Medicare/Medicaid Insurance, Rurality, and Black Race Associated With Provision of Hepatocellular Carcinoma Treatment and Survival

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  • 1 Division of Gastroenterology and Hepatology, Department of Medicine, and
  • 2 Division of Hematology/Oncology, Department of Medicine;
  • 3 Lineberger Comprehensive Cancer Center;
  • 4 Center for Pharmacoepidemiology, Department of Epidemiology; and
  • 5 Division of Surgical Oncology, Department of Surgery, University of North Carolina, Chapel Hill, North Carolina.

Background: Early treatment of hepatocellular carcinoma (HCC) is associated with improved survival, but many patients with HCC do not receive therapy. We aimed to examine factors associated with HCC treatment and survival among incident patients with HCC in a statewide cancer registry. Materials and Methods: All patients with HCC from 2003 through 2013 were identified in the North Carolina cancer registry. These patients were linked to insurance claims from Medicare, Medicaid, and large private insurers in North Carolina. Associations between prespecified covariates and more advanced HCC stage at diagnosis (ie, multifocal cancer), care at a liver transplant center, and provision of HCC treatment were examined using multivariate logistic regression. A Cox proportional hazards model was developed to assess the association between these factors and survival. Results: Of 1,809 patients with HCC, 53% were seen at a transplant center <90 days from diagnosis, with lower odds among those who were Black (adjusted odds ratio [aOR], 0.54; 95% CI, 0.39–0.74), had Medicare insurance (aOR, 0.35; 95% CI, 0.21–0.59), had Medicaid insurance (aOR, 0.46; 95% CI, 0.28–0.77), and lived in a rural area; odds of transplant center visits were higher among those who had prediagnosis alpha fetoprotein screening (aOR, 1.74; 95% CI, 1.35–2.23) and PCP and gastroenterology care (aOR, 1.66; 95% CI, 1.27–2.18). Treatment was more likely among patients who had prediagnosis gastroenterology care (aOR, 1.68; 95% CI, 0.98–2.86) and transplant center visits (aOR, 2.42; 95% CI, 1.74–3.36). Survival was strongly associated with age, cancer stage, cirrhosis complications, and receipt of HCC treatment. Individuals with Medicare (adjusted hazard ratio [aHR], 1.58; 95% CI, 1.20–2.09) and Medicaid insurance (aHR, 1.55; 95% CI, 1.17–2.05) had shorter survival than those with private insurance. Conclusions: In this population-based cohort of patients with HCC, Medicare/Medicaid insurance, rural residence, and Black race were associated with lower provision of HCC treatment and poorer survival. Efforts should be made to improve access to care for these vulnerable populations.

Background

Hepatocellular carcinoma (HCC) incidence and mortality are increasing in the United States.1,2 The prognosis for HCC is poor, in part because potentially curative treatments, including surgical resection, ablation, and transplantation, are feasible in just a minority of patients with early-stage HCC.3 In the absence of curative therapy, liver-directed locoregional therapies and drug therapy prolong survival, yet up to half of all patients with HCC never receive any cancer-directed therapy.47

Despite accumulating evidence that the provision of timely HCC treatment decreases cancer-related mortality,8 treatment rates remain low and the reasons for nonreceipt of therapy in patients with HCC remain unclear. Medical comorbidities, decompensated liver disease, and advanced HCC often preclude specific HCC-directed therapies. Other potential factors have been associated with the low provision of HCC therapy, including older patient age, insurance status, and care at a low-volume center.911 In addition, racial and ethnic disparities in the receipt of HCC treatment and survival have been well-documented.1216 Finally, subspecialist consultation has been associated with improved treatment outcomes in the US Department of Veterans Affairs system.17 This evidence suggests that both patient- and facility-level factors likely influence the provision of HCC treatment. However, relatively few data sources allow for the simultaneous investigation of these many potential variables in a population-based sample.

