eTable. Kaplan-Meier 5-Year Overall Survival Stratified by Insurance Status
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Shin JY, Yoon JK, Shin AK, Blumenfeld P, Mai M, Diaz AZ. Association of Insurance and Community-Level Socioeconomic Status With Treatment and Outcome of Squamous Cell Carcinoma of the Pharynx. JAMA Otolaryngol Head Neck Surg. 2017;143(9):899–907. doi:https://doi.org/10.1001/jamaoto.2017.0837
What is the association of insurance and community-level socioeconomic status with outcomes for patients with squamous cell carcinoma of the pharynx?
In this study of the National Cancer Database records of 35 559 patients with squamous cell carcinoma of the pharynx, patients with private insurance or higher household income had earlier disease status at presentation, were likely to start their primary treatment earlier, and had better outcomes compared with patients who were uninsured or had lower household income.
Insurance status and household income level are important independent prognosticators for overall survival.
Community-level socioeconomic status, particularly insurance status, is increasingly becoming important as a possible determinant in patient outcomes.
To determine the association of insurance and community-level socioeconomic status with outcome for patients with pharyngeal squamous cell carcinoma (SCC).
Design, Setting, and Participants
This study extracted data from more than 1500 Commission on Cancer–accredited facilities collected in the National Cancer Database. A total of 35 559 patients diagnosed with SCC of the pharynx from 2004 through 2013 were identified. The χ2 test, Kaplan-Meier method, and Cox regression models were used to analyze data from April 1, 2016, through April 16, 2017.
Main Outcomes and Measures
Overall survival was defined as time to death from the date of diagnosis.
Among the 35 559 patients identified (75.6% men and 24.4% women; median age, 61 years [range, 18-90 years]), 15 146 (42.6%) had Medicare coverage; 13 061 (36.7%), private insurance; 4881 (13.7%), Medicaid coverage; and 2471 (6.9%), no insurance. Uninsured patients and Medicaid recipients were more likely to be younger, black, or Hispanic; to have lower median household income and lower educational attainment; to present with higher TNM stages of disease; and to start primary treatment at a later time from diagnosis. Those with private insurance (reference group) had significantly better overall survival than uninsured patients (hazard ratio [HR], 1.72; 95% CI, 1.59-1.87), Medicaid recipients (HR, 1.99; 95% CI, 1.88-2.12), or Medicare recipients (HR, 2.07; 95% CI, 1.99-2.16), as did those with median household income of at least $63 000 (reference) vs $48 000 to $62 999 (HR, 1.19; 95% CI, 1.13-1.26), $38 000 to $47 999 (HR, 1.31; 95% CI, 1.24-1.38), and less than $38 000 (HR, 1.51; 95% CI, 1.43-1.59). On multivariable analysis, insurance status and median household income remained independent prognostic factors for overall survival even after accounting for educational attainment, race, Charlson/Deyo comorbidity score, disease site, and TNM stage of disease.
Conclusions and Relevance
Insurance status and household income level are associated with outcome in patients with SCC of the pharynx. Those without insurance and with lower household income may significantly benefit from improving access to adequate, timely medical care. Additional investigations are necessary to develop targeted interventions to optimize access to standard medical treatments, adherence to physician management recommendations, and subsequently, prognosis in these patients at risk.
