in Appalachia is relatively sparse, studies examining lung, colorectal, cervical, prostate, head and neck, breast, and esophageal cancer, as well as lymphoma, indicate an unfortunate commonality in barriers to optimal RT access for Appalachian patients with cancer. These barriers are predominantly socioeconomic in nature (low income and lack of private insurance) but are exacerbated by paucities in both the number and quality of radiation centers that are accessible to this patient population.

      Conclusions

      Regardless of organ system, there are significant barriers for Appalachian patients with cancer to receive RT. Such diminished access is alarming and warrants resources devoted to addressing these disparities, which often go overlooked because of the assumption that the overall wealth of the United States is tangibly applicable to all of its citizens. Without intelligently targeted investments of time and finances in this arena, there is great risk of exacerbating rather than alleviating the already heavy burden facing Appalachian patients with cancer.

      Introduction

      Optimal treatment of cancer requires access to the most advanced tools of care, among which radiation therapy (RT) is a prominent component.
      • Delaney G.
      • Jacob S.
      • Featherstone C.
      • Barton M.
      The role of radiotherapy in cancer treatment: Estimating optimal utilization from a review of evidence-based clinical guidelines.
      Given the advances in radiation oncology technology and efficacy over the past 3 decades, disparities in RT access arguably result in larger discrepancies in patient care than ever before.
      • McClelland 3rd, S.
      • Deville C.
      • Thomas Jr., C.R.
      • Jaboin J.J.
      An overview of disparities research in access to radiation oncology care.
      The current Advances in Radiation Oncology disparities series has focused on the vulnerable populations within the United States that most likely to suffer disparities in RT access and previously examined African American, Native American, and Hispanic American patients.
      • Miller R.C.
      • Goyal S.
      • McClelland 3rd, S.
      • et al.
      ASTRO’s Advances in Radiation Oncology – Success to date and future plans.
      • McClelland 3rd, S.
      • Page B.R.
      • Jaboin J.J.
      • Chapman C.H.
      • Deville C.
      • Thomas Jr., C.R.
      The pervasive crisis of diminishing radiation therapy access for vulnerable populations in the United States – Part 1: African-American patients.
      • McClelland 3rd, S.
      • Leberknight J.
      • Guadagnolo B.A.
      • Coleman C.N.
      • Petereit D.G.
      The pervasive crisis of diminishing radiation therapy access for vulnerable populations in the United States – Part 2: American Indian patients.
      • McClelland 3rd, S.
      • Perez C.A.
      The pervasive crisis of diminishing radiation therapy access for vulnerable populations in the United States – Part 3: Hispanic-American patients.
      This manuscript concludes the series by investigating the barriers Appalachian patients with cancer face in receiving RT care, a population from which prior research has produced important information for intervention, research, and control of cancer.
      • Friedell G.H.
      • Rubio A.
      • Maretzki A.
      • et al.
      Community cancer control in a rural, underserved population: The Appalachian Leadership Initiative on Cancer Project.
      According to the Appalachian Regional Commission (federally mandated in 1965 to support social and economic development in the Appalachian region), Appalachia comprises 406 counties that span 13 states (Alabama, Georgia, Kentucky, Maryland, Mississippi, New York, North Carolina, Ohio, Pennsylvania, South Carolina, Tennessee, Virginia, and West Virginia) along the Appalachian mountain chain, containing >8% of the U.S. population.
      Centers for Disease Control and Prevention
      Cancer death rates--Appalachia, 1994-1998.
      The Appalachian Regional Commission is composed of the governors of these 13 states as well as a presidential appointee who represents the federal government (most recently Earl Gohl in 2010).
      However, a March 2017 federal budget proposal for the 2018 fiscal year proposed the complete elimination of Appalachian Regional Commission federal funding.
      Centers for Disease Control and Prevention
      Cancer death rates--Appalachia, 1994-1998.
      Appalachian Regional Commission
      Federal Co-Chair Earl F. Gohl.
      Executive Office of the President of the United States
      America first: A budget blueprint to make America great again. Major agency budget highlights.
      Compared with the rest of the United States, Appalachians have lower education levels, higher rates of poverty, and limited access to health care.
      • Friedell G.H.
      • Linville L.H.
      • Hullet S.
      Cancer control in rural Appalachia.
      Consequently, the National Cancer Institute has designated any rural population as a special population due to high death risk from cancer and other diseases.
      • Portnoy B.
      Healthy people in rural America by the year 2000.
      An analysis of mortality by the Centers for Disease Control National Center for Health Statistics using Surveillance, Epidemiology, and End Results (SEER) data from 1994 to 1998 found the cancer death rate for rural Appalachia to be 176.3 per 100,000 people and 173.1 per 100,000 for all Appalachia, compared with the general United States at 166.7 per 100,000 population.
      Centers for Disease Control and Prevention
      Cancer death rates--Appalachia, 1994-1998.
      Death rates for lung (57.2 vs 48.9 per 100,000) and cervical (3.1 vs 2.7 per 100,000) cancer were each significantly higher in rural Appalachia than in the United States overall, with the Appalachian region of Kentucky having the highest death rate for lung cancer (73.7 per 100,000), cervical cancer (3.8 per 100,000), and all cancers (196.6 per 100,000). The colorectal cancer death rate of 6 of 13 Appalachian states was significantly higher than that of the overall U.S. rate of 16.9 per 100,000.
      Centers for Disease Control and Prevention
      Cancer death rates--Appalachia, 1994-1998.
      The Centers for Disease Control attempted to address these findings by promoting screening services through the National Breast and Cervical Cancer Early Detection Program and the National Colorectal Cancer Action Campaign.
      Centers for Disease Control
      Cancer prevention and control.
      The cancer with the largest impact on the all-cancer death rate for Appalachian patients is lung cancer, which has been attributed to a high prevalence of smoking in this population.
      Centers for Disease Control and Prevention
      Cancer death rates--Appalachia, 1994-1998.

