Implementation of Universal Hepatitis C Virus Screening in a Tertiary Cancer Center

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Harrys A. Torres Department of Infectious Diseases, Infection Control and Employee Health, The University of Texas MD Anderson Cancer Center, Houston, TX
Department of Gastroenterology, Hepatology and Nutrition, The University of Texas MD Anderson Cancer Center, Houston, TX

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Khalis Mustafayev Department of Infectious Diseases, Infection Control and Employee Health, The University of Texas MD Anderson Cancer Center, Houston, TX

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Ruston P. Juneau Information Services–Liaison Program, Epic Boost, Epic, Verona, WI

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Jessica P. Hwang Department of General Internal Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX

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Lan Sun Wang Department of Gastroenterology, Hepatology and Nutrition, The University of Texas MD Anderson Cancer Center, Houston, TX

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Georgios Angelidakis Department of Infectious Diseases, Infection Control and Employee Health, The University of Texas MD Anderson Cancer Center, Houston, TX

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Ernest Hawk Division of Cancer Prevention and Population Sciences, The University of Texas MD Anderson Cancer Center, Houston, TX

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Bruno P. Granwehr Department of Infectious Diseases, Infection Control and Employee Health, The University of Texas MD Anderson Cancer Center, Houston, TX

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Eduardo Yepez Guevara Department of Infectious Diseases, Infection Control and Employee Health, The University of Texas MD Anderson Cancer Center, Houston, TX

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Anita K. Ying Department of Endocrine Neoplasia and Hormonal Disorders, The University of Texas MD Anderson Cancer Center, Houston, TX

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Background: The prevalence of chronic hepatitis C virus (HCV) infection in the United States is ≤1%. Universal HCV screening is recommended nationwide. Here we describe our experience implementing universal HCV screening at a cancer center. Methods: In October 2016, universal HCV screening with HCV antibody (anti-HCV) was initiated for all new outpatients. Universal screening was promoted through widespread provider education, orders in the Epic electronic health records (EHRs), SmartSets, and automated EHR reminders. The effort focused on patients with solid tumors, because universal screening in patients with hematologic malignancies was already standard practice. Primary outcomes were the proportion of patients screened and the proportion of patients with reactive anti-HCV test results linked to HCV care. The secondary outcome was the incidence of HCV-associated hepatocellular carcinoma as a second primary malignancy (HCC-SPM) in patients with a history of other cancers before HCC diagnosis. Epic’s Reporting Workbench Business Intelligence tools were used. Statistical significance was defined as P<.05 on chi-square analysis. Results: From April 2016 through April 2023, 56,075 patients with solid tumors were screened for HCV, of whom 1,300 (2.3%) had reactive anti-HCV test results. The proportion of patients screened was 10.1% in the 6 months before study implementation and 34.4% in the last 6 months of the study (P<.001). HCV screening was ordered using SmartSets in 39,332 (45.8%) patients and in response to automated EHR reminders in 10,972 (12.8%) patients. Most patients with reactive anti-HCV test results were linked to care (765/1,300; 59%), most with proven HCV infection were treated (425/562; 76%), and most treated patients achieved sustained virologic response (414/425; 97%). The incidence of HCC-SPMs was 15% in historical controls treated from 2011 to 2017 and 5.7% following implementation of universal screening (P=.0002). Conclusions: Universal HCV screening can be successfully implemented in cancer hospitals using an EHR-based multipronged approach to eliminate HCV and prevent HCV-associated HCC-SPMs.

Background

Globally, 58 million people are chronically infected with hepatitis C virus (HCV), including an estimated 2.4 million people in the United States alone.13 However, approximately 80% of the people infected with HCV worldwide3 and 40% of those infected with HCV in the United States are unaware of their infection.4 In 2016, the WHO adopted the first global hepatitis plan, which called for the elimination of viral hepatitis as a public health threat by 2030 and established targets for countries to meet in order to achieve that goal.5 A total of 76 countries, including the United States, are not on track to meet the HCV elimination targets by 2050.3 To achieve global HCV elimination targets, multiple interventions must be implemented to increase population engagement along the HCV care cascade.6 Therefore, the US federal government has proposed a National Hepatitis C Elimination Program to eliminate HCV infection nationwide.7,8

In the general US population, the prevalence of chronic HCV infection is ≤1%.2 According to data from the Centers for Disease Control and Prevention, the rate of reported cases of acute HCV infection in the general US population increased by 400% between 2010 and 2020, likely related to the opioid epidemic.9 Because of the natural history of HCV infection, most cases of acute HCV infection will progress to chronic infection if untreated.10