An estimated 16 420 new cases of pharyngeal cancer were diagnosed in the United States in 2016, with an estimated 3080 deaths.1 The pharynx is generally divided into the nasopharynx, oropharynx, and the hypopharynx.2 Known prognostic factors for nasopharyngeal carcinoma include tumor and nodal stage, involved neck node locations, and DNA levels of Epstein-Barr virus.3,4 Human papillomavirus infection, age at diagnosis, race, tumor and nodal stage, and number of pack-years of tobacco smoking are known determinants of overall survival (OS) for oropharyngeal squamous cell carcinoma (SCC).5 Tumor location, age, sex, and race are known prognosticators in patients with cancer of the hypopharynx.6,7
In addition to biological and disease factors, community-level socioeconomic status (SES), particularly insurance status, is increasingly being analyzed as a possible determinant in patient outcomes.8-10 On March 23, 2010, President Barack Obama introduced the Affordable Care Act, which brought significant regulatory changes of the US health care system that were intended to increase access to affordable and quality health insurance coverage.11 In 2014, 10.4% of the US population was noted to be uninsured for the entire calendar year, a decrease from 13.3% in 2013.12 Studies on several cancer types, including lung, breast, colorectal, and testicular, have demonstrated that patients without medical insurance have more difficulty gaining adequate access to care, with associated poorer outcomes.13-16 The objective of this hospital-based retrospective study of 35 559 patients diagnosed with SCC of the pharynx was to determine the association of insurance and community-level SES with the treatment and prognosis for patients in the United States to potentially identify those who may be more vulnerable to poorer disease outcomes.
Our study population consisted of 35 559 patients diagnosed with SCC of the nasopharynx, oropharynx, hypopharynx, or pharynx not otherwise specified (International Classification of Diseases for Oncology, Third Edition histology codes 8070/3 to 8078/3) from 2004 through 2013 in the National Cancer Database (NCDB). The NCDB contains hospital registry data collected from more than 1500 Commission on Cancer–accredited facilities representing 70% of newly diagnosed cancer cases annually in the United States.17 The NCDB is a joint project of the Commission on Cancer of the American College of Surgeons and the American Cancer Society. The data used in our investigation are derived from a deidentified NCDB file. This study was approved by the institutional review board of Rush University Medical Center, Chicago, Illinois, which waived the need for informed consent for use of these deidentified data.
Insurance status was identified as the patient’s primary insurance carrier at the time of initial diagnosis and/or treatment.17 For each patient’s area of residence, the median household income and measure of educational attainment were estimated by matching the patient’s zip code recorded at the time of diagnosis against files derived from the 2012 American Community Survey data from 2008 through 2012 and adjusted for 2012 inflation with regard to income. Categories supplied by the NCDB for insurance status include uninsured, private, Medicaid, and Medicare. Categories for median household income include less than $38 000, $38 000 to $47 999, $48 000 to $62 999, and $63 000 or more. Categories for measure of educational attainment (percentage of adults in the patient’s zip code who graduated from high school) include 79% or less, 79.1% to 87.0%, 87.1% to 93.0%, and more than 93.0%. The American Community Survey collects information on a large number of economic, social, and demographic characteristics of persons, as well as housing characteristics.18 The survey is conducted by collecting data from a random sample of housing unit addresses every month, for a total of 3.5 million housing units contacted each year.18 The US Census Bureau presents annual estimates of median household income and poverty by state and other smaller geographic units based on data collected in the American Community Survey.19 Five-year income and poverty estimates are available for all geographic units, including census tracts and block groups by pooling 5 years of American Community Survey data.19 Comorbidities as described by the Charlson/Deyo comorbidity score were defined by a weighted score derived from the sum of the scores for each of the comorbid conditions listed in the Charlson/Deyo comorbidity score mapping table.20,21 A score of 0 indicated no significant comorbid conditions, and higher scores indicated greater comorbidity burden. Because of the small proportion of cases with a Charlson/Deyo comorbidity score exceeding 2, the NCDB has truncated the data to 0, 1, and 2 (>1). Patients younger than 18 years or whose insurance or community-level SES were unknown was excluded from our analysis.