       Most common cancer-related death sites in Appalachian patients (lung, colorectal, cervical)

       Lung cancer

      Overall, lung cancer has a higher incidence in Appalachia than non-Appalachia areas of the United States. In a recent review by Wilson et al., the male rate of lung and bronchus cancer incidence is 100.4 cases per 100,000 persons, and the female rate is 61.0 per 100,000. This is relatively higher than the rates in the U.S. non-Appalachia areas, with 79.5 cases per 100,000 for men and 54.7 cases per 100,000 for women.
      • Wilson R.J.
      • Ryerson A.B.
      • Singh S.D.
      • King J.B.
      Cancer incidence in Appalachia, 2004-2011.
      Moreover, for both female and male Appalachian residents, there has been a steady increase of 1.4% for men and 0.6% for women.
      • Wilson R.J.
      • Ryerson A.B.
      • Singh S.D.
      • King J.B.
      Cancer incidence in Appalachia, 2004-2011.
      A higher incidence has been attributed to lifestyle, occupation, low income, and lack of education.
      Centers for Disease Control
      State-specific prevalence and trends in adult cigarette smoking-United States, 1998-2007.
      • Van Ryn M.
      • Burke J.
      The effect of patient race and socio-economic status on physicians' perceptions of patients.
      Rural areas tend to have variations in quality, availability, and access to medical services compared with metro areas.
      • Casey M.M.
      • Call K.T.
      • Klingner J.M.
      Are rural residents less likely to obtain recommended preventive healthcare services?.
      In North Carolina, surveys showed that among respondent rural facilities, only 52% followed lung cancer screening guidelines. Moreover, in the active facilities, overall patient volumes were low.
      • Henderson L.M.
      • Jones L.M.
      • Marsh M.W.
      • Benefield T.
      • Rivera M.P.
      • Molina P.L.
      Lung cancer screening practices in North Carolina CT facilities.
      However, when a free lung screening program was implemented in the southeastern United States, a 2-fold increase in prevalence was found compared with the National Lung Screening Trial.
      • Simmerman E.L.
      • Thomson 3rd, N.B.
      • Dillard T.A.
      • et al.
      Free lung cancer screening trends toward a twofold increase in lung cancer prevalence in the underserved Southeastern United States.
      This indicates that more patients can be diagnosed if guidelines are followed.
      Along with higher incidence and poor access to facilities for preventative services in Appalachia, several demographic factors serve as a barrier to obtaining treatment, specifically RT. Whether radiation is received by patients with non-small cell lung cancer in rural areas based on demographic factors have been reviewed by several studies. In a study performed in Georgia, higher disease stage and number of comorbidities were associated with less radiation receipt, but race was not.
      Interestingly, nonmetropolitan area residents had a higher probability of receiving radiation compared with patients residing in metropolitan areas.
      • Hua X.
      • Ward K.C.
      • Gillespie T.W.
      • Lipscomb J.
      • Goodman M.
      Non-small cell lung cancer treatment receipt and survival among African-Americans and whites in a rural area.
      In this particular study, this counterintuitive finding was explained by the fact that even though travel distances were greater for patients in rural areas, many radiation facilities provided transportation to help minimize the gap in care. In general, 26.3% of patients did not receive any therapy within a year of diagnosis. These patients were more likely to be older and without insurance coverage.
      • Hua X.
      • Ward K.C.
      • Gillespie T.W.
      • Lipscomb J.
      • Goodman M.
      Non-small cell lung cancer treatment receipt and survival among African-Americans and whites in a rural area.
      In rural areas of Alabama, race was not a significant factor for RT receipt, which was the case in urban areas.
      • Steele C.B.
      • Pisu M.
      • Richardson L.C.
      Urban/rural patterns in receipt of treatment for non-small cell lung cancer among black and white Medicare beneficiaries, 2000-2003.
      This may highlight that racial disparities tend to become minimal in the context of Appalachian locations.
      Factors leading to disparities in rural areas (eg, age) have been found to translate to worse outcomes. In rural West Virginia, elderly patients had significantly better survival outcomes with lung cancer if they received the appropriate therapy, which may be surgery plus RT and chemotherapy. Appropriate care was only received by 46% of patients in the cohort and was not affected by timeliness of care. The disparity was attributed to the disproportionate lung cancer burden, facilities in the area that did not completely follow guideline concordant care, and underuse of diagnostic and management services of Medicare.
      • Nadpara P.A.
      • Madhavan S.S.
      • Tworek C.
      Disparities in lung cancer care and outcomes among elderly in a medically underserved state population-A cancer registry-linked database study.
      Another study evaluating disparities in cancer care in West Virginia noted that the supply and proximity of radiation oncologist and facilities may contribute to the significant disparity. Of note, the author urges large university centers in the area to develop radiation oncology residency programs to ensure a better cancer care workforce.
      • Singh R.
      • Goebel M.
      • Lynne J.
      Rural disparities in cancer care: A review of its implications and possible interventions.
      Lung cancer is a prominent burden in the Appalachian population compared with the U.S. non-Appalachian population because of many demographic and lifestyle factors. However, the difficulty of access to radiation facilities with adequate resources to guideline-driven practices provides a significant barrier to obtaining radiation if necessary and can subsequently translate to worse outcomes.

       Colorectal cancer

      The incidence of colon cancer in Appalachia is 56.6 per 100,000 persons for men and 41.8 per 100,000 for women. These statistics are higher than those of non-Appalachian men and women in the United States.
      • Wilson R.J.
      • Ryerson A.B.
      • Singh S.D.
      • King J.B.
      Cancer incidence in Appalachia, 2004-2011.
      When comparing rural and non-rural Appalachia using SEER data, Appalachia incidence was found to be greater than what was shown in the SEER data.
      • Lengerich E.J.
      • Tucker T.C.
      • Powell R.K.
      • et al.
      Cancer incidence in Kentucky, Pennsylvania, and West Virginia: disparities in Appalachia.
      Moreover, the incidence of unstaged colon and rectal cancer in rural Appalachia was substantially elevated, which translated to access to and use of diagnostic and treatment services.
      • Lengerich E.J.
      • Tucker T.C.
      • Powell R.K.
      • et al.
      Cancer incidence in Kentucky, Pennsylvania, and West Virginia: disparities in Appalachia.
      In Kentucky, patients from Appalachian counties were half as likely to have a colonoscopy or sigmoidoscopy performed within the past 10 years compared with non-Appalachian patients.
      • Fleming S.T.
      • Love M.M.
      • Bennett K.
      Diabetes and cancer screening rates among Appalachian and non-Appalachian residents of Kentucky.
      Recent data also suggest decreased odds of receiving RT for rural Georgia residents.
      • Hines R.B.
      • Markossian T.W.
      Differences in late-stage diagnosis, treatment, and colorectal cancer-related death between rural and urban African Americans and whites in Georgia.
      Treatment access and use has great implication in terms of outcomes. The presence of a radiation facility in a county in Appalachia results in a 12% to 47% decline in mortality.
      • Aneja S.
      • Yu J.
      Radiation oncologist density and colorectal cancer mortality.
      Beyond a higher incidence and barriers to access of care, up-to-date medical facilities are scarce as well. Hatzell et al performed a study evaluating the impact of educational activities updating on newer methodologies in colon and rectal treatments. Pre-and-post surveys showed that 70% of participants failed to acknowledge chemotherapy as experimental for patients with Dukes’ B colon cancer, and 25% failed to recognize a combination of surgery, chemotherapy, and RT as a standard treatment for rectal cancer. The authors concluded that a stronger consensus for appropriate cancer treatment is necessary.
      • Hatzell T.A.
      • Ricketts T.C.
      • Tropman S.E.
      • Paskett E.D.
      • Cooper M.R.
      Rural physicians' understanding of the state-of-the-art in breast, colon and rectum cancer treatment.
      The disparity in colon and rectal cancer in Appalachia is a domino effect that starts with inadequate screening and leads to the scarcity of radiation facilities in the vicinity. Additionally, rural facilities may not be up to date on recent guidelines, and patients may not be receiving standard of care in terms of RT. However, other factors such as race and socioeconomic factors have not been completely elucidated. Further research on the specific barriers to receipt of adequate radiation in colorectal cancer should be further explored and described.