The reported prevalence of chronic HCV infection among patients with cancer in US cancer centers ranges from 1.5% to 2.4%, but these prevalences may be inaccurate due to the lack of routine HCV screening in many cancer centers.1113 Chronic HCV infection causes virologic, hepatic, and oncologic concerns in patients with cancer.10 Our group has demonstrated the development of HCV-associated hepatocellular carcinoma (HCC) as a second primary malignancy (HCC-SPM) in patients who presented for treatment of a different primary cancer.14,15

Government agencies and cancer professional societies recommend universal HCV screening for patients with cancer.4,8,10,16 Here, we describe our experience in implementing universal screening at The University of Texas MD Anderson Cancer Center (MDACC), one of the largest cancer centers in the United States and the world, which houses the first clinic in the United States devoted to the management of HCV in patients with cancer.17,18

Methods

Study Design and Patient Population

In October 2016, universal HCV screening with HCV antibody (anti-HCV) was initiated at MDACC for all new outpatients. Universal screening was promoted through widespread provider education, newly created orders in the electronic health record (EHR; SmartSets), and automated EHR reminders (best practice alerts [BPAs]) in the Epic EHR software. The effort focused on patients with solid tumors, because universal screening in patients with hematologic malignancies had been standard since 2006.

The ongoing HCV screening initiative was launched in phases. Starting in October 2016, a SmartSet for HCV screening was made available in the EHR at the initial visit. Beginning in December 2019, for all new patients aged ≥18 years with solid tumors, a reminder or BPA was displayed on the EHR screen if the patient had never been tested for HCV, including those not screened using new-patient SmartSet. This BPA was linked to an order for anti-HCV testing. HCV prevalence and linkage to care were assessed after the implementation of SmartSets and BPAs. The study was approved by the MDACC Institutional Review Board.

Clinical and Laboratory Parameters

The PRISM HCV assay (Abbott) was used for all anti-HCV testing. As part of the standard of care, patients with reactive anti-HCV test results were referred to HCV specialists (ie, specialists in infectious diseases or gastroenterology/hepatology) for additional workup and management. At our center, reflex HCV RNA testing is not required before discussion of anti-HCV results with patients. Multidisciplinary care starts at the patient’s first clinic visit in either the Department of Infectious Diseases or the Department of Gastroenterology/Hepatology. During discussions between patients and HCV specialists, patients were asked about their history of HCV and its treatment, the presence of advanced liver disease, and the history of screening for other carcinogenic viruses (eg, hepatitis B virus, HIV).

Outcome Assessments

The primary outcomes of the study were the proportion of patients with solid tumors who were tested for HCV after implementation of universal screening and the proportion of patients with reactive anti-HCV test results linked to HCV care. The secondary outcome was the incidence of HCC-SPM after implementation of universal screening; we compared this incidence with the incidence in historical controls from our institution with HCV-related HCC-SPM.14 Epic’s Reporting Workbench tools were used to identify the HCV orders. To evaluate the impact of our intervention, we compared the total number of patients tested for anti-HCV in the 6 months before implementation of universal HCV screening (April 2016 to October 2016) and during a 6-month period after implementation of universal HCV screening (October 2022 to April 2023). The outcome was also compared by individual specialty clinics to identify those with lower screening rates.

Definitions

Linkage to care was defined as any attendance at a scheduled appointment in the Infectious Diseases or Gastroenterology/Hepatology departments. Proven HCV was defined as reactive anti-HCV test results and detectable HCV RNA. Sustained virologic response was defined as undetectable HCV RNA level at 12 weeks after completion of antiviral treatment. HCC-SPM was defined as development of HCV-associated HCC in a patient with a history of any other type of cancer.14

Statistical Analysis

Patient characteristics were analyzed using descriptive statistics. All descriptive statistical analyses were performed using Stata/IC, version 12.0 (StataCorp LP). Descriptive P values at a 2-sided significance level of .05 were reported. Statistical significance was defined as P<.05 on chi-square analysis.

Results

Of the 85,836 patients with cancer screened for HCV during the study period, 56,075 (65.3%) had solid tumors and were further analyzed (Figure 1). HCV screening was ordered using SmartSets in 39,332 (45.8%) patients and in response to BPAs in 10,972 (12.8%) patients. The proportion of new patients screened increased from 10.1% during the 6 months before study implementation to 34.4% during the last 6 months of the study period (P<.001). The number of patients screened for HCV each month increased over time except during the peak of the COVID-19 pandemic (Figure 2).

