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Published in final edited form as: Prev Med. 2021 Jul 22;152(Pt 2):106741. doi: 10.1016/j.ypmed.2021.106741

Identifying Key Barriers to Effective Breast Cancer Control in Rural Settings

Brian L Sprague 1,2,3,4, Thomas P Ahern 1,2,3, Sally D Herschorn 3,4, Michelle Sowden 2,3, Donald L Weaver 3,5, Marie E Wood 1,3,6
PMCID: PMC8545865  NIHMSID: NIHMS1732341  PMID: 34302837

Abstract

Breast cancer is the most common cancer and the second most common cause of cancer mortality among women in the United States. Efforts to promote breast cancer control in rural settings face specific challenges. Access to breast cancer screening, diagnosis, and treatment services is impaired by shortages of primary care and specialist providers, and geographic distance from medical facilities. Women in rural areas have comparable breast cancer mortality rates compared to women in urban settings, but this is due in large part to lower incidence rates and masks a substantial rural/urban disparity in breast cancer survival among women diagnosed with breast cancer. Mammography screening utilization rates are slightly lower among rural women than their urban counterparts, with a corresponding increase in late stage breast cancer. Differences in breast cancer survival persist after controlling for stage at diagnosis, largely due to disparities in access to treatment. Travel distance to treatment centers is the most substantial barrier to improved breast cancer outcomes in rural areas. While numerous interventions have been demonstrated in controlled studies to be effective in promoting treatment access and adherence, widespread dissemination in public health and clinical practice remains lacking. Efforts to improve breast cancer control in rural areas should focus on implementation strategies for improving access to breast cancer treatments.

Keywords: breast cancer, rural health, cancer control, cancer prevention, cancer screening, cancer treatment

Breast cancer is the most common cancer among women in the United States. Approximately 280,000 women are diagnosed with breast cancer and 40,000 women die from breast cancer each year (Siegel et al., 2021). Rural/urban disparities have been observed in cancer incidence and mortality for many organ sites (Henley et al., 2017). Breast cancer epidemiology demonstrates a unique pattern in that incidence is lower on average in rural areas than in urban areas, but breast cancer mortality rates are comparable due to the balancing effect of poorer survival rates among women diagnosed in rural settings. In this commentary the authors use the framework of the cancer control continuum to evaluate factors contributing to poorer breast cancer survival in rural areas, identify key barriers to improving outcomes, and discuss potential interventions that could reduce the burden of breast cancer in rural settings.

1. The epidemiology of breast cancer in rural settings

Over the past two decades, female breast cancer incidence has persistently been about 10% lower among women living in non-metropolitan versus metropolitan counties in the United States (Figure). Prior analyses suggest that socioeconomic status and healthcare provider density appear to explain much of the difference in incidence (Moss et al., 2017; Zahnd et al., 2018), as discussed in further detail below. Breast cancer mortality, however, is comparable in metropolitan and non-metropolitan areas, with a steady decline in both over the past two decades (Figure). The similar mortality rate despite lower incidence among rural women indicates that breast cancer survival is poorer among rural women compared with urban women. Data from the National Cancer Institute’s Surveillance, Epidemiology, and End Results (SEER) cancer registries indicate that the 10-year risk of breast cancer death among women diagnosed with breast cancer is 17.1% among women living in non-metropolitan counties, compared to 14.6% among women living in metropolitan counties (Surveillance Epidemiology and End Results Program, 2021). Poorer survival in rural areas could be due to differences in breast cancer biology (e.g., hormone receptor subtype), early detection and stage at diagnosis, access to high quality treatments, and access to follow-up surveillance imaging and supportive care. We review these factors below through the lens of the cancer control continuum.

Figure.

Figure.

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Age-adjusted female breast cancer incidence and mortality in the United States according to county-level urbanization. Incidence data (plotted on left axis) are from the SEER Cancer Registries (Surveillance Epidemiology and End Results Program) and mortality data (right axis) are from CDC Wonder (Centers for Disease Control and Prevention).

An important caveat in any discussion of breast cancer in rural areas is that not all rural areas are the same. For example, markers of socioeconomic status vary widely across different rural regions in the US (Singh et al., 2011). Likewise, breast cancer mortality varies across rural areas in the US, with lower mortality observed in western US states and highest mortality observed in southern US states (Callaghan et al., 2018). Thus, local public health initiatives and clinical interventions should be informed by the epidemiology of breast cancer and evaluation of barriers to breast cancer control in the specific rural setting of interest.