       Cervical cancer

      The epidemiology, risk factors, and clinical outcome of patients with cervical cancer are closely related to race, smoking, and poor socioeconomic status. In a study of 153 women by the University of Maryland,
      • Brooks S.E.
      • Baquet C.R.
      • Gardner J.F.
      • Moses G.
      • Ghosh A.
      Cervical cancer--the impact of clinical presentation, health and race on survival.
      African-American women were more likely to have stages III and IV cervical cancer and had poorer survival across all stages of disease compared with white women. Another study
      • Brooks S.E.
      • Chen T.T.
      • Ghosh A.
      • Mullins C.D.
      • Gardner J.F.
      • Baquet C.R.
      Cervical cancer outcomes analysis: Impact of age, race, and comorbid illness on hospitalizations for invasive carcinoma of the cervix.
      by the same institution noted that being African American and/or having Medicaid or uninsured status were associated with more emergency visits and admissions for cervical cancer and treatment-related complications in the Appalachian regions. In a large study of >2000 patients, alarmingly increased rates of African-American women were found to have locally advanced or stage IV cervical cancer at diagnosis, even after adjusting for insurance status, compared with their white counterparts.
      • Fleming S.
      • Schluterman N.H.
      • Tracy J.K.
      • Temkin S.M.
      Black and white women in Maryland receive different treatment for cervical cancer.
      However, there is certainly good news as well: At a large and experienced tertiary hospital in Kentucky with patients with cervical cancer, no differences were observed by race, insurance coverage, or socioeconomic status in patient outcomes including survival over a 10-year period.
      • Seamon L.G.
      • Tarrant R.L.
      • Fleming S.T.
      • et al.
      Cervical cancer survival for patients referred to a tertiary care center in Kentucky.
      Furthermore, the increased case volumes of the medical facility were proportionally related to improved cervical cancer outcomes in a study using the Virginia state cancer registry.
      • Showalter T.N.
      • Camacho F.
      • Cantrell L.A.
      • Anderson R.T.
      Determinants of quality care and mortality for patients with locally advanced cervical cancer in Virginia.

       Additional cancer sites in Appalachian patients

       Prostate cancer

      Data on the use of RT for the Appalachian region is limited; however, current studies suggest that RT disparities may indeed exist. The Virginia Prostate Cancer registry was published, analyzing 28,244 men with stage 0 to IV prostate cancer between 1970 and 1997.
      Prostate Cancer in Virginia
      Virginia Cancer Registry (1970-1997).
      Only 3.3% had stage 0 disease and 13.2% had stage IV at diagnosis. The registry showed that the first course of treatment for the entire cohort consisted of surgery alone for 9632 patients (34.1%) and radiation alone for 5556 patients (19.7%). Combined surgery and radiation were given to 898 patients (3.2%), surgery and hormone therapy to 1398 patients (4.9%), and RT and hormone therapy to 1246 patients (4.4%). The article compared the results to those of a prior National Cancer Database on prostate cancer statistics, which showed a similar national trend with surgery alone in 41.0% and radiation only in 22.0% of patients for first-line treatment.
      American College of Surgeons
      National cancer data base prostate cancer statistics.
      The American Cancer Society along with Massachusetts General Hospital published a National Cancer Database report that focused on the declining use of postoperative RT after radical prostatectomy for prostate cancer with adverse features between 2005 and 2011.
      • Sineshaw H.M.
      • Gray P.J.
      • Efstathiou J.A.
      • Jemal A.
      Declining use of radiotherapy for adverse features after radical prostatectomy: Results from the national cancer data base.
      The adverse features were either pathologic T3/4 or positive margins. Overall, the use of postoperative radiation in this high-risk population decreased by approximately 2% (9.1% to 7.3%) across the United States. Geographically, the article showed that the majority of patients received surgery alone versus the addition of radiation with or without hormones in the Midwest (89% vs 8.9%) and South (91% vs. 7.3%). These regions encapsulate the Appalachian population. Also, the odds ratio showed that patients in the South were less likely to receive postoperative radiation compared with those in the Northeast.
      Although there is sparse data on the use of RT for prostate cancer in the Appalachian region, we can use the available literature to state that disparity in radiation management is likely.