We therefore assessed the potential predictors of advanced cancer, care at a transplant center, provision of treatment, and mortality among patients from a population-based state registry linked to insurance claims data.

Materials and Methods

This work was approved by the Biomedical Institutional Review Board at the University of North Carolina (#12-1828).

Patients

The cohort comprised patients diagnosed with HCC in 2003 through 2013, identified from the North Carolina Central Cancer Registry (NCCCR) by ICD-10 code C22.0 and ICD-O-3 histology codes 8170–8175 and 8180. These patients were linked to insurance claims from Medicare, Medicaid, and large private insurance providers in North Carolina by the UNC Lineberger Cancer Information & Population Health Resource.18 This subset consisted of patients with continuous healthcare enrollment in any health plan for 12 months preceding and 12 months after diagnosis (or death). Patients participating in a Medicare HMO/Advantage plan were excluded because claims are not required to be reported to Medicare.

To evaluate factors associated with treatment and survival, only patients surviving the 90-day exposure window after diagnosis were included in multivariable models, thereby including only patients who may have been eligible for treatment.

Covariates

Patient age, sex, marital status, race, county and zip code of residence, and insurance status at diagnosis were derived from the NCCCR demographics file. We used the NCCCR collaborative staging extension variables of number of tumors and presence/absence of vascular invasion to group cancers into clinically meaningful categories (ie, single or multiple, with or without vascular invasion, and extrahepatic disease). Multifocal cancer was defined as the presence of multiple intrahepatic tumors with or without vascular spread, extrahepatic spread, or unstaged HCC. As has been done in previous studies of HCC outcomes using claims data,5 unstaged HCC was considered together with extrahepatic spread given the similar outcomes among these groups. These categories are similar to the tumor extent component of the Barcelona Clinic Liver Cancer staging system and approximate patients who may qualify for liver transplantation, surgical resection, or locoregional therapies.19,20

County-level economic and healthcare covariates were taken from the Area Health Resources File21 and the North Carolina Health Professions Data System (https://nchealthworkforce.unc.edu/). Measures were selected to cover domains used in other composite measures of census tract–based socioeconomic status.2224 Given the large number of covariates measured across 100 North Carolina counties, we used factor analysis to create representative indices. Factor analysis was conducted separately for health system factors that together had an average variance extracted of 58% across counties and for economic factors (see supplemental eTable 1, available with this article at JNCCN.org). For economic variables, 2 factors combined for an average variance extracted of 83.2% across counties. The first factor was described as an economic disadvantage index because it was dominated by median home value, percentage of White patients, and unemployment rate. The second was described as the rurality index because it was dominated by level of rurality and percentage of agricultural/forestry/hunting/mining industries. For each index, the lowest quartile described the least disadvantaged patients according to these measures.

Additional patient-level covariates were determined from ICD-9 claims in the 12 months prediagnosis, including nonliver comorbidity using the Klaubunde modification of the Charlson-Deyo comorbidity index (excluding liver disease),25 psychiatric comorbidity not including substance abuse (eg, depression, anxiety, bipolar disorder, schizophrenia, posttraumatic stress disorder), liver-related complications (eg, encephalopathy, ascites, varices, hepatorenal syndrome),26 and underlying cause of liver disease. Because many patients had low healthcare utilization in the year before diagnosis, codes for the cause of liver disease were evaluated from 12 months before diagnosis to 1 month after diagnosis.

Prediagnosis healthcare utilization was determined by visits with a primary care provider or gastroenterology/hepatology provider in the year before diagnosis (excluding 2 months prediagnosis, when consultations may reflect referrals for cancer), prediagnosis alpha fetoprotein (AFP) screening27 (American Association for the Study of Liver Diseases guidelines recommended every 6 months during this era for patients with cirrhosis and hepatitis virus),28 and number of unique contacts with the healthcare system (inpatient or outpatient visits). Consultation with HCC-specific subspecialty clinicians and at a liver transplant center was measured in the 90 days after diagnosis. Distance from each patient’s zip code to the closest liver transplant center was calculated. Treatment was defined as the initial treatment received as described in earlier research,5 acknowledging that many patients go on to receive multiple therapies.