2. Prevention

The lower incidence of breast cancer in rural areas likely reflects differences in the prevalence of lifestyle and behavioral risk factors, many of which are associated with socioeconomic status. Unlike many chronic diseases and other cancers, breast cancer incidence increases with socioeconomic status (Heck and Pamuk, 1997; Yu et al., 2014). While socioeconomic indicators vary widely within urban and rural areas in the United States, overall 33.5% of urban residents have a college degree compared to 19.6% in rural counties and per-capita income was $56,567 in urban areas compared to $35,765 in rural areas (United States Department of Agriculture, 2021). Women of higher socioeconomic status tend to have a higher prevalence of some breast cancer risk factors, including low parity, late age at first birth, use of postmenopausal hormones, and alcohol consumption (Heck and Pamuk, 1997; Hiatt et al., 2020; Palmer et al., 2012; Suzuki et al., 2005). Greater access to and utilization of primary care and cancer screening services in urban areas also contributes to increased surveillance for breast cancer (Akinyemiju et al., 2015a; Moss et al., 2017), as discussed in further detail below.

Nevertheless, there remain opportunities for breast cancer prevention in rural areas. Rural women on average are less likely to be physically active and maintain healthy body weights (Bolin et al., 2015; Trivedi et al., 2015), which would be expected to increase breast cancer risk. Lifestyle and behavioral interventions tailored specifically to the needs of rural women (Cleland et al., 2017; Porter et al., 2019) would likely be more effective in achieving reductions in breast cancer incidence.

Breast cancer is a heterogeneous disease, with subtypes that differ in aggressiveness. Differences in risk factor profiles and access to early detection associated with socioeconomic status indicators translate to differential impacts on subtype-specific breast cancer incidence. Higher socioeconomic status is associated with higher incidence of hormone receptor positive breast cancer, which is generally slower growing and readily detected on mammography screening (Akinyemiju et al., 2015b). There is no difference by socioeconomic status in incidence of hormone receptor negative breast cancer, which is more aggressive and less likely to be detected on screening (Akinyemiju et al., 2015b). Thus, the elevated incidence of breast cancer in urban vs. rural areas consists primarily of the less aggressive subtypes. Data from the SEER cancer registries indicate that incidence of the most aggressive breast cancer subtype, triple negative for estrogen receptor, progesterone receptor, and HER2 expression, was comparable in rural areas (13.3 per 100,000; 95) and urban areas (13.2 per 100,000) during 2013-2017 (Surveillance Epidemiology and End Results Program, 2021).

3. Detection

Regular breast cancer screening is important for early detection of breast cancer. Access to a primary care provider is an important determinant of screening utilization (Schueler et al., 2008), has long been identified as an important factor for improving population health in rural areas (Kirby and Yabroff, 2020; Ricketts, 2005). A recent study reported that the density of primary care physicians in rural counties in the US in 2017 was 2.54 per 3500 residents compared with 3.25 per 3500 residents in urban counties (Zhang et al., 2020). Similarly, a low density of radiology facilities impairs utilization of mammography screening in rural areas. One prior study indicated that median travel times to breast imaging services were 4-8 times longer for rural vs. urban women (Onega et al., 2014).

Despite these challenges, the literature is mixed on the magnitude of differences in breast cancer screening utilization between urban and rural women, with wide variation across specific study populations. One meta-analysis concluded that women residing in rural areas were 41% less likely to have had a recent mammogram (Leung et al., 2014). However, national data from the Behavioral Risk Factor Surveillance System showed that, overall, women living in rural areas have self-reported breast cancer screening rates approximately 1-2% lower than women in urban areas (Tran and Tran, 2019). Notably, screening utilization rates have declined overall in the US over the past decade, including in rural areas (Jiang et al., 2015; Sprague et al., 2014a). While the reasons for this decline are not well understood, it is likely that public controversies about the optimal start age and frequency of breast cancer screening have had spillover effects that have reduced compliance with the consensus minimum recommendation of biennial screening for women aged 50-74. Efforts to promote breast cancer screening utilization continue to be needed.