       Head and neck cancer

      Reports on the disparities of RT for head and neck cancer (HNC) are sparse, and we were unable to find reports targeting this specific subset. However, data are available that tangentially reflect radiation delivery in this population. A SEER analysis of patients with HNC who were treated between 2007 and 2010 was reported in 2016.
      • Inverso G.
      • Mahal B.A.
      • Aizer A.A.
      • Donoff R.B.
      • Chuang S.K.
      Health insurance affects head and neck cancer treatment patterns and outcomes.
      The retrospective analysis showed that Medicaid patients were less likely to be treated with definitive radiation and/or surgery. Also, patients with Medicare coverage or no insurance were less likely to have definitive treatment and present with metastatic disease. Patients in disadvantaged areas such as the Appalachian region are more likely to be uninsured or have government-sponsored insurance as opposed to private insurance. Thus, they may also have a higher risk of not receiving definitive RT.
      Harvard also conducted a SEER analysis on the use of intensity modulated RT (IMRT) and conformal RT for HNC.
      • Sher D.J.
      • Neville B.A.
      • Chen A.B.
      • Schrag D.
      Predictors of IMRT and conformal radiotherapy use in head and neck squamous cell carcinoma: A SEER Medicare analysis.
      The authors showed that having a higher median income predicted for a higher use of IMRT. The interaction seemed to have a linear relationship because the second lowest income quartile had a higher use of IMRT than the lowest income quartile. Because IMRT has been shown to decrease morbidity,
      • Nutting C.M.
      • Morden J.P.
      • Harrington K.J.
      • et al.
      Parotid-sparing intensity modulated versus conventional radiotherapy in head and neck cancer (PARSPORT): A phase 3 multicentre randomised controlled trial.
      an increase in toxicity from treatment may dissuade this patient population from receiving or completing RT. Because patients in the Appalachian region are usually low income, this study may pertain to care in their community.
      Although there is sparse data regarding use of RT in this population, income and insurance seem to be associated with receipt and type of care. This shows the need for more reports targeting this patient population.

       Esophageal cancer

      Although the disparities in incidence rates for esophageal cancer, lymphoma/leukemia, and other miscellaneous cancers are not as large, they still exist. For esophageal cancer, the incidence in Appalachian men is 9.0 cases per 100,000 compared with 8.5 cases per 100,000 for non-Appalachian men (P < .05).
      • Wilson R.J.
      • Ryerson A.B.
      • Singh S.D.
      • King J.B.
      Cancer incidence in Appalachia, 2004-2011.
      When specifically looking at adenocarcinomas of the esophagus, this difference becomes much more pronounced. According to a study by Hebert et al. on esophageal cancer disparities in South Carolina, a steady increase in the incidence of esophageal adenocarcinomas was observed since the late 1980s, with rates rising at approximately 3% to 4% per year.
      • Hebert J.R.
      • Adams S.A.
      • Daguise V.G.
      • et al.
      Esophageal cancer disparities in South Carolina: early detection, special programs, and descriptive epidemiology.
      Furthermore, this increase is predominantly seen in the European-American population.
      • Hebert J.R.
      • Adams S.A.
      • Daguise V.G.
      • et al.
      Esophageal cancer disparities in South Carolina: early detection, special programs, and descriptive epidemiology.
      Another study, from 2005, estimated the increase in incidence of esophageal adenocarcinoma to be in the range of 300% to 500% over the last 40 years (contemporary to the time of the study) and again predominantly in European-Americans.
      • Shaheen N.J.
      Advances in Barrett's esophagus and esophageal adenocarcinoma.
      One hypothesis suggests that the geographic pattern of incidence of esophageal adenocarcinoma overlaps that of obesity fairly substantially, which could in part explain the increased rates of esophageal adenocarcinoma in these areas.
      • Shaheen N.J.
      Advances in Barrett's esophagus and esophageal adenocarcinoma.
      Although this disparity exists and some research has been done into why it exists, there is very little research on the impact of any disparities in the receipt of treatment on overall survival.

       Hematologic malignancies

      Although RT has a more limited role in leukemia, there are disparities with regard to leukemia incidence and survival between Appalachian and non-Appalachian patients that need to be addressed. Appalachian men have a leukemia incidence of 16.9 cases per 100,000 compared with 16.7 cases per 100,000 for non-Appalachian men. Appalachian women have a leukemia incidence of 10.4 cases per 100,00 in comparison with 10.2 cases per 100,000 for non-Appalachian women.
      • Wilson R.J.
      • Ryerson A.B.
      • Singh S.D.
      • King J.B.
      Cancer incidence in Appalachia, 2004-2011.
      In a paper analyzing the geographical variation in survival outcomes for adult patients with acute myeloid leukemia within the state of North Carolina, Medicaid patients had an increased likelihood of death when compared with patients covered by private insurance (hazard ratio, 1.36; confidence interval, 1.00-1.85; P < .05).
      • Freeman A.T.
      • Meyer A.
      • Smitherman A.B.
      • et al.
      Statewide geographic variation in outcomes for adults with acute myeloid leukemia in North Carolina.
      Also, as an independent association, patients who did not undergo allogenic hematopoietic stem cell transplantation (standard of care for definitive treatment) within 1 year of diagnosis had a hazard ratio of 2.09 compared with those who were able to receive allogenic hematopoietic stem cell transplantation (confidence interval, 1.15-3.83; P < .05).
      • Freeman A.T.
      • Meyer A.
      • Smitherman A.B.
      • et al.
      Statewide geographic variation in outcomes for adults with acute myeloid leukemia in North Carolina.
      Although these data are for hematopoietic stem cell transplantation, access to RT may have a role to play in this disparity because total body irradiation is a prerequisite for stem cell transplantation.
      Although data are sparse, there is some context for increasing research of radiation-related cancer disparities for esophageal cancer, lymphoma, leukemis, and other miscellaneous cancers.