Analysis

We extracted patient- and county-level factors for all patients with HCC and linked claims data, and performed univariate analyses on demographic characteristics, insurance status, socioeconomic status, rurality, medical/psychiatric comorbidities, liver disease etiology and complications, and cancer stage at diagnosis, calculating the median and interquartile range (IQR) for continuous variables and proportions for categorical variables. We calculated annual rates for subspecialty consultation within 90 days of HCC diagnosis and provision of HCC treatments. Multivariable logistic regression analysis was used to assess the variables associated with multifocal cancer at diagnosis, transplant center visits, and provision of HCC treatments. Finally, we developed a Cox proportional hazards model to assess variables associated with overall survival. All statistical analyses were performed with SAS 9.4 (SAS Institute Inc).

Results

Cohort Description

Our cohort included 1,809 patients with HCC (supplemental eFigure 1 and eTable 2). Most patients had single (37%) or multiple (25%) tumors without vascular invasion or extrahepatic spread. A smaller proportion had vascular spread at diagnosis, including 6% and 13% of those with single and multiple lesions, respectively. Median age was 68 years (IQR, 59–76 years) and patients were predominantly male (73%), White (76%), and had Medicare insurance (59%).

Multifocal HCC at Diagnosis

A total of 1,033 patients (57%) had multifocal HCC at presentation. Multifocal cancer at presentation was significantly associated with age, marital status, and sex. Receipt of prediagnosis AFP screening (adjusted odds ratio [aOR], 0.72; 95% CI, 0.58–0.90) and PCP and gastroenterology/hepatology care (aOR, 0.77; 95% CI, 0.61–0.96) was associated with decreased odds of multifocal disease (Table 2).

Visits to a Liver Transplant Center

In the 90 days after diagnosis, 957 (53%) of patients were seen at a liver transplant center for any reason (Figure 1 and eTable 3). A transplant center visit was significantly less likely among patients who were older (age ≥75 vs <50 years: aOR, 0.52; 95% CI, 0.28–0.94), Black (vs White: aOR, 0.54; 95% CI, 0.39–0.74), insured by Medicare (vs private insurance: aOR, 0.35; 95% CI, 0.21–0.59), and insured by Medicaid/dual (vs private insurance: aOR, 0.46; 95% CI, 0.28–0.77).

Figure 1.
Figure 1.

Time trends of subspecialty consultation within 90 days of diagnosis among incident patients with HCC diagnosed between 2004 and 2012.

Abbreviations: GE, gastroenterology; HCC, hepatocellular carcinoma; Hem/Onc, hematology/oncology.

Citation: Journal of the National Comprehensive Cancer Network J Natl Compr Canc Netw 2021; 10.6004/jnccn.2020.7616

Patients residing a median of 53 miles (aOR, 0.46; 95% CI, 0.32–0.66) and 106 miles (aOR, 0.27; 95% CI, 0.18–0.41) from the closest transplant center were less likely to have visited a transplant center than those living in the closest tertile (median, 17.4 miles). Transplant center visits were also less likely among those living in the most rural counties (vs least rural: aOR, 0.24; 95% CI, 0.14–0.47). Prediagnosis healthcare was also a major determinant of transplant center visit, with increased odds among patients with more prediagnosis healthcare utilization (highest vs lowest tertile: aOR, 2.14; 95% CI, 1.57–2.93), AFP screening (aOR, 1.74; 95% CI, 1.35–2.23), and gastroenterology/hepatology care (aOR, 1.66; 95% CI, 1.27–2.18).

Provision of HCC Treatment

Of the 1,809 patients with HCC, 30% died within the 90-day treatment exposure window after diagnosis and were excluded from treatment and survival analyses. These patients were older (ie, more likely to be aged ≥75 years), had greater comorbidity, had more advanced cancer, were more likely to be divorced, and were less likely to have received prediagnosis care. They were significantly less likely to be seen at a transplant center or to have received treatment for their HCC.