Lower utilization of screening among rural women would be expected to result in a later stage at diagnosis. Again there is wide variation in the literature, but a systematic review and meta-analysis concluded that, overall, rural breast cancer patients had an approximately 20% increased odds of late stage breast cancer compared with urban breast cancer patients (Nguyen-Pham et al., 2014). A large study from the National Cancer Database reported that 33.9% of breast cancers diagnosed among women in rural areas were stage II or greater, compared to an overall population average of 30.9% (Obeng-Gyasi et al., 2020). Stage at diagnosis is a key determinant of breast cancer survival, thus these stage differences likely contribute to poorer outcomes among rural women diagnosed with breast cancer. Travel time to a mammography facility does not appear to be independently associated with stage at diagnosis after adjusting for age, race/ethnicity, census tract poverty, urban/rural residence, and health insurance status (Henry et al., 2011). This suggests that differences in stage at diagnosis between urban and rural women are likely due to complex interplays of cancer biology and healthcare access factors aside from travel distance.

Cancer fatalism – deterministic thoughts about the inability to prevent cancer or survive a cancer diagnosis – may also contribute to lower screening utilization and later stage at diagnosis. A national study found that fatalistic beliefs about cancer prevention are more common in rural compared to urban areas, even after adjusting for other sociodemographic factors (Befort et al., 2013). Fatalism has been associated with greater engagement in high-risk behaviors, avoidance of cancer screening, and delays in diagnosis (Beeken et al., 2011; Lyratzopoulos et al., 2015; Niederdeppe and Levy, 2007). Recent work suggests that interventions supporting health literacy and alleviating challenges in health information seeking may be effective in addressing cancer fatalism (Paige et al., 2021).

Importantly, mammography screening does not work equally well for all women. High risk women need supplementary screening with MRI in addition to mammography and women with dense breasts may also need alternative supplementary screening such as ultrasound, abbreviated MRI, or contrast mammography (Monticciolo et al., 2018). The availability of these modalities is limited outside of academic centers or specialty urban breast centers. Although high risk women account for a small percentage of the population, women with dense breasts comprise 40% of the screening population (Sprague et al., 2014b).

Apart from mammography utilization, mammography interpretive performance is known to vary widely across healthcare facilities and radiologists. Breast imaging specialists generally have better performance metrics (e.g., sensitivity and specificity) compared to general radiologists, and performance improves with volume and years of experience (Smith-Bindman et al., 2005; Smith-Bindman et al., 2008). Many rural facilities are served by general radiologists who read lower volumes. However, national data from the Breast Cancer Surveillance Consortium (BCSC) indicate that overall the accuracy of screening mammography performance is comparable at rural and urban facilities (Goldman et al., 2008). Thus, as a whole, women undergoing mammography screening in rural areas do not appear to experience poorer screening accuracy than women in urban areas.

4. Diagnosis

High quality diagnostic services, including diagnostic imaging and biopsy, are important for prompt, accurate, and comprehensive diagnosis of breast cancer. Women with an abnormal mammography screening exam and women presenting with symptoms undergo diagnostic imaging, which may include diagnostic mammography views and/or ultrasound imaging. Reports from the BCSC indicate that the timeliness of follow-up with additional imaging after an abnormal screening exam is comparable at urban vs. rural facilities (Rosenberg et al., 2011). Rural mammography facilities also have comparable diagnostic mammography sensitivity compared to urban facilities, but have poorer diagnostic mammography specificity with an approximately 55% higher false positive rate (Goldman et al., 2011). Thus, women undergoing diagnostic breast imaging at rural facilities are more likely to experience a higher burden additional imaging and biopsies for benign lesions. The timeliness of biopsy following positive diagnostic imaging is also slower in rural facilities compared to urban facilities, and more women in rural areas never complete their recommended biopsy (Goldman et al., 2013).

Clinical best practice for biopsy of suspected breast cancer is core needle biopsy, which provides numerous advantages over surgical biopsy including increased patient safety and comfort, preservation of tumor margins, and facilitation of neo-adjuvant therapy for women with a positive biopsy finding (The American Society of Breast Surgeons, 2017). While national data indicates substantial progress over the past decade in expanding use of core needle biopsy (Teberian et al., 2020), there remain concerns about continued use of surgical biopsy in rural areas where earlier studies suggested access to minimally invasive breast biopsy technology was limited (Adepoju et al., 2014; James et al., 2012; Zimmermann et al., 2013). Updated evidence is needed to evaluate the degree to which this remains a barrier to high quality breast cancer diagnosis in rural settings.