       Breast cancer

      Multiple studies have suggested that women in Appalachia are at a higher risk for inadequate health access and appropriate clinical screening for breast cancer.
      • Anderson R.T.
      • Kimmick G.G.
      • Camacho F.
      • et al.
      Health system correlates of receipt of radiation therapy after breast-conserving surgery: A study of low-income Medicaid-enrolled women.
      • Anderson R.T.
      • Yang T.C.
      • Matthews S.A.
      • et al.
      Breast cancer screening, area deprivation, and later-stage breast cancer in Appalachia: Does geography matter?.
      • Bickell N.A.
      • LePar F.
      • Wang J.J.
      • Leventhal H.
      Lost opportunities: Physicians' reasons and disparities in breast cancer treatment.
      • Christiansen N.
      • Chen L.
      • Gilmore J.
      • Pechar D.
      • Szabo S.
      Association between African American race and outcomes in patients with nonmetastatic triple-negative breast cancer: A retrospective analysis by using results from the Georgia Cancer Specialist Database.
      • Dragun A.E.
      • Huang B.
      • Gupta S.
      • Crew J.B.
      • Tucker T.C.
      One decade later: Trends and disparities in the application of post-mastectomy radiotherapy since the release of the American Society of Clinical Oncology clinical practice guidelines.
      • Elward K.S.
      • Penberthy L.T.
      • Bear H.
      • Swartz D.M.
      • Boudreau R.M.
      • Cook S.S.
      Variation in the use of breast-conserving therapy for Medicare beneficiaries in Virginia: Clinical, geographic, and hospital characteristics.
      Using central cancer registry data, Anderson et al.
      • Anderson R.T.
      • Yang T.C.
      • Matthews S.A.
      • et al.
      Breast cancer screening, area deprivation, and later-stage breast cancer in Appalachia: Does geography matter?.
      showed that less-populated counties in 3 Appalachian states were statistically significantly underscreened, especially for the early detection of locally advanced breast cancer. Another study of 344 women in North Carolina
      • Anderson R.T.
      • Kimmick G.G.
      • Camacho F.
      • et al.
      Health system correlates of receipt of radiation therapy after breast-conserving surgery: A study of low-income Medicaid-enrolled women.
      reported that up to one third of patients did not receive RT after breast-conserving surgery (BCS), and risk factors included living in less populated counties, having BCS at smaller hospitals, and residing in counties that were specialist scarce. Similar findings were reported in South Carolina.
      • Samson M.E.
      • Porter N.G.
      • Hurley D.M.
      • Adams Sa
      • Eberth J.M.
      Disparities in breast cancer incidence, mortality, and quality of care among African American and European American women in South Carolina.
      Having on-site RT availability increased breast-conserving therapy rates at a community hospital.
      • Hahn C.A.
      • Marks L.B.
      • Chen D.Y.
      • Lind P.A.
      • Lind H.M.
      • Prosnitz L.R.
      Breast conservation rates-barriers between tertiary care and community practice.
      Surgeons were also less likely to refer patients for adjuvant therapies if the patient had Medicaid coverage or was not insured.
      • Bickell N.A.
      • LePar F.
      • Wang J.J.
      • Leventhal H.
      Lost opportunities: Physicians' reasons and disparities in breast cancer treatment.
      Additionally, working women, especially those receiving aggressive treatments, experienced significant employment disruptions.
      • Jagsi R.
      • Abrahamse P.H.
      • Lee K.L.
      • et al.
      Treatment decisions and employment of breast cancer patients: Results of a population-based survey.
      Two studies using the Kentucky Cancer Registry reported that postmastectomy
      • Dragun A.E.
      • Huang B.
      • Gupta S.
      • Crew J.B.
      • Tucker T.C.
      One decade later: Trends and disparities in the application of post-mastectomy radiotherapy since the release of the American Society of Clinical Oncology clinical practice guidelines.
      and whole-breast
      • Dragun A.E.
      • Huang B.
      • Tucker T.C.
      • Spanos W.J.
      Disparities in the application of adjuvant radiotherapy after breast-conserving surgery for early stage breast cancer: Impact on overall survival.
      RT were still vastly underused, especially for older and poorer patients in rural regions. Overall, only 66% of women received breast-conserving therapy between 1998 and 2007.
      • Dragun A.E.
      • Huang B.
      • Tucker T.C.
      • Spanos W.J.
      Disparities in the application of adjuvant radiotherapy after breast-conserving surgery for early stage breast cancer: Impact on overall survival.
      Older age, race, poor socioeconomic status, and lack of access or further distance to a RT center were also noted as factors for more women choosing mastectomy or forgoing RT altogether after BCS in Appalachian states.
      • Elward K.S.
      • Penberthy L.T.
      • Bear H.
      • Swartz D.M.
      • Boudreau R.M.
      • Cook S.S.
      Variation in the use of breast-conserving therapy for Medicare beneficiaries in Virginia: Clinical, geographic, and hospital characteristics.
      • Guy Jr., G.P.
      • Lipscomb J.
      • Gillespie T.W.
      • Goodman M.
      • Richardson L.C.
      • Ward K.C.
      Variations in guideline-concordant breast cancer adjuvant therapy in rural Georgia.
      • Sio T.T.
      • Chang K.
      • Jayakrishnan R.
      • et al.
      Patient age is related to decision-making, treatment selection, and perceived quality of life in breast cancer survivors.
      • Royak-Schaler R.
      • Pelser C.
      • Langenberg P.
      • et al.
      Characteristics associated with the initiation of radiation therapy after breast-conserving surgery among African American and white women diagnosed with early-stage breast cancer in Maryland, 2000-2006.
      • White A.
      • Richardson L.C.
      • Krontiras H.
      • Pisu M.
      Socioeconomic disparities in breast cancer treatment among older women.
      In rural Virginia, increased distance to an RT center was the only independently predicted factor for increased mastectomy rates in 20,094 patients.
      • Schroen A.T.
      • Brenin D.R.
      • Kelly M.D.
      • Knaus W.A.
      • Slingluff Jr., C.L.
      Impact of patient distance to radiation therapy on mastectomy use in early-stage breast cancer patients.
      Similar findings were noted in North Carolina
      • Wheeler S.B.
      • Kuo T.M.
      • Durham D.
      • Frizzelle B.
      • Reeder-Hayes K.
      • Meyer A.M.
      Effects of distance to care and rural or urban residence on receipt of radiation therapy among North Carolina Medicare enrollees with breast cancer.
      and Kentucky
      • Yao N.
      • Matthews S.A.
      • Hillemeier M.M.
      • Anderson R.T.
      Radiation therapy resources and guideline-concordant radiotherapy for early-stage breast cancer patients in an underserved region.
      (mountainous states).
      There are multiple opportunities and needs for intervention. A study that surveyed rural physicians in North and South Carolina found that 55% failed to acknowledge that adjuvant RT was required after lumpectomy for breast cancer treatment.
      • Hatzell T.A.
      • Ricketts T.C.
      • Tropman S.E.
      • Paskett E.D.
      • Cooper M.R.
      Rural physicians' understanding of the state-of-the-art in breast, colon and rectum cancer treatment.
      Another report also highlighted the need for standardized pathologic information on surgical specimen reports (eg, margin status, tumor size, histologic grade, and angiolymphatic invasion) in both urban and rural hospitals.
      • Imperato P.J.
      • Waisman J.
      • Wallen M.D.
      • Llewellyn C.C.
      • Pryor V.
      Improvements in breast cancer pathology practices among medicare patients undergoing unilateral extended simple mastectomy.
      In a large study of >4500 patients with breast cancer in Appalachian regions,
      • Louis C.J.
      • Clark J.R.
      • Hillemeier M.M.
      • Camacho F.
      • Yao N.
      • Anderson R.T.
      The effects of hospital characteristics on delays in breast cancer diagnosis in Appalachian communities: A population-based study.
      the authors pointed out that nonprofit hospitals in rural and underserved areas may experience delays in diagnosing new breast cancer cases. For many regions in Appalachia, the main efforts remain reaching out to rural and very rural populations and systemically improving the entire care network at individual components (screening, diagnosis, surgery, and adjuvant therapies) with local health care providers.
      • Markossian T.W.
      • Hines R.B.
      Disparities in late stage diagnosis, treatment, and breast cancer-related death by race, age, and rural residence among women in Georgia.
      • Markossian T.W.
      • Hines R.B.
      • Bayakly R.
      Geographic and racial disparities in breast cancer-related outcomes in Georgia.