Figure 1.
Figure 1.

Flow diagram of study participants.

Abbreviation: HCV, hepatitis C virus.

aOf the 562 patients with proven HCV, 236 (42%) had cirrhosis, most (n=174; 74%) with compensated cirrhosis.

Citation: Journal of the National Comprehensive Cancer Network 2024; 10.6004/jnccn.2023.7332

Figure 2.
Figure 2.

Number of orders for HCV screening by month, April 2016 through April 2023. Implementation of HCV screening for linking patients with solid tumors to care increased the total number of screened patients (linear increase).

Abbreviations: BPA, best practice alert; COVID-19, coronavirus disease 2019; HCV, hepatitis C virus.

Citation: Journal of the National Comprehensive Cancer Network 2024; 10.6004/jnccn.2023.7332

The prevalence of reactive anti-HCV test results was 2.3% (1,300/56,075). The highest HCV prevalence rates were seen in patients with gastrointestinal (5.6%), head and neck (4.0%), and thoracic cancers (4.0%) (Table 1).

Table 1.

New Patients Tested for Anti-HCV After Implementation of Universal HCV Screening

Table 1.

Most of the patients with reactive anti-HCV test results were linked to HCV care (765/1,300; 59%), most patients linked to HCV care had proven HCV infection (562/765; 73%), most patients with proven HCV infection were treated (425/562; 76%), and most treated patients achieved a sustained virologic response (414/425; 97%) (Figure 3). Of the 535 patients who were not linked to care, 370 (69%) were lost to follow-up (many of them seen only for a second opinion from oncologists), 72 (13%) were found not to have chronic HCV infection, likely due to previous exposure and spontaneous clearance, and 93 (17%) died. Of the 425 patients treated, 322 (76%) received treatment before they arrived at the cancer center and 103 (24%) were treated at the cancer center. Of the 137 patients who were not treated, 103 (75%) were not offered direct-acting antiviral treatment because of progressive cancer, 28 (20%) were lost to follow-up, and 6 (4%) were not offered treatment to avoid potential drug–drug interactions (Figure 1).

Figure 3.
Figure 3.

Cascade of care for patients with solid tumors and positive anti-HCV test results after implementation of universal HCV screening.

Abbreviations: HCV, hepatitis C virus; SVR, sustained virologic response.

Citation: Journal of the National Comprehensive Cancer Network 2024; 10.6004/jnccn.2023.7332

We identified 402 patients with HCV-associated HCC during the study period. The incidence of HCC-SPM decreased from 15% in the historical control group of patients seen at our institution between 2011 and 201714 to 5.7% (23/402) between 2017 and 2023, following the initiation of universal screening (P=.0002).

Discussion

To our knowledge, this is the first study focused on universal HCV screening in a large cancer center. We showed the successful implementation of the first institution-wide intervention aimed at HCV testing for all new patients with solid tumors. We found that the universal screening program offers several benefits, including screening of a large number of patients with cancer, successful treatment of most identified HCV-infected patients, and significant reduction in the rate of HCV-associated HCC-SPM. Our experience suggests that this EHR-based screening strategy can be implemented by other cancer centers in the United States and worldwide.

Of note, the prevalence of anti-HCV positivity among patients with cancer in our study was 2.3%, which is higher than the HCV prevalence in the US general population of ≤1%.2 Our findings emphasize the need for increased efforts to identify cases of HCV infection among patients with solid tumors and effective linkage to care, consistent with the goals of the National Hepatitis C Elimination Program.3,7,8

Our study showed an effective way to screen patients using the combination of SmartSets supplemented by BPAs carefully designed to capture patients not screened at the initial visit to generate one-time screening without unnecessary repeat testing.

A multicenter prospective study that included 3,051 patients with newly diagnosed cancer in the United States showed that a substantial proportion (31%) of chronically infected patients were unaware of their HCV infection,12 which supports the use of universal HCV screening among patients with cancer. HCV-infected patients can be linked to HCV care, with access to curable direct-acting antiviral treatment to reduce the risk of liver disease progression, allow patients access to cancer clinical trials, prevent HCV-associated primary and second primary cancers, and cure selected HCV-related cancers.11,1315,19

We found that patients with gastrointestinal, head and neck, and thoracic cancers had the highest prevalence of HCV infection. Previous reports show that head and neck cancers and lung cancer are non-HCC solid tumors with a significantly increased incidence among patients with HCV infection in the United States.20