In the 1,250 patients surviving the 90-day treatment exposure window, 857 (69%) were treated (Table 1). The types of treatments used over time can be seen in Figure 2. Of these patients, 478 (56%) had a surgical consultation, 425 (50%) had a gastroenterology/hepatology consultation, and 469 (55%) saw a hematologist/oncologist; these rates slowly increased from 2003 to 2013 (Figure 1).

Table 1.

Factors Associated With Treatment Among Patients Surviving 90 Days From Diagnosis (N=1,250)

Table 1.
Figure 2.
Figure 2.

Time trends of type of initial treatment received by year of diagnosis among incident patients with HCC diagnosed between 2004 and 2012. Most patients diagnosed with HCC received no treatment every year during the study period.

Abbreviations: HCC, hepatocellular carcinoma; TACE, transarterial chemoembolization; Y90, yttrium-90.

Citation: Journal of the National Comprehensive Cancer Network J Natl Compr Canc Netw 2021; 10.6004/jnccn.2020.7616

Factors most strongly associated with receipt of HCC treatment included prediagnosis AFP screening (aOR, 2.61; 95% CI, 1.90–3.60), surgical consultation (aOR, 3.40; 95% CI, 2.48–4.67), and visit to a liver transplant center (aOR, 2.42; 95% CI, 1.74–3.36) (Table 1). In contrast, advanced age (65–74 or ≥75 years), unmarried status, psychiatric comorbidity, and liver-related complications all significantly reduced the odds of receiving HCC treatment.

Overall Survival

Across the study period, survival increased from a median of 6 months (IQR, 2–21) in 2004 through 2006 to 8 months (IQR, 2–28) in 2010 through 2012. In adjusted models accounting for disease severity and treatment, patients diagnosed in 2008 and beyond had significantly better survival than those diagnosed in 2004 through 2007 (adjusted hazard ratio [aHR] for death, 0.75; 95% CI, 0.66–0.85).

In addition to year of diagnosis, cancer stage and receipt of cancer treatment were strongly associated with survival. Compared with the 12% of patients who underwent curative surgery, risk of death was higher among those treated with ablation (aHR, 1.60; 95% CI, 1.20–2.13) and locoregional therapy (aHR, 2.47; 95% CI, 1.90–3.19). Patients treated with drug therapy (aHR, 4.57; 95% CI, 3.27–6.40) or radiation (aHR, 3.79; 95% CI, 2.55–5.65) and those who were untreated (aHR, 4.97; 95% CI, 3.79–6.51) had a higher risk of mortality, although these results were not adjusted for factors that may influence treatment selection (eg, bilirubin level) (Table 2).

Table 2.

Factors Associated With Survival Among Patients Surviving 90 Days From Diagnosis (N=1,250)

Table 2.

Survival was better among younger patients (aged <55 years) and those without comorbidities. Receipt of prediagnosis gastroenterology/hepatology care was associated with improved survival compared with patients who saw neither a primary care nor a gastroenterology/hepatology physician in the year before diagnosis (aHR, 0.74; 95% CI, 0.58–0.94). Despite adjusting for age and treatment received, patients with Medicare (aHR, 1.58; 95% CI, 1.20–2.09) and Medicaid/dual (aHR, 1.55; 95% CI, 1.17–2.05) had significantly worse survival than those with private insurance (Table 2).

Discussion

In this population-based retrospective cohort study examining the effects of patient characteristics, county-level resources, and healthcare utilization on HCC outcomes, we found patient-level sociodemographic factors (age >65 years, Black race, unmarried status, type of insurance) to be key determinants of stage at diagnosis and survival after an HCC diagnosis. These same patient factors were associated with liver transplant center visits and cancer-directed treatment. When further analyzing the root causes, we found that survival was most strongly associated with receipt of cancer-directed treatment. Treatment in turn was more likely in patients with prediagnosis gastroenterology/hepatology specialty care and AFP screening and with postdiagnosis liver transplant center visits, which are likely a surrogate for receipt of multidisciplinary care. The disparities in outcomes were therefore largely accounted for by lower-quality healthcare before and after an HCC diagnosis. In all analyses, Medicaid and Medicare beneficiaries experienced significantly inferior outcomes, including a marked reduction in survival, compared with patients who were privately insured.