5. Treatment

There is widespread evidence that access to high quality breast cancer treatment is an important barrier in rural areas. The American Society of Clinical Oncology has estimated that less than 6% of oncologists work in rural settings and 70% of counties in the United States do not have even a single oncologist (American Society of Clinical Oncology, 2017). A recent study of data from the SEER cancer registries showed that breast cancer patients living in rural areas traveled nearly 3 times as far as those from urban areas (40.8 miles vs. 15.4 miles) to reach a facility for radiation treatment (Longacre et al., 2020). Long travel time have been associated with treatment choice, including increased use of mastectomy compared to breast conserving surgery, reduced receipt of radiation treatment, and delay in initiation of chemotherapy (Johnson et al., 2016; Lin et al., 2018; Onega et al., 2011). Similarly, women living in rural states are less likely to receive radiation therapy after breast conserving surgery and guideline-concordant adjuvant endocrine therapy (Camacho et al., 2017; Martinez et al., 2012). Newer techniques in surgical care of breast cancer appear to lag in rural areas as well. For example, the adoption of sentinel lymph node biopsy was much slower in rural hospitals, lagging at least two years behind their urban counterparts, likely due to a lack of sub-specialists and difficulties with rural surgeons accessing training for new techniques (Arrington et al., 2013).

Aside from geographic proximity to specialty care, socioeconomic factors are likely to mediate urban/rural differences in access and adherence to treatments. Numerous studies have demonstrated poorer access to treatment and poorer breast cancer survival among women with low income, lower educational attainment, and women covered by Medicaid (Abdel-Rahman, 2019; Dreyer et al., 2018; Sprague et al., 2011).

An analysis of data from randomized clinical trials showed that rural women enrolled in trials have similar outcomes as urban women in those trials, suggesting that when treatments are carefully managed and provided equitably, and after controlling for stage at diagnosis, there is nothing inherent to rural breast cancer that leads to poorer outcomes (Unger et al., 2018). Efforts are urgently needed to realize these equitable outcomes in community practice.

6. Survivorship

Following primary treatment, women diagnosed with breast cancer have special healthcare needs, including surveillance for breast cancer recurrence, screening for second primary cancers, assessment and management of physical and psychological long-term and late effects of breast cancer and treatment, health promotion to reduce recurrence risk and improve quality of life, and care coordination (Runowicz et al., 2016). The American Cancer Society and American Society of Clinical Oncology recommend annual mammography surveillance for breast cancer survivors who received a unilateral mastectomy or underwent breast conserving surgery (Runowicz et al., 2016). A meta-analysis concluded that detection of breast cancer recurrence by mammography when it was still asymptomatic was associated with reduction in absolute breast cancer mortality of approximately 20% compared to symptomatic detection (Lu et al., 2009). Rural residence and travel time to a mammography facility do not appear to be associated with adherence to mammography surveillance imaging or follow-up with an oncology specialist (Keating et al., 2006; Onega et al., 2011; Quyyumi et al., 2019).

The American College of Radiology recommends annual MRI surveillance for women with a personal history of breast cancer who also have dense breasts, and all women diagnosed with breast cancer before age 50 (Monticciolo et al., 2018). While utilization of MRI surveillance among rural women has not been well characterized, the limited availability of breast MRI in rural areas likely impairs access (Lee et al., 2016; Onega et al., 2016).

A number of behavioral aspects, including physical inactivity, smoking, and obesity have been associated with breast cancer recurrence and survival (Chan et al., 2014; Lahart et al., 2018; McLaughlin et al., 2014; Veal et al., 2017). While there is widespread variability across and within rural and urban regions in the US, on the whole, smoking and physical inactivity among cancer survivors are more prevalent in rural areas while obesity rates are comparable (Weaver et al., 2013). Numerous interventions and health promotion programs have been designed to support healthy behaviors among breast cancer survivors (Chlebowski and Reeves, 2016; Fong et al., 2012; Knobf and Coviello, 2011). Access to programs based at healthcare facilities may be limited for rural residents due to long travel distance, but a number of home-, telephone-, and telemedicine interventions have been shown to be comparable in effectiveness to clinic-based interventions (Cheng et al., 2017; Harvey et al., 2017; Smith-Turchyn et al., 2020).