Data for this study were analyzed from April 1, 2016, through April 16, 2017. All data analyses were performed using SPSS software (version 22.0; IBM Corp). Proportional distribution of demographic and clinicopathologic factors and treatment by insurance status were compared using the 2-tailed χ2 test. The χ2 test of independence was used to determine whether an association between categorical variables existed. A cross-tabulation was performed, and the P value (significance level of .05) was used to determine whether the null hypothesis (no significant difference between specified populations, with any observed difference due to sampling error) could be rejected and whether a statistical association between categorical variables existed. Kaplan-Meier estimates were used to analyze estimates for our primary end point, which was OS, with the comparison of rates among the groups performed using the 2-tailed log-rank test. The OS end point was defined as time to death from the date of diagnosis of SCC of the pharynx. The 2009-2013 subgroup was excluded from 5-year OS calculation to allow for a minimum of 5 years of follow-up for data available through 2013. Factors significant on univariate analysis were included in Cox regression multivariable analysis, which was used to compute hazard ratios (HRs) with 95% CIs to identify independent prognostic factors for OS using a forward-selection variable-selection process. A 2-sided P < .05 was considered statistically significant.
A total of 35 559 patients (75.6% men and 24.4% women) with SCC of the pharynx who received the diagnosis from 2004 through 2013 were identified (Table 1). The median patient age was 61 years (range, 18-90 years); 15 146 (42.6%) were Medicare recipients, 13 061 (36.7%) had private insurance, 4881 (13.7%) were Medicaid recipients, and 2471 (6.9%) were uninsured. Uninsured patients or Medicaid recipients were significantly more likely to be younger, have lower median household incomes, live in areas with lower educational attainment, present with more advanced TNM stage of disease, and start primary treatment at a later time from diagnosis (Table 1).
The median time to follow-up was 24.9 months (range, 1.0-130.5 months). Five-year OS for the study population was 35.6% (eTable in the Supplement). White (reference group), Hispanic (HR, 0.96; 95% CI, 0.85-1.10), and Asian (HR, 0.51; 95% CI, 0.43-0.59) patients had significantly better OS than did black patients (HR, 1.27; 95% CI, 1.19-1.34) (Table 2). Those with private insurance (reference group) had significantly better OS than did uninsured patients (HR, 1.72; 95% CI, 1.59-1.87), Medicaid recipients (HR, 1.99; 95% CI, 1.88-2.12), or Medicare recipients (HR, 2.07; 95% CI, 1.99-2.16) (Figure 1), as did those with a median household income of $63 000 or higher (reference group) compared with $48 000 to $62 999 (HR, 1.19; 95% CI, 1.13-1.26), $38 000 to $47 999 (HR, 1.31; 95% CI, 1.24-1.38), or less than $38 000 (HR, 1.51; 95% CI, 1.43-1.59) (Figure 2). Univariate analysis also revealed that educational attainment, Charlson/Deyo comorbidity score, and TNM stage of disease were statistically significant outcome factors (Table 2).
On Cox regression multivariable analysis, private medical insurance, compared with no insurance (HR, 1.39; 95% CI, 1.26-1.54), Medicaid (HR, 1.59; 95% CI, 1.47-1.72), and Medicare(HR, 1.81; 95% CI, 1.71-1.91), and median household income of at least $63 000, compared with $48 000 to $62 999 (HR, 1.08; 95% CI, 1.00-1.16), $38 000 to $47 999 (HR, 1.10; 95% CI, 1.02-1.19), and less than $38 000 (HR, 1.15; 95% CI, 1.06-1.26), were significant prognosticators for improved OS. Lower Charlson/Deyo comorbidity score and lower TNM stage of disease also were significant prognostic factors for better OS (Table 3).
In our hospital-based analysis of 35 559 patients with SCC of the pharynx, insurance status and household income level were significantly associated with outcome. Those with private insurance presented with earlier stages of disease, started primary treatment sooner, and had significantly better outcomes than did uninsured patients or Medicaid or Medicare recipients.
