Abstract
Background
Racial/ethnic disparities in prognosis have been reported in patients with hepatocellular carcinoma (HCC); however, few studies have evaluated racial/ethnic disparities in the context of insurance status.
Aims
Characterize racial/ethnic and insurance status in early tumor detection, receipt of curative therapy and overall survival in a multicenter diverse cohort of HCC patients from the USA.
Study
We included patients with HCC diagnosed between June 2012 and May 2013 at four centers in the USA. Generalized linear mixed effects models were used to compare early tumor detection (defined using Milan Criteria) and curative treatment receipt (liver transplantation, surgical resection, or local ablation) as a function of patient race/ethnicity and insurance status. A multivariable frailty survival model was used to compare risk of death between patient groups.
Results
Of 379 HCC patients (52.8% non-Hispanic White, 19.5% Hispanic White, 19.8% Black), 46.4% and 48.0% were found at an early stage and underwent curative therapy, respectively, and median overall survival of the cohort was 25.7 months. Early detection of HCC was associated with gastroenterology subspecialty care and receipt of HCC surveillance but not race/ethnicity or insurance status in adjusted models. However, commercial insurance was significantly associated with higher odds of curative treatment receipt, which in turn was the strongest correlate for overall survival. After adjusting for health system and insurance status, race/ethnicity was not associated with curative treatment receipt or overall survival.
Conclusions
Insurance status and access to gastroenterology subspecialty care may be important drivers of racial/ethnic disparities in prognosis among HCC patients.
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References
Petrick JL, Kelly SP, Altekruse SF, et al. Future of hepatocellular carcinoma incidence in the United States forecast through 2030. J Clin Oncol. 2016;34:1787–1794.
White DL, Thrift AP, Kanwal F, et al. Incidence of hepatocellular carcinoma in all 50 United States, from 2000 through 2012. Gastroenterology. 2017;152:812–820.e5.
Ulahannan SV, Duffy AG, McNeel TS, et al. Earlier presentation and application of curative treatments in hepatocellular carcinoma. Hepatology. 2014;60:1637–1644.
Tapper EB, Parikh ND. Mortality due to cirrhosis and liver cancer in the United States, 1999–2016: observational study. BMJ. 2018;. https://doi.org/10.1136/bmj.k2817.
Shebl FM, Capo-Ramos DE, Graubard BI, et al. Socioeconomic status and hepatocellular carcinoma in the United States. Cancer Epidemiol Biomarkers Prev. 2012;21:1330–1335.
Artinyan A, Mailey B, Sanchez-Luege N, et al. Race, ethnicity, and socioeconomic status influence the survival of patients with hepatocellular carcinoma in the United States. Cancer. 2010;116:1367–1377.
Mathur AK, Osborne NH, Lynch RJ, et al. Racial/ethnic disparities in access to care and survival for patients with early-stage hepatocellular carcinoma. Arch Surg. 2010;145:1158–1163.
Ge D, Fellay J, Thompson AJ, et al. Genetic variation in IL28B predicts hepatitis C treatment-induced viral clearance. Nature. 2009;461:399–401.
Singal AG, Yopp A, Skinner CS, et al. Utilization of hepatocellular carcinoma surveillance among American patients: a systematic review. J Gen Intern Med. 2012;27:861–867.
Njei B, Rotman Y, Ditah I, et al. Emerging trends in hepatocellular carcinoma incidence and mortality. Hepatology. 2015;61:191–199.
Singal AG, Li X, Tiro J, et al. Racial, social, and clinical determinants of hepatocellular carcinoma surveillance. Am J Med. 2015. https://doi.org/10.1016/j.amjmed.2014.07.027.
Zaydfudim V, Whiteside MA, Griffin MR, et al. Health insurance status affects staging and influences treatment strategies in patients with hepatocellular carcinoma. Ann Surg Oncol. 2010;17:3104–3111.
Siegel AB, McBride RB, El-Serag HB, et al. Racial disparities in utilization of liver transplantation for hepatocellular carcinoma in the United States, 1998–2002. Am J Gastroenterol. 2008;103:120–127.
Xu L, Kim Y, Spolverato G, et al. Racial disparities in treatment and survival of patients with hepatocellular carcinoma in the United States. Hepatobiliary Surg Nutr. 2016;5:43–52.
Sonnenday CJ, Dimick JB, Schulick RD, et al. Racial and geographic disparities in the utilization of surgical therapy for hepatocellular carcinoma. J Gastrointest Surg. 2007;11:1636–1646. (discussion 1646).
Serper M, Taddei TH, Mehta R, et al. Association of provider specialty and multidisciplinary care with hepatocellular carcinoma treatment and mortality. Gastroenterology. 2017;152:1954–1964.
Taplin SH, Anhang Price R, Edwards HM, et al. Introduction: understanding and influencing multilevel factors across the cancer care continuum. J Natl Cancer Inst Monogr. 2012;2012:2–10.
