Identifying and improving disparities in esophageal cancer care: a narrative review

Introduction

Background and epidemiology

Esophageal cancer is the 6^th leading cause of tumor-related deaths and the 8^th most common cancer worldwide. It is the 7^th most common cancer in men and the 13^th most common cancer in women. The incidence is roughly 600,000 cases in 2020 worldwide (1).

There are two predominant types of esophageal cancer: squamous cell carcinoma (SqCC) and adenocarcinoma (ADC). SqCC is predominant in developing countries, particularly in a region called the Esophageal Cancer Belt which includes Central Asia, North and Central China, Iran, etc. (2). ADC is more predominant in developed countries such as North America, Australia, and Western Europe (3,4). However, there are a few clusters of SqCC in developed countries such as northwestern France, Iceland, Scotland, and Finland, and in the United States in coastal South Carolina and metropolitan Washington, DC/Baltimore (4).

The global financial burden of esophageal cancer is significantly high amounting to 9.78 million disability-adjusted life years and is increasing with the increase of new cases by 52.3% and number of deaths by 40% (5,6). The median hospital charge for esophagectomy in the United States is quoted at roughly $59,000 which places uninsured patients at risk of financial toxicity (7). Furthermore, only 30–40% of patients undergoing esophagectomy return to work at 1 year and a concerning 30% never return to work (8). Center for Medicare and Medicaid has required hospitals to report social determinants of health (SDOH) with inpatient quality reporting starting in 2024 and will soon be tied to reimbursements (9).

Rationale and knowledge gap

SDOH disproportionately affects the natural history of esophageal cancer. Surgeons are key stakeholders in improving outcomes for esophageal cancer. The delivery of cancer care is affected by a complex multifactorial construct of socio-economic status (SES). To better understand these healthcare disparities, Delman et al. defined five themes of disparities: patient-level factors, provider-level factors, system and access issues, clinical care and quality, and postoperative outcomes, care, and rehabilitation (10). To execute equitable healthcare across several socio-economic levels, each of these themes needs to be addressed.

Many surgeons do not believe that SDOH is a surgical problem, rather it is a more upstream problem of primary care. Long gone are the days when surgeons only came at the end of the pipeline, as advanced technicians to perform esophagectomies (11). Surgical care does not begin in the operating room. It begins at the onset of the disease process or arguably even before. There is an increasing interest in SDOH and its impact on surgical quality. Everyone from primary care to surgery has a role to play in building these ‘clinical community relationships’ and contribute to tackling the complex construct of SDOH and how it affects overall patient outcomes (12). It is time for surgeons to be involved not only in biology but also in the social aspect of diseases for better patient care access, delivery, and outcomes. Advocacy for policy change is the responsibility of surgeons as much as any other discipline. It is high time we took charge of these responsibilities.

Objective

Our objective was to identify disparities in esophageal cancer originating from SDOH. This would provide actionable targets for surgeons and healthcare providers to improve esophageal cancer outcomes. We present this article in accordance with the Narrative Review reporting checklist (available at https://ccts.amegroups.com/article/view/10.21037/ccts-23-24/rc).

Methods

We searched English publications in PubMed and Ovid MEDLINE with the phrases “social determinants of esophageal cancer”, “healthcare disparities in esophageal cancer”, “high-income, low income”, “social inequality”, “social class”, “poverty”, “urban-rural”, “economic factors”, and “food deserts”. The complete list is detailed in Table 1. We included clinical trials, case reports, case series, retrospective studies, literature, and systematic reviews. Our search yielded 737 papers. We excluded papers not available in English. We included 92 papers between 1999 and 2023 in our literature review based on appropriate relevance.

Discussion

Role of surgeons in esophageal cancer shared decision model

Oncologic care is complex due to the intricacies of risk factors, variations in tumor biology, and various SDOH, thus needing a multidisciplinary approach (13). We have seen the care pathways shift towards the integration of surgeons in the early decision-making in breast (14), colorectal (15), and lung cancer (16). Randhawa et al. call for surgeons to be involved in designing screening programs and care pathways early on to develop a shared decision model, minimizing unwarranted procedures and complications (16). There are Society of Thoracic Surgeons outlines for lung cancer screening which are designed by surgeons (17). Similar outlines and focused guidelines are needed for esophageal cancer as well. Furthermore, many surgeons in low- and middle-income countries find themselves in the position of managing peri-operative chemotherapy due to a shortage of specialized medical oncologists and sometimes even managing their overall oncologic care, not just the surgical aspect. In high-income countries, medicine is progressively becoming personalized. There is increasing interest in understanding the effects of SDOH on perioperative care (18). Therefore, it is incumbent that surgeons are involved in esophageal cancer patient care early on to streamline the process and practice personalized medicine considering not only the tumor biology and genetics but also their unique SDOH that are closely tied to the development of esophageal cancer disease process and its contribution to patient outcomes and surgical complications.