A recent review found that there are significant gaps in our knowledge of care coordination among rural breast cancer survivors (Anbari et al., 2020). Relevant domains include access to a multidisciplinary care team, management of treatment side effects, psychosocial support, and the effectiveness of survivorship care plans. Further research is needed to identify critical barriers in these areas – the limited access to primary care and cancer specialists in rural areas raises particular concerns about these domains.

7. Interventions

A number of interventions have been demonstrated to improve breast cancer screening, diagnosis, treatment, and survivorship care in rural settings. A full review of these is beyond the scope of this commentary, but briefly, these include patient navigation programs, mobile imaging and treatment services, remote interpretation of diagnostic imaging by breast imaging specialists, guest housing near oncology practices, transportation assistance programs, and telemedicine approaches (Charlton et al., 2015; Hughes et al., 2020; Petereit et al., 2016; Roland et al., 2017; Sabesan et al., 2012; Smith-Turchyn et al., 2020). Specific telemedicine areas identified for cancer care include patient-provider videoconferencing for genetic counseling, symptom management, behavioral health support, medication adherence, and palliative care (Sirintrapun and Lopez, 2018).

A particularly advantageous use of patient navigation in the rural setting is facilitating consultation with all specialists involved in a patient’s care on one day to minimize travel time and time away from work. This can be accomplished in conjunction with a provider pre-visit chart review to assess the need for additional imaging and laboratory testing so that it can be scheduled on the same visit day. Navigators are also essential in setting up televideo visits with providers such as genetic counselors, who may not need to perform a physical examination. Clustered and remote visits allow patients to receive state of the art care with less impact on their day to day life.

While these interventions have been shown to improve care in rural settings, there are significant barriers to widespread implementation of these findings. Important barriers include inadequate financial incentives, subsidies, and/or reimbursement to make these practices financially sustainable. This is particularly challenging given the financial pressures on many small rural hospitals and clinics. The COVID-19 pandemic has dramatically increased the utilization of telehealth approaches throughout all aspects of medicine, and the associated policy changes and newly developed infrastructure may greatly facilitate the delivery of high quality cancer care in rural areas. However, early evidence suggests that uptake of telehealth approaches have lagged in rural compared to urban areas (Jaffe et al., 2020), with access to broadband internet identified as a key barrier (Hirko et al., 2020).

8. Conclusion

Women living in rural areas have lower overall incidence of breast cancer but similar incidence of aggressive breast cancer subtypes compared to women in urban areas. Rural women have slightly lower use of screening mammography, and tend to have a somewhat later stage at diagnosis. Larger disparities are found in the areas of diagnostic work-up and treatment. Women in rural areas experience higher false positive rates on diagnostic mammography, delays in biopsy, lower access to core needle biopsy, and impaired access to treatments. Thus, initiatives seeking to improve access to high quality diagnostic management and treatments would be expected to provide the most benefit for improving breast cancer outcomes in rural settings.

Rural disparities in breast cancer control are most pronounced in the diagnostic and treatment settings. Access to high quality specialized care is a significant challenge, due largely to long travel times associated with the dearth of oncology specialists in rural areas. Care requiring multiple visits, such as radiation treatments and chemotherapy, is particularly challenging. Healthcare finance reform is needed to support the implementation of existing interventions shown to improve access to care for rural patients.

HIGHLIGHTS.

  • Rural women living have lower incidence of breast cancer compared to women in urban areas.

  • Rural women have lower use of screening mammography and are more likely to have a late stage breast cancer diagnosis.

  • Women in rural areas experience substantial barriers to accessing high quality diagnostic care and treatments.

  • Initiatives to improve access to guideline concordant treatments and survivorship care in rural areas are needed.

ACKNOWLEDGEMENTS

Funding

This work was supported in part by a Centers of Biomedical Research Excellence award (P20GM103644) from the National Institute of General Medical Sciences and research grants (U01CA196383, R01CA248068) from the National Cancer Institute.

Role of the Funder/Sponsor

The sponsors had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.

ABBREVIATIONS

SEER

Surveillance, Epidemiology and End Results Program

CDC

Centers for Disease Control and Prevention

BCSC

Breast Cancer Surveillance Consortium

Footnotes

Conflict of Interest Disclosures

The authors have no conflicts of interest to disclose.

Declaration of interests

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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