Singal AG, Mittal S, Yerokun OA, et al. Hepatocellular carcinoma screening associated with early tumor detection and improved survival among patients with cirrhosis in the US. Am J Med. 2017;130:1099–1106.e1.
Parikh ND, Scaglione S, Li Y, et al. A comparison of staging systems for hepatocellular carcinoma in a multicenter US cohort. Clin Gastroenterol Hepatol. 2018;16:781–782.
Heimbach JK, Kulik LM, Finn RS, et al. AASLD guidelines for the treatment of hepatocellular carcinoma. Hepatology. 2018;67:358–380.
Kenward MG, Roger JH. Small sample inference for fixed effects from restricted maximum likelihood. Biometrics. 1997;53:983–997.
Lin DY, Wei L, Ying Z. Checking the Cox model with cumulative sums of martingale-based residuals. BioMetrika. 1993;80:557–572.
Ha J, Yan M, Aguilar M, et al. Race/ethnicity-specific disparities in hepatocellular carcinoma stage at diagnosis and its impact on receipt of curative therapies. J Clin Gastroenterol. 2016;50:423–430.
Rich NE, Hester C, Odewole M, et al. Racial and ethnic differences in presentation and outcomes of hepatocellular carcinoma. Clin Gastroenterol Hepatol. 2018;16:198–210.
Tan D, Yopp A, Beg MS, et al. Meta-analysis: underutilisation and disparities of treatment among patients with hepatocellular carcinoma in the United States. Aliment Pharmacol Ther. 2013;38:703–712.
Dalton-Fitzgerald E, Tiro J, Kandunoori P, et al. Practice patterns and attitudes of primary care providers and barriers to surveillance of hepatocellular carcinoma in patients with cirrhosis. Clin Gastroenterol Hepatol. 2015;13:791–798.e1.
Singal AG, El-Serag HB. Hepatocellular carcinoma from epidemiology to prevention: translating knowledge into practice. Clin Gastroenterol Hepatol. 2015;13:2140–2151.
Sommers BD, Gawande AA, Baicker K. Health insurance coverage and health—what the recent evidence tells us. N Engl J Med. 2017;377:586–893.
Baicker K, Taubman SL, Allen HL, et al. The Oregon experiment—effects of Medicaid on clinical outcomes. N Engl J Med. 2013;368:1713–1722.
Wherry LR, Miller S. Early coverage, access, utilization, and health effects associated with the affordable care act medicaid expansions: a quasi-experimental study. Ann Intern Med. 2016;164:795–803.
Davila JA, Morgan RO, Richardson PA, et al. Use of surveillance for hepatocellular carcinoma among patients with cirrhosis in the United States. Hepatology. 2010;52:132–141.
Simmons OL, Feng Y, Parikh ND, et al. Primary care provider practice patterns and barriers to hepatocellular carcinoma surveillance. Clin Gastroenterol Hepatol. 2019;17:766–773.
Mokdad AA, Murphy CC, Pruitt SL, et al. Effect of hospital safety net designation on treatment use and survival in hepatocellular carcinoma. Cancer. 2018;124:743–751.
Su GL, Glass L, Tapper EB, et al. Virtual consultations through the veterans administration SCAN-ECHO project improves survival for veterans with liver disease. Hepatology. 2018;68:2317–2324.
Singal AG, Tiro JA, Marrero JA, et al. Mailed outreach program increases ultrasound screening of patients with cirrhosis for hepatocellular carcinoma. Gastroenterology. 2017;152:608–615.e4.
Shavers VL. Measurement of socioeconomic status in health disparities research. J Natl Med Assoc. 2007;99:1013–1023.
Funding
Dr. Singal was supported in part by NIH RO1 MD12565. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institute of Health.
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SS was involved in study concept and design, acquisition of data, analysis and interpretation of data, drafting of the manuscript, critical revision of manuscript for important intellectual content, and study supervision. He is the guarantor of the article. WA was involved in data analysis and interpretation of data, drafting of the manuscript, and critical revision of the manuscript for important intellectual content. AC was involved in study concept and design, acquisition of data, and critical revision of manuscript for important intellectual content. PD was involved in acquisition of data and critical revision of manuscript for important intellectual content. SM was involved in study concept and design, acquisition of data, interpretation of data, critical revision of manuscript for important intellectual content, and study supervision. AS was involved in study concept and design, acquisition of data, analysis and interpretation of data, critical revision of manuscript for important intellectual content, and study supervision. NP was involved in study concept and design, acquisition of data, analysis and interpretation of data, critical revision of manuscript for important intellectual content, and study supervision.
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Scaglione, S., Adams, W., Caines, A. et al. Association Between Race/Ethnicity and Insurance Status with Outcomes in Patients with Hepatocellular Carcinoma. Dig Dis Sci 65, 1669–1678 (2020). https://doi.org/10.1007/s10620-019-05890-2
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DOI: https://doi.org/10.1007/s10620-019-05890-2