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Interventions to Improve Surveillance for Hepatocellular Carcinoma in High-Risk Patients: A Scoping Review

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Abstract

Purpose

Hepatocellular carcinoma (HCC) is most often a sequela of chronic liver disease or chronic hepatitis B infection. Among high-risk patients, surveillance for HCC every 6 months is recommended by international guidelines. However, rates of HCC surveillance are suboptimal (11–64%). Barriers at the patient, provider, and healthcare delivery system levels have been identified.

Methods

We performed a systemic scoping review to identify and characterize interventions to improve HCC surveillance that has previously been evaluated. Searches using key terms in PubMed and Embase were performed to identify studies examining interventions designed to improve the surveillance rate for HCC in patients with cirrhosis or chronic liver disease that were published in English between January 1990 and September 2021.

Results

Included studies (14) had the following study designs: (1) randomized clinical trials (3, 21.4%), (2) quasi-experimental (2, 14.3%), (3) prospective cohort (6, 42.8%), and (4) retrospective cohort (3, 21.4%). Interventions included mailed outreach invitations, nursing outreach, patient education with or without printed materials, provider education, patient navigation, chronic disease management programs, nursing-led protocols for image ordering, automated reminders to physicians and nurses, web-based clinical management tools, HCC surveillance databases, provider compliance reports, radiology-led surveillance programs, subsidized HCC surveillance, and the use of oral medications. It was found that HCC surveillance rates increased after intervention implementation in all studies.

Conclusion

Despite improvements in HCC surveillance rates with intervention, compliance remained suboptimal. Further analysis of which interventions yield the greatest increases in HCC surveillance, design of multi-pronged strategies, and improved implementation are needed.

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Abbreviations

HCC:

Hepatocellular carcinoma

HBV:

Hepatitis B virus

HCV:

Hepatitis C virus

AASLD:

American Association for the Study of Liver Diseases

EASL-EORTC:

European Association for the Study of the Liver and European Organization for Research and Treatment of Cancer

APASL:

Asian Pacific Association for the Study of the Liver

NCCN:

National Comprehensive Cancer Network (NCCN)

US:

Ultrasound

AFP:

Alpha-fetoprotein

UK:

United Kingdom

NCSP:

National Cancer Screening Program

USPSTF:

United States Preventive Services Task Force

References

  1. El-Serag HB. Epidemiology of viral hepatitis and hepatocellular carcinoma. Gastroenterology; 142. Epub ahead of print 2012. https://doi.org/10.1053/j.gastro.2011.12.061.

  2. Sangiovanni A, Prati GM, Fasani P, et al. The natural history of compensated cirrhosis due to hepatitis C virus: a 17-year cohort study of 214 patients. Hepatology. 2006;43:1303–10.

    Article  PubMed  Google Scholar 

  3. Singal AG, Lampertico P, Nahon P. Epidemiology and surveillance for hepatocellular carcinoma: new trends. J Hepatol. 2020 Feb;72(2):250–61. https://doi.org/10.1016/j.jhep.2019.08.025http://gco.iarc.fr/today.

  4. El-Serag HB. Hepatocellular carcinoma: recent trends in the United States. In: Gastroenterology. W.B. Saunders, 2004. Epub ahead of print 2004. https://doi.org/10.1053/j.gastro.2004.09.013.

  5. Singal AG, Marrero JA. Recent advances in the treatment of hepatocellular carcinoma. Curr Opin Gastroenterol. 2010;26:189–95.

    Article  CAS  PubMed  Google Scholar 

  6. Kansagara D, Papak J, Pasha AS, et al. Screening for hepatocellular carcinoma in chronic liver disease: a systematic review. Ann Intern Med. 2014;161:261–9.

    Article  PubMed  Google Scholar 

  7. Kanwal F, Singal AG. Surveillance for hepatocellular carcinoma: current best practice and future direction. Gastroenterology. 2019;157:54–64.

    Article  PubMed  Google Scholar 

  8. Heimbach JK, Kulik LM, Finn RS, et al. AASLD guidelines for the treatment of hepatocellular carcinoma. Hepatology. 2018;67:358–80.

    Article  PubMed  Google Scholar 

  9. EASL. EASL Clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol. 2018;69:182–236.

  10. Benson AB, D’Angelica MI, Abbott DE, et al. Hepatobiliary cancers, Version 2.2021. JNCCN J Natl Compr Canc Netw. 2021;19:541–565.

  11. Marrero JA, Kulik LM, Sirlin CB, et al. Diagnosis, Staging, and Management of Hepatocellular Carcinoma: 2018 Practice guidance by the American Association for the Study of Liver Diseases. Hepatology. 2018;68:723–50.