As the US health care system becomes increasingly driven by insurers, the need to explore the association of insurance and community-level SES with oncologic care and outcome is mounting, especially in an era of increasing premiums for insurance coverage and costs for diagnosis and treatment.22-24 Patients diagnosed with a serious medical condition such as a malignant neoplasm may not possess the means to receive necessary resources for optimal management and thus are at risk for poorer prognosis. In a Surveillance, Epidemiology, and End Results (SEER) analysis25 of more than 1 million patients with breast, prostate, lung, colorectal, liver, pancreatic, ovarian, and esophageal cancers and non–Hodgkin lymphoma diagnosed from 2007 through 2010, uninsured patients or Medicaid recipients were more likely to present with distant disease, less likely to receive cancer-directed surgery and/or radiotherapy, and more likely to die of their disease. Another SEER analysis of 34 437 patients with head and neck cancer26 diagnosed from 2007 through 2010 revealed that uninsured patients were more likely to present with metastatic cancer, not receive definitive treatment, and have higher risk for disease-specific mortality. However, caution has been advised when using the SEER data to analyze insurance status because most patients who were at least 65 years of age and were classified as being uninsured, having private insurance, or unknown insurance status were Medicare eligible, whereas patients diagnosed at younger than 65 years were not.27
Other smaller studies have examined the association of insurance status with head and neck cancer outcomes. In a single-institutional retrospective cohort study15 of 1231 patients with head and neck cancer diagnosed from 1998 to 2007, patients who were uninsured or receiving Medicaid or Medicare had lower OS compared with patients with private insurance. Furthermore, Medicaid recipients and uninsured patients were significantly more likely to present with an advanced stage of disease (odds ratio [OR], 2.94; P < .05) and nodal metastasis (OR, 1.84; P < .05).15 Another single-institutional retrospective study28 of 1698 patients with SCC of the head and neck diagnosed from 1998 through 2011 found that patients receiving Medicaid were more likely to present with locally advanced disease and experience a higher rate of treatment delays. These patients were also noted to have significantly decreased rates of locoregional control and OS compared with non-Medicaid recipients. Similar to these studies, our analysis of patients with SCC of the pharynx revealed that patients with private insurance present at an earlier stage of disease, start definitive treatment earlier, and have better outcomes than do uninsured patients or Medicaid or Medicare recipients.
The proportion of the US minority population is increasing, and these individuals have been shown to have a greater likelihood of being uninsured and thus may be vulnerable to the consequences, including decline in health outcomes.12 Of individuals younger than 65 years, Hispanic patients were 3 times more likely than white patients to be uninsured in 2002, and white and Asian women were more likely to have private insurance coverage than were Hispanic and black women.29 Even among those with greater median household income levels, Hispanic patients were almost 3 times more likely than white patients to be uninsured. Similarly, our analysis of patients with pharyngeal cancer showed that black and Hispanic populations are more likely to be uninsured.
The association of SES with cancer outcomes for various primary disease sites has also been investigated. In our analysis, patients with pharyngeal cancer and higher median household income levels were more likely to have private insurance and significantly higher OS. Of those younger than 65 years, individuals in higher-income households are more likely to have health insurance.30 The Breast, Colon, and Prostate Cancer Data Quality and Patterns of Care Study of the National Program of Cancer Registries31 showed that women with breast cancer who lived in high-SES regions were significantly more likely to receive adjuvant radiotherapy after breast-conserving surgery than were those living in low-SES regions (77% vs 60%; P < .001). Patients with localized colon cancer who lived in high-SES areas were significantly more likely to receive adjuvant chemotherapy (56% vs 50%; P = .02). In addition, men with prostate cancer who lived in high-SES regions were significantly more likely to undergo definitive, cancer-directed treatment than were those from low-SES areas (78% vs 67%; P < .001). The health benefits associated with educational attainment have also been studied and demonstrated to be an important component in terms of access to resources and health care–related characteristics of the community.32 Our investigation also showed that patients with pharyngeal cancer and higher rates of educational attainment were significantly more likely to have private insurance, which was subsequently associated with higher OS. Our results demonstrated that insurance status and higher household income are significantly associated with receipt of earlier definitive treatment, which has been shown to be an independent prognostic factor for improved OS in head and neck cancers.33 These findings may also explain why Medicaid coverage is associated with poorer outcomes compared with private insurance because patients who qualify for Medicaid generally have lower incomes and cannot afford private insurance.34