      Discussion

      An unfortunate commonality of these disease sites in Appalachian patients is the disparate access to optimal RT as a result of a number of socioeconomic factors, including but not limited to low income, lack of private insurance, limited access to diagnostic and treatment services (ie, colonoscopy for colorectal cancer screening), paucities in both number and quality of radiation centers, decreased access to up-to-date treatment recommendations, and the geographic region of the United States. In fact, the median household income in Appalachia is 82% of the U.S. median income, with only 19 Appalachian counties having household incomes at or above the national mean.
      • Pollard K.
      • Jacobsen L.A.
      The Appalachian Region: A data overview from the 2006-2010 American community survey chartbook.
      This patient population suffers from these socioeconomic barriers and from the barrier of relative invisibility. The disparities they face in receiving optimal care are not as widely publicized as those of racial and ethnic minorities, such as African Americans or Hispanic Americans. Furthermore, an unfortunate reality is that many people both within and outside the United States rely on the flawed assumption that the overall wealth of the United States is tangibly applicable to all of its citizens, which may diminish their understanding of the great lack of resources Appalachian patients with cancer face.
      We hope that this manuscript will help to shed light on the difficulties Appalachian patients with cancer face, with the goal of inspiring financial and policy-driven interventions to tackle these difficulties, many of which may be less formidable than they appear at first glance. Based on the results elucidated in this manuscript for multiple cancer sites, it may be wiser for the federal government to increase aid to Appalachian patients with cancer rather than (as the 2018 fiscal year budget proposed) completely eliminating financial aid to this vulnerable population.
      Centers for Disease Control and Prevention
      Cancer death rates--Appalachia, 1994-1998.
      Appalachian Regional Commission
      Federal Co-Chair Earl F. Gohl.
      Executive Office of the President of the United States
      America first: A budget blueprint to make America great again. Major agency budget highlights.
      Furthermore, newer tools developed to identify patients at increased risk of toxicity after RT will need to be governed with the priority of optimizing access to care rather than optimizing profit.
      • Palmer J.D.
      • Patel T.T.
      • Eldredge-Hindy H.
      • et al.
      Patients undergoing radiation therapy are at risk of financial toxicity: a patient-based prospective survey study.
      • McClelland 3rd, S.
      • Jaboin J.J.
      Will financial toxicity screening help or harm minority patient access to radiation therapy?.
      Otherwise, there is great risk of exacerbating rather than alleviating the already heavy burden facing Appalachian patients with cancer.