    Article  PubMed  Google Scholar 

  12. Bruix J, Sherman M. Management of hepatocellular carcinoma: an update. Hepatology. 2011;53:1020–2.

    Article  PubMed  Google Scholar 

  13. Eslam M, Sarin SK, Wong VWS, et al. The Asian Pacific Association for the Study of the Liver clinical practice guidelines for the diagnosis and management of metabolic associated fatty liver disease. Hep Intl. 2020;14:889–919.

    Article  Google Scholar 

  14. Singal AG, Yopp A, Skinner CS, et al. Utilization of hepatocellular carcinoma surveillance among American patients : a systematic review. J Gen Intern Med. 2012;27:861–7.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Farvardin S, Patel J, Khambaty M, et al. Patient-reported barriers are associated with lower hepatocellular carcinoma surveillance rates in patients with cirrhosis. Hepatology. 2017;65:875–84.

    Article  PubMed  Google Scholar 

  16. 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. 2016;13:791–8.

    Article  Google Scholar 

  17. Singal AG, Tiro JA, Murphy CC, et al. Patient-reported barriers are associated with receipt of hepatocellular carcinoma surveillance in a multicenter cohort of patients with cirrhosis. Clin Gastroenterol Hepatol. 2021;19:987-995.e1.

    Article  PubMed  Google Scholar 

  18. Mahfouz M, Nguyen H, Tu J, et al. Knowledge and perceptions of hepatitis B and hepatocellular carcinoma screening guidelines among trainees: a tale of three centers. Dig Dis Sci. 2020;65:2551–61.

    Article  PubMed  Google Scholar 

  19. Goldberg DS, Taddei TH, Serper M, et al. Identifying barriers to hepatocellular sample of patients with cirrhosis. 2017;65:864–74.

    Google Scholar 

  20. El-Serag HB, Rudolph KL. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology. 2007;132:2557–76.

    Article  CAS  PubMed  Google Scholar 

  21. 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;116:1367–77.

    Article  PubMed  Google Scholar 

  22. Arksey H, Malley LO. Scoping studies : towards a methodological framework. Int J Soc Res Methodol. 2005;8:19–32.

    Article  Google Scholar 

  23. Levac D, Colquhoun H, Brien KKO. Scoping studies : advancing the methodology. Implement Sci. 2010;5:1–9.

    Article  Google Scholar 

  24. 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.

    Article  PubMed  Google Scholar 

  25. Singal AG, Tiro JA, Murphy CC, et al. Mailed outreach invitations significantly improve HCC surveillance rates in patients with cirrhosis: a randomized clinical trial. Hepatology; 69. Epub ahead of print 2019. https://doi.org/10.1002/hep.30129/suppinfo.

  26. Wigg AJ, McCormick R, Wundke R, et al. Efficacy of a chronic disease management model for patients with chronic liver failure. Clin Gastroenterol Hepatol. 2013;11:850-858.e4.

    Article  PubMed  Google Scholar 

  27. Shaw J, Patidar KR, Reuter B, et al. Focused education increases hepatocellular cancer screening in patients with cirrhosis regardless of functional health literacy. Dig Dis Sci. 2021;66:2603–9.

    Article  PubMed  Google Scholar 

  28. Cahill JA, Rizvi S, Saeian K. Assessment of adherence to baseline quality measures for cirrhosis and the impact of performance feedback in a Regional VA Medical Center. Am J Med Qual. 2018;33:262–8.

    Article  PubMed  Google Scholar 

  29. O’Leary DA, Cropp E, Isaac D, et al. “B in IT” - a community-based model for the management of hepatitis B patients in primary care clinics using a novel web-based clinical tool. Hepatol Med Policy. 2018;3:1–10.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Kim HY, Kim CW, Choi JY, et al. A decade-old change in the screening rate for hepatocellular carcinoma among a hepatitis b virus-infected population in Korea. Chin Med J (Engl). 2016;129:15–21.

    Article  PubMed  Google Scholar 

  31. Aberra FB, Essenmacher M, Fisher N, et al. Quality improvement measures lead to higher surveillance rates for hepatocellular carcinoma in patients with cirrhosis. Dig Dis Sci. 2013;58:1157–60.

    Article  PubMed  Google Scholar 

  32. Kennedy NA, Rodgers A, Altus R, et al. Optimisation of hepatocellular carcinoma surveillance in patients with viral hepatitis: a quality improvement study. Intern Med J. 2013;43:772–7.

    Article  CAS  PubMed  Google Scholar 

  33. Rogal SS, Yakovchenko V, Gonzalez R, et al. The hepatic innovation team collaborative: a successful population-based approach to hepatocellular carcinoma surveillance. Cancers (Basel). 2021;13:1–10.