Given that HCC incidence is higher among racial and ethnic minorities and in socioeconomically disadvantaged regions,29,30 we hypothesized that a lack of access to local healthcare resources and greater socioeconomic status disadvantage are key contributing factors to the low rates of treatment and the disparities in care that have been previously reported. After investigating a wide array of county-level determinants of economic health and healthcare availability, we found that the only clear associations between county factors and quality of HCC care were that patients residing in the most rural counties and counties farthest from a transplant center were least likely to be seen at a transplant center in the 90 days after diagnosis. No other county-level factors clearly influenced treatment or survival among patients with HCC.

Health insurance was strongly associated with the likelihood of transplant center visits and survival. The association between Medicare insurance and these outcomes could be confounded by age, given that Medicare beneficiaries are usually aged >65 years and some patients may be ineligible for liver transplantation based on advanced age. However, recent data suggest that an increased proportion of patients with HCC aged >65 years are being listed for transplantation,31 and the negative associations between Medicare insurance and transplant center visits and survival persisted in multivariable models adjusting for age. Patients with Medicare and Medicaid had a 24% and 57% increased risk of death, respectively, compared with those with private insurance; this risk was 67% higher for those who were uninsured. The effect of insurance status on survival did not diminish after adjusting for patient age, comorbidity, and treatment, with a 58% and 55% increase in risk of death for patients with Medicare and Medicaid, respectively. The influence of public insurance on outcomes could reflect limitations imposed by Medicare and Medicaid on access to care; however, public insurance in this analysis is also likely a proxy for individual socioeconomic resources, given that income limits for North Carolina Medicaid are strict.32 Regardless of county resources, individuals with Medicare or Medicaid likely face additional financial challenges that could compromise access compared with their privately insured counterparts. The marked and persistently inferior outcomes among patients who were single, divorced/separated, or widowed (ie, advanced stage at presentation, less consultative care and treatment) and those with psychiatric comorbidity (ie, lower rates of treatment and inferior survival) also speak to the importance of individual resources (eg, social support) on the ability of patients with HCC to receive the care they need.

This study is strengthened by its large population-based sample and the availability of linked insurance claims, allowing for the simultaneous exploration of patient, treatment, and facility factors on outcomes. However, this study must be interpreted in the context of potential limitations. First, the survival analysis was limited to patients who survived the 90-day treatment exposure window after diagnosis. Although this restriction was necessary to evaluate the effect of treatment on survival, omitting these sickest patients may have obscured the effect of county economic and healthcare factors on HCC outcomes. Although we generally found that the same factors that were associated with treatment were associated with early mortality (ie, age >65 years and cancer stage, greater comorbidity, single/divorced/separated status, Medicare/Medicaid insurance, less prediagnostic care), a potentially meaningful difference was that patients with early mortality were more likely to live in a county with fewer healthcare services and lower density of gastroenterology/hepatology physicians. Second, the data source did not allow for adjustment for liver disease severity via the Model for End-Stage Liver Disease or Child-Pugh score, although we did account for prediagnosis liver-related complications. Finally, our data source did not allow us to assess for factors that could have contributed to improved survival over time, including improved treatments for underlying liver disease (eg, direct-acting antiviral therapy for hepatitis C virus), expanded access to HCC therapies and clinical trials, and broader adoption of multidisciplinary tumor boards and clinics.