Components of SDOH

SDOH is a complex construct with multiple components such as race, income, education, occupation, housing, neighborhood, etc. Different indexes are available to analyze SDOH such as the Social Vulnerability Index (SVI) (19) or Area Deprivation Index in the United States (20). However, no index comprehensively catches all the contributing factors. Here, we describe some of the common contributing factors that complicate esophageal cancer development and care delivery. The risk factors of esophageal cancer are outlined in Table 2 and the socio-economic conditions associated with adverse outcomes including post-operative outcomes are outlined in Table 3.

Race

Studies show that minority groups are more likely to be diagnosed at a higher stage {odds ratio (OR) 1.64 [95% confidence interval (CI): 1.53, 1.76] African Americans, 1.19 (1.08, 1.32) Hispanics, 1.78 (1.55, 2.06) Asians} (21). This could be due to a lack of access to early screening or delay in seeking care due to financial constraints in these subgroups. African Americans are more likely to be either offered no treatment (22) or not offered surgery for stage-appropriate diagnosis (16.3% versus 33.1% overall) (21,23-26). African Americans are less than half as likely to undergo esophagectomy compared to Caucasians [OR 0.31 (95% CI: 0.25, 0.38)] (27). If offered surgery, they are more likely to refuse it or not undergo it for multifactorial reasons (28-30). Furthermore, immigrants were less likely to undergo esophagectomy compared to US citizens (42% vs. 76%, P=0.001) (31). When undergoing surgery, African Americans are less likely to utilize high-volume hospitals [OR 0.18 (95% CI: 0.14, 0.24)] even if they live within 10 miles of a high volume center (32,33). Operations performed in high-volume centers has lower mortality [OR 0.48 (95% CI: 0.35, 0.65)] and complication rates. This further worsens the post-surgical outcomes making mortality rate for African American patients almost twice that of their Caucasian counterparts [OR 2.04 (95% CI: 1.5, 4.03)] (32,34). A similar trend is noted in the Hispanic population (35). However, if Hispanics [hazard ratio 0.82 (95% CI: 0.79, 0.85)] and Asians [hazard ratio 0.78 (95% CI: 0.74, 0.83)] received surgery, improved survival was observed compared to Caucasians (21). This raises the question of why the surgical outcomes within minority populations are different and what can be done to improve them. Their post-surgical care pattern should be studied in a granular manner.

Education

Low education level was closely related to certain risk factors causing SqCC such as cigarette smoking [OR 4.2 (95% CI: 2.5, 7)], betel chewing [OR 2.3 (95% CI: 1.6, 3.4)], and alcohol abuse [OR 13.9 (95% CI: 9.1, 21.2)] (36). The combined effect of the 3 can have up to 40 times higher risk of SqCC indicating a dose-response relationship. High school education or higher is associated with a decreased risk of SqCC [OR 0.6 (95% CI: 0.41, 0.87)] (37,38). Significant delay [15 (range, 4–64) weeks] in seeking care and staying consistent with screening was also noted with low education levels (39). There is a 50% higher chance of being allocated to curative treatment for higher education level and subsequent adherence to treatment rendering improved survival (40-42) and quality of life (43). Patients with lower education levels were less likely to be offered any treatment [OR 1.6 (95% CI: 1.3, 2)] (22). It is incumbent on surgeons and other healthcare providers to identify patients with poor medical literacy and ensure they are provided stage-specific timely care.

Income

Income and by-extension insurance status (in the United States) are closely tied to delays in the diagnosis and treatment of esophageal cancers. Low-income bracket groups and patients with no insurance or with Medicare/Medicaid insurance are at risk of being diagnosed at a higher stage (71% diagnosed at stage III or IV) (44,45) and longer time to surgery or neoadjuvant or definitive chemoradiotherapy [OR 1.98 (95% CI: 1.49, 2.62)] (31,46) increasing peri-operative and post-operative mortality (median survival 26 versus 40 months, log-rank P<0.001) (22,38,41,47-51). The delay in seeking care was related to fear of losing jobs and livelihood, limited access to specialized care, and associated transportation costs (52). Medicare and Medicaid patients had higher chances of not being offered any treatment when diagnosed as stage II and stage III (22). Low SES patients also had a decreased rate of seeking a second opinion (24% vs. 66% P<0.01) (53). Lower-income patients need stronger social worker support to obtain care and maintain appropriate follow-up after surgery for better outcomes.

Regionalization

Esophageal cancer patients who live in rural areas have a higher incidence (OR: 29.52) and worse prognosis than those who live in urban areas (54,55). There is approximately a 20% higher risk of death among rural patients than among urban patients in the first three years of diagnosis (48,56,57) despite reportedly receiving equivalent post-operative care (58). The condition is worsened by the paucity of peri-operative chemotherapy and radiation therapy centers in rural areas (59). One study analyzed that outcomes worsen with the increase of distance from the cancer center starting at 10 km (60). However, the etiology of this difference based on distance is not very well comprehended.

High-volume esophagectomy centers (minimum 20 esophagectomy, 3 surgeons) are primarily located in urban areas. Esophagectomies at high-volume hospitals are associated with lower mortality (61) and 40% lower complication rate (62). Furthermore, patients who traveled longer distances to high-volume centers were more likely to undergo esophagectomy than those who received care in local low-volume centers (25,63). Regionalization of esophageal cancer (minimum of 15 per year) has been implemented in several countries due to the aforementioned findings (64,65).