Possible causes of the association of low SES with poorer outcomes can be attributed to several potential variables, including more advanced disease at presentation, higher burden of significant medical comorbidities, poorer adherence to physician recommendations, and/or lack of social support.10 In Hodgkin lymphoma, low SES (OR, 1.47; P = .003) and being uninsured (OR, 1.76; P < .001) have been associated with more advanced stage disease at presentation,35 and Bradley et al9 found that Medicaid-insured patients with breast cancer were more likely to be diagnosed with a more advanced stage of disease than were those without Medicaid (OR,1.85; P < .05). These findings may be secondary to lower rates of cancer screening, diagnosis, and treatment, all of which have been associated with low SES.36 Patients with low SES are more likely to have lower educational attainment and literacy rates, which may limit patient understanding and ultimately decision making, increasing the likelihood of the patients not proceeding with definitive treatments and subsequently leading to poorer prognosis.37,38 In a California Cancer Registry analysis39 of 11 865 patients with advanced-stage ovarian cancer, patients with low SES were significantly less likely to undergo debulking surgery (OR, 0.71; P < .05) and more likely to not receive chemotherapy (OR, 1.80; P < .05). In a study9 of more than 5000 Medicaid-insured women with breast cancer, patients were more likely to receive no cancer-directed surgery (OR, 1.79; P < .05) and less likely to receive postoperative radiotherapy if a partial mastectomy was performed (OR, 0.49; P < .05). Socioeconomic status has also been shown to be a predictor of adherence to adjuvant therapy in patients with breast cancer, with those from low-SES regions being less likely to adhere to treatment recommendations.40
Risk factors by disease site are known to vary by SES. Lower SES has been found to be associated with a higher risk for nasopharyngeal carcinoma.41,42 Consumption of preserved foods, given that these are among the least expensive foods available, has been found to be a risk factor for malignant disease in lower-SES populations in Asia, whereas occupational exposure to dust and smoke among lower-SES patients has been found to be a risk factor for malignant disease in the United States.41 In a population-based follow-up study42 of 4691 Taiwanese patients with nasopharyngeal carcinoma diagnosed from 2002 to 2006, low SES was associated with fewer health care resources, lower levels of education, lower median household income, and a 2-fold higher risk for mortality compared with with higher SES among those younger than 65 years. No difference in mortality by SES was observed in those 65 years or older. Known risk factors for oropharyngeal and hypopharyngeal cancers, including excessive alcohol consumption, tobacco use, and poor nutrition, have been consistently associated with poorer socioeconomic conditions.43,44 Cancers of the pharynx have been found to be inversely and strongly related to community-level SES, with direct associations between tobacco use and alcohol consumption and cancers of the pharynx.45,46 Human papillomavirus infection is prevalent in oropharyngeal cancers, and its association with community-level SES has been a source of policy development to reduce disparities in cancer prevalence and increase access to adequate medical care in the United States.47
Patients with lower SES are also at risk of being diagnosed with chronic medical conditions that may contribute significantly to their prognosis.48 A study49 of 15 626 cases of malignant neoplasms demonstrated that a higher comorbidity burden was associated with lower SES. Medical comorbidities in patients with breast cancer have been shown to be associated with survival, and those with a higher burden of comorbidities were found to have a significantly higher mortality rate than those with no significant chronic medical conditions.50 Risk factors for malignant disease associated with medical comorbidities, such as smoking, poor nutrition, and occupational hazards, have also been shown to be related to the increased incidence and mortality among those with low SES.51 Our multivariable analysis revealed that the Charlson/Deyo comorbidity score was a significant prognostic factor for OS among patients with pharyngeal cancers, with lower comorbidity scores associated with better outcomes. The aforementioned studies on the association of SES with disease outcomes further highlighted by the findings of our study, suggest the need for interventions targeting socioeconomically disadvantaged populations to help address disparities in health care and outcomes. Socioeconomic background and adaptation of medical services to meet the unique needs of a disadvantaged population need to be taken into consideration when developing practical measures and implementing a framework to address these variables and their association with cancer outcomes.