Conclusions

Our findings that an individual’s use of the healthcare system before diagnosis and visits to an expert center early during the cancer course are major driving forces behind treatment and survival for HCC are critical when considering how to improve outcomes of patients with HCC—both in North Carolina and across the nation. To reduce the rates of very early mortality from HCC, public health efforts must focus on detection of cirrhosis and gastroenterology/hepatology referrals for affected individuals. To improve survival among patients who present earlier in their disease course, efforts must focus on increasing access to subspecialty care and treatment. Our ongoing work will examine patient-reported barriers to accessing care after an HCC diagnosis, with a focus on high-risk Black and rural residents and Medicare and Medicaid beneficiaries.

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If the inline PDF is not rendering correctly, you can download the PDF file here.

Submitted February 4, 2020; accepted for publication July 1, 2020.

Author contributions: Study concept and design: Sanoff, Chang, Lund, Barritt, Hayashi, Stitzenberg. Data interpretation: All authors. Statistical analysis: Chang. Drafting of manuscript: Sanoff. Critical revision: All authors.

Disclosures: Dr. Sanoff has disclosed that she has received grant/research support from Bayer. Dr. Lund has disclosed that her spouse is employed by GlaxoSmithKline. Dr. Barritt has disclosed that he has received grant/research support from Intercept Pharmaceuticals, Genfit Pharmaceuticals, Bristol-Myers Squibb, NuSirt, and Target Pharmasolutions. The remaining authors have disclosed that they have not received any financial consideration from any person or organization to support the preparation, analysis, results, or discussion of this article.

Funding: Research reported in this article was supported by the NCI of the NIH under award number K07CA160722 (H.K.S.) and by the NIH under award number T32 DK007634 (A.M.M.). The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH. Additional support was provided by the Cancer Information & Population Health Resource, UNC Lineberger Comprehensive Cancer Center, with funding provided by the University Cancer Research Fund via the State of North Carolina.

Correspondence: Hanna K. Sanoff, MD, MPH, University of North Carolina, Division of Hematology/Oncology, Department of Medicine, 170 Manning Drive, CB 7305, Chapel Hill, NC 27599. Email: hanna_sanoff@med.unc.edu

Supplementary Materials

  • View in gallery

    Time trends of subspecialty consultation within 90 days of diagnosis among incident patients with HCC diagnosed between 2004 and 2012.

    Abbreviations: GE, gastroenterology; HCC, hepatocellular carcinoma; Hem/Onc, hematology/oncology.

  • View in gallery

    Time trends of type of initial treatment received by year of diagnosis among incident patients with HCC diagnosed between 2004 and 2012. Most patients diagnosed with HCC received no treatment every year during the study period.

    Abbreviations: HCC, hepatocellular carcinoma; TACE, transarterial chemoembolization; Y90, yttrium-90.

  • 1.

    White DL, Thrift AP, Kanwal F, . Incidence of hepatocellular carcinoma in all 50 United States, from 2000 through 2012. Gastroenterology 2017;152:812820.e5.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2.

    Petrick JL, Kelly SP, Altekruse SF, . Future of hepatocellular carcinoma incidence in the United States forecast through 2030. J Clin Oncol 2016;34:17871794.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    Kohler BA, Sherman RL, Howlader N, . Annual report to the nation on the status of cancer, 1975-2011, featuring incidence of breast cancer subtypes by race/ethnicity, poverty, and state. J Natl Cancer Inst 2015;107:djv048.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4.

    El-Serag HB, Siegel AB, Davila JA, . Treatment and outcomes of treating of hepatocellular carcinoma among Medicare recipients in the United States: a population-based study. J Hepatol 2006;44:158166.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Sanoff HK, Chang Y, Stavas JM, . Effectiveness of initial transarterial chemoembolization for hepatocellular carcinoma among Medicare beneficiaries. J Natl Compr Canc Netw 2015;13:11021110.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Davila JA, Kramer JR, Duan Z, . Referral and receipt of treatment for hepatocellular carcinoma in United States veterans: effect of patient and nonpatient factors. Hepatology 2013;57:18581868.

    • Crossref
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