Dietary habits

Dietary habits are responsible for different histology of esophageal cancers differently. Smoking and alcohol use are known risk factors for both ADC and SqCC while diets enriched with fruits and vegetables are protective against them and reduce risk by 30% (54,66-70). ADC is associated with obesity resulting in gastroesophageal reflux disease and Barrett’s Esophagus causing columnar metaplasia of the distal esophagus. High-calorie diets with protein and cholesterol diets have been associated with an increased risk of ADC (4).

The risk factors for SqCC are slightly more well-defined. Along with smoking and alcohol abuse, drinking hot beverages such as tea or coffee more than twice a day has a 5-fold increase in SqCC risk (71,72). Red meat consumption above the 75^th percentile increases the odds of SqCC by almost 3 fold while consumption of fish decreases the risk by 68% (73). These diets are often measured with the High Dietary Inflammatory Index (DII) to determine risk for SqCC (74). Some region-specific risk factors for SqCC are khat chewing (Ethiopia) (66), consumption of maize beer (contains mycotoxins) (75) in South Africa, drinking of sugar-distilled beverages in Puerto Rico, moonshine whiskeys in South Carolina, chewing areca nut in South and Southeast Asia (4), consumption of N-nitroso compounds in smoked food in Japan (76), and consumption of pickled vegetables, salted meat, and barbecued food in China (77).

Cessation of these habits for surgery is paramount. Involvement of surgeons early in the care of these patients with risk factors can allow for early counseling and gradual discontinuation instead of quitting instantly before surgery which can be coupled with relapse post-surgically.

Food deserts

Food deserts and food insecurity disproportionately affect the population across the globe. In developed countries, it manifests as cheap high-caloric fast foods devoid of fresh fruits and vegetables resulting in obesity and in turn ADC (78). On the flip side, in developing countries, food insecurity (defined as hunger and hidden hunger) results in malnutrition. Many people in these low-income countries resort to addictive appetite-reducing behavior such as khat, tobacco, or areca nut chewing which are known risk factors for SqCC (79,80).

The outcomes of patients with esophageal cancer residing in these food deserts are not very well studied. The only known outcome is the 5-fold readmission rate of esophagectomy patients residing in these food deserts (81,82). This is an important area to explore to understand the complicated relationship between the two and improve post-esophagectomy outcomes.

SES index

Healthcare disparities are a complex and multifactorial construct. Deconstructing this into simple pieces as above gives us a simpler understanding of the contribution of each component but to understand the complete influence of the disparities the different components need to be studied together systematically. Different SES indexes have thus come into existence. Each has its unique characteristics and usages. They are predominantly influenced by income, race, neighborhood of residence, etc. However, there is no singular way to analyze SDOH. Table 4 outlines some of the different indexes available for analyzing SDOH. Using the income domain of the Index of Multiple Deprivation as a marker for SES, Henson et al. found that more deprived patients were consistently less likely to be treated with chemotherapy alone [OR 0.82 (95% CI: 0.78, 0.87)] or chemotherapy and radiotherapy combined [OR 0.78 (95% CI: 0.71, 0.85)] compared to privileged patients with equally advanced disease (83).

Using neighborhood-level postal codes and combining mean household income and the mean value of housing, as provided by the Netherlands Statistics Agency as a marker for SES, Bus et al. commented on the advanced age and tumor stage at the time of diagnosis for low SES patients (84). Wang et al. found the same using religion, years of schooling and high education, place of residence (rural or urban), occupation, annual household income, and insurance as SES markers (85).

Using economic characteristics such as household fuel consumption, residential facilities, personal family facilities, household appliances used by the family, the source of household income, and total monthly household income as the basis of SES. Zarean and colleagues reported the inferior outcomes of low SES groups such as mortality, surgery rate, and survival (86,87). This demonstrates that deprivation indices have the potential to be integrated with the electronic medical record. Such an endeavor can lead to early identification of at-risk patients and pre-emptive measures to counteract disparities from SDOH (Table 5).

Conclusion and future directions

Surgeons and providers treating esophageal cancer need to recognize the disparities in outcomes arising from SDOH. SDOH affecting esophageal cancer care include but are not limited to race, income, education, and food deserts. Strategies to improve outcomes include regionalization, increasing social worker engagement, integrating electronic medical records with automatically calculated disparity indices, and use of telehealth for closer post-operative follow-up.

Acknowledgments

Funding: None.

Footnote

Reporting Checklist: The authors have completed the Narrative Review reporting checklist. Available at https://ccts.amegroups.com/article/view/10.21037/ccts-23-24/rc

Peer Review File: Available at https://ccts.amegroups.com/article/view/10.21037/ccts-23-24/prf

Conflicts of Interest: Both authors have completed the ICMJE uniform disclosure form (available at https://ccts.amegroups.com/article/view/10.21037/ccts-23-24/coif). M.S. serves as an unpaid editorial board member of Current Challenges of Thoracic Surgery from July 2023 to June 2025. The other author has no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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