In our study, nearly two-thirds (59%) of patients with reactive anti-HCV test results were linked to HCV care after implementation of universal HCV screening, 76% of patients with proven HCV infection were treated, and 97% of treated patients achieved a sustained virologic response. These rates were significantly higher than those in previous reports of linkage-to-care programs.2123 Our study’s high linkage-to-care and treatment rates are a significant achievement and are among our most important findings, especially considering that the Polaris Observatory Dashboard reports that only 20% to 30% of detected cases of HCV infection are treated in countries with high-quality patient registries.3 The latest report from the Centers for Disease Control and Prevention highlights that between 2013 and 2022, only 1 in 6 individuals aged <40 years without insurance achieved a virologic cure in the United States.24 If HCV is left untreated, these infected patients can develop primary or second primary cancers related to HCV, such as HCC and B-cell non-Hodgkin lymphoma, and also develop extrahepatic manifestations of HCV infection.13

Our study is the first to address the impact of universal screening on HCV-associated HCC-SPM. We found that the incidence of HCC-SPM significantly decreased after initiating universal screening compared with historical controls from our center,10,24 which suggests that universal HCV screening, linkage to care, and treatment of infected patients is an effective cancer prevention strategy that can save many lives.

This study has limitations. First, our study was conducted at a single tertiary care cancer center with a particular EHR, and our results may not apply to other centers. Second, 41% of patients were not linked to care, and 24% were not treated. However, the high sustained virologic response rates in this study improved oncologic outcomes as reflected in the reduced rate of HCV-associated HCC-SPMs. Third, despite the significant increase in HCV screening rates due to universal screening during the study period, the COVID-19 pandemic led to a decrease in new HCV infection diagnoses, as reported in many countries.3 Fourth, we did not perform a cost-effectiveness analysis, but previous studies have shown that HCV screening and treatment are cost-effective.25,26 Fifth, the HCV screening is still not reaching all new patients with cancer. It is possible that the use of other available support tools (eg, Health Maintenance) or EHR software might improve screening rates. Needless to say, successful screening and microelimination programs require a multidisciplinary team including screening champions, HCV specialists, pharmacists, case managers, patient navigators, EHR analysts, and hospital leadership.

Conclusions

The prevalence of HCV infection remains higher in patients with cancer than in the general population. Our experience shows that universal HCV screening can be successfully implemented in cancer hospitals nationwide using an EHR-based multipronged approach. The high rates of screening, linkage to care, and HCV treatment in our study may positively affect HCV elimination targets and prevent HCV-associated HCCs, leading to improved public health outcomes.

Acknowledgments

The authors thank Stephanie Deming of the Research Medical Library at MD Anderson Cancer Center for editorial assistance.

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Submitted October 31, 2023; final revision received December 15, 2023; accepted for publication December 18, 2023. Published online May 10, 2024.

Previous presentation: A portion of this work was presented at The Liver Meeting 2023; November 10–14, 2023; Boston, Massachusetts.

Author contributions: Study concept and design: Torres. Investigation: Mustafayev. Formal analysis: Torres, Mustafayev, Juneau. Resources: Torres. Writing—original draft: All authors. Writing—review & editing: All authors.

Disclosures: Dr. Torres has disclosed receiving institutional grant/research support from Gilead Sciences and Merck & Co., Inc.; and serving as a scientific advisor for Dynavax Technologies, AbbVie, Gilead Sciences, Janssen Pharmaceuticals, Inc., and Merck & Co., Inc. Dr. Hawk has disclosed serving as a consultant for Exact Sciences. 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 publication was supported by the National Cancer Institute of the National Institutes of Health under award number P30CA016672.

Disclaimer: The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Correspondence: Harrys A. Torres, MD, Department of Infectious Diseases, Infection Control and Employee Health, The University of Texas MD Anderson Cancer Center, 1515 Holcombe Boulevard, Unit 1460, Houston, TX 77030. Email: htorres@mdanderson.org
  • Collapse
  • Expand
  • Figure 1.

    Flow diagram of study participants.

    Abbreviation: HCV, hepatitis C virus.

    aOf the 562 patients with proven HCV, 236 (42%) had cirrhosis, most (n=174; 74%) with compensated cirrhosis.

  • Figure 2.

    Number of orders for HCV screening by month, April 2016 through April 2023. Implementation of HCV screening for linking patients with solid tumors to care increased the total number of screened patients (linear increase).

    Abbreviations: BPA, best practice alert; COVID-19, coronavirus disease 2019; HCV, hepatitis C virus.

  • Figure 3.