      References

        • Delaney G.
        • Jacob S.
        • Featherstone C.
        • Barton M.
        The role of radiotherapy in cancer treatment: Estimating optimal utilization from a review of evidence-based clinical guidelines.
        Cancer. 2005; 104: 1129-1137
        • McClelland 3rd, S.
        • Deville C.
        • Thomas Jr., C.R.
        • Jaboin J.J.
        An overview of disparities research in access to radiation oncology care.
        J Radiat Oncol. 2016; 5: 437-444
        • Miller R.C.
        • Goyal S.
        • McClelland 3rd, S.
        • et al.
        ASTRO’s Advances in Radiation Oncology – Success to date and future plans.
        Adv Radiat Oncol. 2017; 2: 245-248
        • McClelland 3rd, S.
        • Page B.R.
        • Jaboin J.J.
        • Chapman C.H.
        • Deville C.
        • Thomas Jr., C.R.
        The pervasive crisis of diminishing radiation therapy access for vulnerable populations in the United States – Part 1: African-American patients.
        Adv Radiat Oncol. 2017; 2: 523-531
        • McClelland 3rd, S.
        • Leberknight J.
        • Guadagnolo B.A.
        • Coleman C.N.
        • Petereit D.G.
        The pervasive crisis of diminishing radiation therapy access for vulnerable populations in the United States – Part 2: American Indian patients.
        Adv Radiat Oncol. 2018; 3: 3-7
        • McClelland 3rd, S.
        • Perez C.A.
        The pervasive crisis of diminishing radiation therapy access for vulnerable populations in the United States – Part 3: Hispanic-American patients.
        Adv Radiat Oncol. 2018; 3: 93-99
        • Friedell G.H.
        • Rubio A.
        • Maretzki A.
        • et al.
        Community cancer control in a rural, underserved population: The Appalachian Leadership Initiative on Cancer Project.
        J Health Care Poor Underserved. 2001; 12: 5-19
        • Centers for Disease Control and Prevention
        Cancer death rates--Appalachia, 1994-1998.
        MMWR Morb Mortal Wkly Rep. 2002; 51: 527-529
        • Appalachian Regional Commission
        Federal Co-Chair Earl F. Gohl.
        (Available at:) (Accessed May 18, 2017)
        • Executive Office of the President of the United States
        America first: A budget blueprint to make America great again. Major agency budget highlights.
        (Available at:) (Accessed May 18, 2017)
        • Friedell G.H.
        • Linville L.H.
        • Hullet S.
        Cancer control in rural Appalachia.
        Cancer. 1998; 83: 1868-1871
        • Portnoy B.
        Healthy people in rural America by the year 2000.
        in: Couto R.A. Simpson N.K. Harris G. Sowing Seeds in the Mountains: Community-based Coalitions for Cancer Prevention and Control. Appalachia Leadership Initiative on Cancer, National Cancer Institute, Bethesda, MD1994: 102-119
        • Centers for Disease Control
        Cancer prevention and control.
        (Available at:) (Accessed May 18, 2017)
        • Wilson R.J.
        • Ryerson A.B.
        • Singh S.D.
        • King J.B.
        Cancer incidence in Appalachia, 2004-2011.
        Cancer Epidemiol Biomarkers Prev. 2016; 25: 250-258
        • Centers for Disease Control
        State-specific prevalence and trends in adult cigarette smoking-United States, 1998-2007.
        MMWR Morb Mortal Wkly Rep. 2009; 58: 221-226
        • Van Ryn M.
        • Burke J.
        The effect of patient race and socio-economic status on physicians' perceptions of patients.
        Soc Sci Med. 2000; 50: 813-828
        • Casey M.M.
        • Call K.T.
        • Klingner J.M.
        Are rural residents less likely to obtain recommended preventive healthcare services?.
        Am J Prev Med. 2001; 21: 182-188
        • Henderson L.M.
        • Jones L.M.
        • Marsh M.W.
        • Benefield T.
        • Rivera M.P.
        • Molina P.L.
        Lung cancer screening practices in North Carolina CT facilities.
        J Am Coll Radiol. 2017; 14: 166-170
        • Simmerman E.L.
        • Thomson 3rd, N.B.
        • Dillard T.A.
        • et al.
        Free lung cancer screening trends toward a twofold increase in lung cancer prevalence in the underserved Southeastern United States.
        South Med J. 2017; 110: 188-194
        • Hua X.
        • Ward K.C.
        • Gillespie T.W.
        • Lipscomb J.
        • Goodman M.
        Non-small cell lung cancer treatment receipt and survival among African-Americans and whites in a rural area.
        J Community Health. 2014; 39: 696-705
        • Steele C.B.
        • Pisu M.
        • Richardson L.C.
        Urban/rural patterns in receipt of treatment for non-small cell lung cancer among black and white Medicare beneficiaries, 2000-2003.
        J Natl Med Assoc. 2011; 103: 711-718
        • Nadpara P.A.
        • Madhavan S.S.
        • Tworek C.
        Disparities in lung cancer care and outcomes among elderly in a medically underserved state population-A cancer registry-linked database study.
        Popul Health Manag. 2016; 19: 109-119
        • Singh R.
        • Goebel M.
        • Lynne J.
        Rural disparities in cancer care: A review of its implications and possible interventions.
        W V Med J. 2016; 112: 76-82
        • Lengerich E.J.
        • Tucker T.C.
        • Powell R.K.
        • et al.
        Cancer incidence in Kentucky, Pennsylvania, and West Virginia: disparities in Appalachia.
        J Rural Health. 2005; 21: 39-47
        • Fleming S.T.
        • Love M.M.
        • Bennett K.
        Diabetes and cancer screening rates among Appalachian and non-Appalachian residents of Kentucky.
        J Am Board Fam Med. 2011; 24: 682-692
        • Hines R.B.
        • Markossian T.W.
        Differences in late-stage diagnosis, treatment, and colorectal cancer-related death between rural and urban African Americans and whites in Georgia.
        J Rural Health. 2012; 28: 296-305
        • Aneja S.
        • Yu J.
        Radiation oncologist density and colorectal cancer mortality.
        J Clin Oncol. 2011; 29: 605
        • Hatzell T.A.
        • Ricketts T.C.
        • Tropman S.E.
        • Paskett E.D.
        • Cooper M.R.
        Rural physicians' understanding of the state-of-the-art in breast, colon and rectum cancer treatment.
        Cancer Causes Control. 1999; 10: 261-267
        • Brooks S.E.
        • Baquet C.R.
        • Gardner J.F.
        • Moses G.
        • Ghosh A.
        Cervical cancer--the impact of clinical presentation, health and race on survival.
        J Assoc Acad Minor Phys. 2000; 11: 55-59
        • Brooks S.E.
        • Chen T.T.
        • Ghosh A.
        • Mullins C.D.
        • Gardner J.F.
        • Baquet C.R.
        Cervical cancer outcomes analysis: Impact of age, race, and comorbid illness on hospitalizations for invasive carcinoma of the cervix.
        Gynecol Oncol. 2000; 79: 107-115
        • Fleming S.
        • Schluterman N.H.
        • Tracy J.K.
        • Temkin S.M.
        Black and white women in Maryland receive different treatment for cervical cancer.
        PLoS One. 2014; 9: e104344
        • Seamon L.G.
        • Tarrant R.L.
        • Fleming S.T.
        • et al.
        Cervical cancer survival for patients referred to a tertiary care center in Kentucky.
        Gynecol Oncol. 2011; 123: 565-570
        • Showalter T.N.
        • Camacho F.
        • Cantrell L.A.
        • Anderson R.T.
        Determinants of quality care and mortality for patients with locally advanced cervical cancer in Virginia.
        Medicine (Baltimore). 2016; 95: e2913
        • Prostate Cancer in Virginia
        Virginia Cancer Registry (1970-1997).
        2000
        • American College of Surgeons
        National cancer data base prostate cancer statistics.
        (Available at:) (Accessed October 30, 2017)
        • Sineshaw H.M.
        • Gray P.J.
        • Efstathiou J.A.
        • Jemal A.