    Article  Google Scholar 

  34. Beste LA, Ioannou GN, Yang Y, et al. Improved surveillance for hepatocellular carcinoma with a primary care-oriented clinical reminder. Clin Gastroenterol Hepatol. 2015;13:172–9.

    Article  PubMed  Google Scholar 

  35. Allard N, Cabrie T, Wheeler E, et al. The challenge of liver cancer surveillance in general practice: do recall and reminder systems hold the answer? Aust Fam Physician. 2017;46:859–64.

    PubMed  Google Scholar 

  36. Nam JY, Lee JH, Kim HY, et al. Oral medications enhance adherence to surveillance for hepatocellular carcinoma and survival in chronic hepatitis B patients. PLoS ONE. 2017;12:1–14.

    Article  Google Scholar 

  37. Farrell C, Halpen A, Cross TJS, et al. Ultrasound surveillance for hepatocellular carcinoma: service evaluation of a radiology-led recall system in a tertiary-referral centre for liver diseases in the UK. Clin Radiol. 2017;72(338):e11-338.e17.

    Google Scholar 

  38. Sabatino SA. Updated recommendations for client- and provider-oriented interventions to increase breast, cervical, and colorectal cancer screening. Am J Prev Med. 2012;43:92–6.

    Article  Google Scholar 

  39. Holden DJ, Jonas DE, Porterfield DS, et al. Systematic review: enhancing the use and quality of colorectal cancer screening. 2010. www.annals.org.

  40. Bonfill Cosp X, Marzo Castillejo M, Pladevall Vila M, et al. Strategies for increasing the participation of women in community breast cancer screening. Cochrane Database Syst Rev. 2016. Epub ahead of print 22 January 2001. https://doi.org/10.1002/14651858.CD002943.

  41. Duffy SW, Myles JP, Maroni R, et al. Rapid review of evaluation of interventions to improve participation in cancer screening services. J Med Screen. 2017;24:127–45.

    Article  PubMed  Google Scholar 

  42. Dougherty MK, Brenner AT, Crockett SD, et al. Evaluation of interventions intended to increase colorectal cancer screening rates in the United States: a systematic review and meta-analysis. JAMA Intern Med. 2018;178:1645–58.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Acharya A, Markar SR, Sodergren MH, et al. Meta-analysis of adjuvant therapy following curative surgery for periampullary adenocarcinoma. Br J Surg. Epub ahead of print 2017. https://doi.org/10.1002/bjs.10563.

  44. Shojania KG, Jennings A, Mayhew A, et al. Effect of point-of-care computer reminders on physician behaviour: a systematic review. CMAJ Can Med Assoc J. 182. Epub ahead of print 23 March 2010. https://doi.org/10.1503/cmaj.090578.

  45. Pedersen ER, Rubenstein L, Kandrack R, et al. Elusive search for effective provider interventions: a systematic review of provider interventions to increase adherence to evidence-based treatment for depression. Implement Sci. 13. Epub ahead of print 20 July 2018. https://doi.org/10.1186/s13012-018-0788-8.

  46. Thomson MJ, Lok AS, Tapper EB. Optimizing medication management for patients with cirrhosis: evidence-based strategies and their outcomes. Liver Int. 2018;38:1882–90.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Episoft. https://episofthealth.com/our-story/. Accessed 25 April 2023.

  48. AviTracks. https://www.avicenna-medical.com/specialty-disease-management-software-hepatology. Accessed 25 April 2023.

  49. Lok ASF, Mcmahon BJ, Brown RS, et al. Antiviral therapy for chronic hepatitis B viral infection in adults: a systematic review and meta-analysis. Epub ahead of print 2015. https://doi.org/10.1002/hep.28280/suppinfo.

  50. Russo MW. Antiviral therapy for hepatitis C is associated with improved clinical outcomes in patients with advanced fibrosis. Expert Rev Gastroenterol Hepatol. 2010;4:535–9.

    Article  PubMed  Google Scholar 

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Authors and Affiliations

Authors

Contributions

All authors contributed to the study conception and design. Literature review, data collection, and analysis were performed by Molly McNamara and Eliza Beal. The first draft of the manuscript was written by Molly McNamara, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Eliza W. Beal.

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Appendix

Appendix

Table 3 Search strategies PubMed and Embase

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Beal, E.W., McNamara, M., Owen, M. et al. Interventions to Improve Surveillance for Hepatocellular Carcinoma in High-Risk Patients: A Scoping Review. J Gastrointest Canc 55, 1–14 (2024). https://doi.org/10.1007/s12029-023-00944-1

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