    Cascade of care for patients with solid tumors and positive anti-HCV test results after implementation of universal HCV screening.

    Abbreviations: HCV, hepatitis C virus; SVR, sustained virologic response.

  • 1.

    Blach S, Zeuzem S, Manns M, et al. Global prevalence and genotype distribution of hepatitis C virus infection in 2015: a modelling study. Lancet Gastroenterol Hepatol 2017;2:161176.

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

    Hofmeister MG, Rosenthal EM, Barker LK, et al. Estimating prevalence of hepatitis C virus infection in the United States, 2013–2016. Hepatology 2019;69:10201031.

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

    Blach S, Terrault NA, Tacke F, et al. Global change in hepatitis C virus prevalence and cascade of care between 2015 and 2020: a modelling study. Lancet Gastroenterol Hepatol 2022;7:396415.

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

    Centers for Disease Control and Prevention. Hepatitis C: by the numbers. Accessed August 8, 2023. Available at: https://www.cdc.gov/nchhstp/newsroom/docs/factsheets/Hepatitis-c-by-the-numbers.pdf

    • PubMed
    • Export Citation
  • 5.

    World Health Organization. Global health sector strategy on viral hepatitis 2016–2021: toward ending viral hepatitis. Accessed August 8, 2023. Available at: https://www.afro.who.int/sites/default/files/2017-06/WHO-HIV-2016.06-eng.pdf

    • PubMed
    • Export Citation
  • 6.

    Martinello M, Bajis S, Dore GJ. Progress toward hepatitis C virus elimination: therapy and implementation. Gastroenterol Clin North Am 2020;49:253277.

  • 7.

    Fleurence RL, Collins FS. A national hepatitis C elimination program in the United States: a historic opportunity. JAMA 2023;329:12511252.

  • 8.

    Terrault NA, Torres H, Price J, et al. The national hepatitis C elimination program—AASLD’s coalition and call to action. Hepatology 2023;78:371374.

  • 9.

    Ghany MG, Morgan TR, Marks KM, et al. Hepatitis C guidance 2019 update: American Association for the Study of Liver Diseases–Infectious Diseases Society of America recommendations for testing, managing, and treating hepatitis C virus infection. Hepatology 2020;71:686721.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Hwang JP, LoConte NK, Rice JP, et al. Oncologic implications of chronic hepatitis C virus infection. J Oncol Pract 2019;15:629637.

  • 11.

    Torres HA, Pundhir P, Mallet V. Hepatitis C virus infection in patients with cancer: impact on clinical trial enrollment, selection of therapy, and prognosis. Gastroenterology 2019;157:909916.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Ramsey SD, Unger JM, Baker LH, et al. Prevalence of hepatitis B virus, hepatitis C virus, and HIV infection among patients with newly diagnosed cancer from academic and community oncology practices. JAMA Oncol 2019;5:497505.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Torres HA, Shigle TL, Hammoudi N, et al. The oncologic burden of hepatitis C virus infection: a clinical perspective. CA Cancer J Clin 2017;67:411431.

  • 14.

    Dandachi D, Hassan M, Kaseb A, et al. Hepatitis C virus-associated hepatocellular carcinoma as a second primary malignancy: exposing an overlooked presentation of liver cancer. J Hepatocell Carcinoma 2018;5:8186.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Mahale P, Kaseb AO, Hassan MM, et al. Hepatocellular carcinoma as a second primary cancer in patients with chronic hepatitis C virus infection. Dig Liver Dis 2015;47:348349.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Owens DK, Davidson KW, Krist AH, et al. Screening for hepatitis C virus infection in adolescents and adults: US Preventive Services Task Force recommendation statement. JAMA 2020;323:970975.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Torres HA, Adachi JA, Roach LR, et al. Hepatitis C clinic operated by infectious disease specialists at a comprehensive cancer center: help is on the way. Clin Infect Dis 2012;54:740742.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Torres HA, Roach LR, Mahale P, et al. Transdisciplinary approach to managing hepatitis C virus infection in patients at a tertiary care cancer center. J Natl Compr Canc Netw 2016;14:11851188.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Torres HA, Economides MP, Angelidakis G, et al. Sofosbuvir-based therapy in hepatitis C virus-infected cancer patients: a prospective observational study. Am J Gastroenterol 2019;114:250257.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Allison RD, Tong X, Moorman AC, et al. Increased incidence of cancer and cancer-related mortality among persons with chronic hepatitis C infection, 2006–2010. J Hepatol 2015;63:822828.

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