        Declining use of radiotherapy for adverse features after radical prostatectomy: Results from the national cancer data base.
        Eur Urol. 2015; 68: 768-774
        • Inverso G.
        • Mahal B.A.
        • Aizer A.A.
        • Donoff R.B.
        • Chuang S.K.
        Health insurance affects head and neck cancer treatment patterns and outcomes.
        J Oral Maxillofac Surg. 2016; 74: 1241-1247
        • Sher D.J.
        • Neville B.A.
        • Chen A.B.
        • Schrag D.
        Predictors of IMRT and conformal radiotherapy use in head and neck squamous cell carcinoma: A SEER Medicare analysis.
        Int J Radiat Oncol Biol Phys. 2011; 81: e197-e206
        • Nutting C.M.
        • Morden J.P.
        • Harrington K.J.
        • et al.
        Parotid-sparing intensity modulated versus conventional radiotherapy in head and neck cancer (PARSPORT): A phase 3 multicentre randomised controlled trial.
        Lancet Oncol. 2011; 12: 127-136
        • Hebert J.R.
        • Adams S.A.
        • Daguise V.G.
        • et al.
        Esophageal cancer disparities in South Carolina: early detection, special programs, and descriptive epidemiology.
        J S C Med Assoc. 2006; 102: 201-209
        • Shaheen N.J.
        Advances in Barrett's esophagus and esophageal adenocarcinoma.
        Gastroenterology. 2006; 128: 1554-1566
        • Freeman A.T.
        • Meyer A.
        • Smitherman A.B.
        • et al.
        Statewide geographic variation in outcomes for adults with acute myeloid leukemia in North Carolina.
        Cancer. 2016; 122: 3041-3050
        • Anderson R.T.
        • Kimmick G.G.
        • 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
        • Anderson R.T.
        • Yang T.C.
        • Matthews S.A.
        • et al.
        Breast cancer screening, area deprivation, and later-stage breast cancer in Appalachia: Does geography matter?.
        Health Serv Res. 2014; 49: 546-567
        • Bickell N.A.
        • LePar F.
        • Wang J.J.
        • Leventhal H.
        Lost opportunities: Physicians' reasons and disparities in breast cancer treatment.
        J Clin Oncol. 2007; 25: 2516-2521
        • Christiansen N.
        • Chen L.
        • Gilmore J.
        • Pechar D.
        • Szabo S.
        Association between African American race and outcomes in patients with nonmetastatic triple-negative breast cancer: A retrospective analysis by using results from the Georgia Cancer Specialist Database.
        Clin Breast Cancer. 2012; 12: 270-275
        • Dragun A.E.
        • Huang B.
        • Gupta S.
        • Crew J.B.
        • Tucker T.C.
        One decade later: Trends and disparities in the application of post-mastectomy radiotherapy since the release of the American Society of Clinical Oncology clinical practice guidelines.
        Int J Radiat Oncol Biol Phys. 2012; 83: e591-e596
        • Elward K.S.
        • Penberthy L.T.
        • Bear H.
        • Swartz D.M.
        • Boudreau R.M.
        • Cook S.S.
        Variation in the use of breast-conserving therapy for Medicare beneficiaries in Virginia: Clinical, geographic, and hospital characteristics.
        Clin Perform Qual Health Care. 1998; 6: 63-69
        • Samson M.E.
        • Porter N.G.
        • Hurley D.M.
        • Adams Sa
        • Eberth J.M.
        Disparities in breast cancer incidence, mortality, and quality of care among African American and European American women in South Carolina.
        South Med J. 2016; 109: 24-30
        • Hahn C.A.
        • Marks L.B.
        • Chen D.Y.
        • Lind P.A.
        • Lind H.M.
        • Prosnitz L.R.
        Breast conservation rates-barriers between tertiary care and community practice.
        Int J Radiat Oncol Biol Phys. 2003; 55: 1196-1199
        • Jagsi R.
        • Abrahamse P.H.
        • Lee K.L.
        • et al.
        Treatment decisions and employment of breast cancer patients: Results of a population-based survey.
        Cancer. 2017; 123: 4791-4799
        • Dragun A.E.
        • Huang B.
        • Tucker T.C.
        • Spanos W.J.
        Disparities in the application of adjuvant radiotherapy after breast-conserving surgery for early stage breast cancer: Impact on overall survival.
        Cancer. 2011; 117: 2590-2598
        • Guy Jr., G.P.
        • Lipscomb J.
        • Gillespie T.W.
        • Goodman M.
        • Richardson L.C.
        • Ward K.C.
        Variations in guideline-concordant breast cancer adjuvant therapy in rural Georgia.
        Health Serv Res. 2015; 50: 1088-1108
        • Sio T.T.
        • Chang K.
        • Jayakrishnan R.
        • et al.
        Patient age is related to decision-making, treatment selection, and perceived quality of life in breast cancer survivors.
        World J Surg Oncol. 2014; 12: 230
        • Royak-Schaler R.
        • Pelser C.
        • Langenberg P.
        • et al.
        Characteristics associated with the initiation of radiation therapy after breast-conserving surgery among African American and white women diagnosed with early-stage breast cancer in Maryland, 2000-2006.
        Ann Epidemiol. 2012; 22: 28-36
        • White A.
        • Richardson L.C.
        • Krontiras H.
        • Pisu M.
        Socioeconomic disparities in breast cancer treatment among older women.
        J Womens Health (Larchmt). 2014; 23: 335-341
        • Schroen A.T.
        • Brenin D.R.
        • Kelly M.D.
        • Knaus W.A.
        • Slingluff Jr., C.L.
        Impact of patient distance to radiation therapy on mastectomy use in early-stage breast cancer patients.
        J Clin Oncol. 2005; 23: 7074-7080
        • Wheeler S.B.
        • Kuo T.M.
        • Durham D.
        • Frizzelle B.
        • Reeder-Hayes K.
        • Meyer A.M.
        Effects of distance to care and rural or urban residence on receipt of radiation therapy among North Carolina Medicare enrollees with breast cancer.
        N C Med J. 2014; 75: 239-246
        • Yao N.
        • Matthews S.A.
        • Hillemeier M.M.
        • Anderson R.T.
        Radiation therapy resources and guideline-concordant radiotherapy for early-stage breast cancer patients in an underserved region.
        Health Serv Res. 2013; 48: 1433-1449
        • Imperato P.J.
        • Waisman J.
        • Wallen M.D.
        • Llewellyn C.C.
        • Pryor V.
        Improvements in breast cancer pathology practices among medicare patients undergoing unilateral extended simple mastectomy.
        Am J Med Qual. 2003; 18: 164-170
        • Louis C.J.
        • Clark J.R.
        • Hillemeier M.M.
        • Camacho F.
        • Yao N.
        • Anderson R.T.
        The effects of hospital characteristics on delays in breast cancer diagnosis in Appalachian communities: A population-based study.
        J Rural Health. 2018; 34: S91-S103
        • Markossian T.W.
        • Hines R.B.
        Disparities in late stage diagnosis, treatment, and breast cancer-related death by race, age, and rural residence among women in Georgia.
        Women Health. 2012; 52: 317-335
        • Markossian T.W.
        • Hines R.B.
        • Bayakly R.
        Geographic and racial disparities in breast cancer-related outcomes in Georgia.
        Health Serv Res. 2014; 49: 481-501
        • Pollard K.
        • Jacobsen L.A.
        The Appalachian Region: A data overview from the 2006-2010 American community survey chartbook.
        (Available at:) (Accessed July 31, 2018)
        • Palmer J.D.
        • Patel T.T.
        • Eldredge-Hindy H.
        • et al.
        Patients undergoing radiation therapy are at risk of financial toxicity: a patient-based prospective survey study.
        Int J Radiat Oncol Biol Phys. 2018; 101: 299-305
        • McClelland 3rd, S.
        • Jaboin J.J.
        Will financial toxicity screening help or harm minority patient access to radiation therapy?.
        Int J Radiat Oncol Biol Phys. 2018; 101: 999-1000