The NCDB is a standardized hospital-based cancer registry undergoing a series of quality assurance measures and checks while collecting information on 70% of newly diagnosed cancer cases annually, thus decreasing selection bias risks that may be associated with smaller studies.17 However, intrinsic limitations to any large database retrospective analysis must also be considered, with lack of certain data variables possibly leading to a confounding effect of important factors that could not be investigated in our study. Cases from the NCDB are only reported by Commission on Cancer–accredited facilities, thus possibly introducing hospital-selection bias. In addition, Medicaid recipients may include uninsured patients at the time of diagnosis who may enroll in Medicaid during hospitalization, thus introducing crossover between uninsured and insured patients that is not recorded in the NCDB and thus is misclassified in the statistical analysis.52 Patient insurance status may have changed during the follow-up period. In addition, the NCDB does not provide information on community-level employment rates and status. Employment-based health insurance has been and continues to be an important source of coverage for many Americans,53 and SES has been shown to have a significant association with illness and the ability to remain employed.54 Future data sets with employment information would allow for analysis of the association of employment and cancer outcomes after controlling for differences in other socioeconomic indicators, including median household income and insurance status.55 Furthermore, the NCDB does not have a record of preoperative and postoperative imaging, patient adherence to treatment guidelines, disease recurrence, or subsequent salvage therapy. Thus, we cannot evaluate the extent to which these factors may have contributed to patient outcomes. Finally, the NCDB does not collect cancer-specific survival information, which may produce different results from that of all-cause death.
Our study demonstrates that insurance status and household income level are important prognosticators for patients with SCC of the pharynx. The care for patients with pharyngeal cancer in the United States, from diagnosis to treatment and follow-up, is likely to become increasingly dictated by insurers. We found an association of private insurance and higher income with presentation at an earlier stage of disease, an earlier start of primary treatment, and better outcomes compared with no insurance or lower income. Additional investigations are necessary to develop targeted interventions to improve rates of earlier diagnosis and use of timely definitive treatment. For groups with the greatest disparities in outcomes, additional initiatives are warranted to expand health insurance coverage for all patients and address other components of SES, including income and educational levels, as well as the mechanisms by which these may affect the health care system. Increasing evidence of outcome disparities warrants the consideration of a systematic approach to optimize access to standard medical treatments, adherence to physician management recommendations, and thus prognosis in patients at risk.
Corresponding Author: Jacob Y. Shin, MD, Department of Radiation Oncology, Rush University Medical Center, 500 S Paulina St, Chicago, IL 60612 (firstname.lastname@example.org).
Accepted for Publication: April 27, 2017.
Published Online: June 29, 2017. doi:10.1001/jamaoto.2017.0837
Author Contributions: Dr J. Y. Shin had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.
Study concept and design: J. Y. Shin, Yoon, Blumenfeld, Mai, Diaz.
Acquisition, analysis, or interpretation of data: J. Y. Shin, Yoon, A. K. Shin, Blumenfeld, Diaz.
Drafting of the manuscript: J. Y. Shin, Yoon, Blumenfeld, Mai, Diaz.
Critical revision of the manuscript for important intellectual content: J. Y. Shin, Yoon, A. K. Shin, Blumenfeld, Diaz.
Statistical analysis: J. Y. Shin, Yoon, A. K. Shin.
Administrative, technical, or material support: J. Y. Shin, Yoon, A. K. Shin.
Study supervision: J. Y. Shin, Blumenfeld, Diaz.
Conflict of Interest Disclosures: All authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest and none were reported.
Disclaimer: The American College of Surgeons and the Commission on Cancer have not verified and are not responsible for the analytic or statistical methods employed or the conclusions drawn from these data by the investigators.
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