Hepatocellular carcinoma surveillance — utilization, barriers and the impact of changing aetiology (original) (raw)
Sung, H. et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin.71, 209–249 (2021). PubMed Google Scholar
Rumgay, H. et al. Global burden of primary liver cancer in 2020 and predictions to 2040. J. Hepatol.77, 1598–1606 (2022). PubMedPubMed Central Google Scholar
Llovet, J. M. et al. Hepatocellular carcinoma. Nat. Rev. Dis. Prim.7, 6 (2021). PubMed Google Scholar
Moon, A. M., Singal, A. G. & Tapper, E. B. Contemporary epidemiology of chronic liver disease and cirrhosis. Clin. Gastroenterol. Hepatol.18, 2650–2666 (2020). PubMed Google Scholar
Reveron-Thornton, R. F. et al. Global and regional long-term survival following resection for HCC in the recent decade: a meta-analysis of 110 studies. Hepatol. Commun.6, 1813–1826 (2022). PubMedPubMed Central Google Scholar
Koh, J. H. et al. Liver resection versus liver transplantation for hepatocellular carcinoma within Milan criteria: a meta-analysis of 18,421 patients. Hepatobiliary Surg. Nutr.11, 78–93 (2022). PubMedPubMed Central Google Scholar
Sangro, B., Sarobe, P., Hervás-Stubbs, S. & Melero, I. Advances in immunotherapy for hepatocellular carcinoma. Nat. Rev. Gastroenterol. Hepatol.18, 525–543 (2021). PubMedPubMed Central Google Scholar
Vogel, A. & Martinelli, E. Updated treatment recommendations for hepatocellular carcinoma (HCC) from the ESMO clinical practice guidelines. Ann. Oncol.32, 801–805 (2021). CASPubMed Google Scholar
Heimbach, J. K. et al. AASLD guidelines for the treatment of hepatocellular carcinoma. Hepatology67, 358–380 (2018). PubMed Google Scholar
EASL Clinical Practice Guidelines. Management of hepatocellular carcinoma. J. Hepatol.69, 182–236 (2018). Google Scholar
Cheng, A.-L. et al. Updated efficacy and safety data from IMbrave150: atezolizumab plus bevacizumab vs. sorafenib for unresectable hepatocellular carcinoma. J. Hepatol.76, 862–873 (2022). CASPubMed Google Scholar
Huang, D. Q. et al. Characteristics and outcomes of hepatocellular carcinoma patients with macrovascular invasion following surgical resection: a meta-analysis of 40 studies and 8,218 patients. Hepatobiliary Surg. Nutr.11, 848–860 (2022). PubMedPubMed Central Google Scholar
Tapper, E. B. & Parikh, N. D. Mortality due to cirrhosis and liver cancer in the United States, 1999-2016: observational study. Br. Med. J.362, k2817 (2018). Google Scholar
Huang, D. Q. et al. Changing global epidemiology of liver cancer from 2010 to 2019: NASH is the fastest growing cause of liver cancer. Cell Metab.34, 969–977.e2 (2022). CASPubMedPubMed Central Google Scholar
El-Serag, H. B. & Rudolph, K. L. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology132, 2557–2576 (2007). CASPubMed Google Scholar
Omata, M. et al. Asia-Pacific clinical practice guidelines on the management of hepatocellular carcinoma: a 2017 update. Hepatol. Int.11, 317–370 (2017). PubMed Google Scholar
Zhang, B.-H., Yang, B.-H. & Tang, Z.-Y. Randomized controlled trial of screening for hepatocellular carcinoma. J. Cancer Res. Clin. Oncol.130, 417–422 (2004). PubMed Google Scholar
Jepsen, P. & West, J. We need stronger evidence for (or against) hepatocellular carcinoma surveillance. J. Hepatol.74, 1234–1239 (2021). PubMed Google Scholar
Singal, A. G. et al. HCC surveillance improves early detection, curative treatment receipt, and survival in patients with cirrhosis: a meta-analysis. J. Hepatol.77, 128–139 (2022). PubMedPubMed Central Google Scholar
Wolf, E., Rich, N. E., Marrero, J. A., Parikh, N. D. & Singal, A. G. Use of hepatocellular carcinoma surveillance in patients with cirrhosis: a systematic review and meta-analysis. Hepatology73, 713–725 (2021). PubMed Google Scholar
Nguyen, M. H. et al. Gaps in hepatocellular carcinoma surveillance among insured patients with hepatitis B infection without cirrhosis in the United States. Hepatol. Commun.6, 3443–3456 (2022). CASPubMedPubMed Central Google Scholar
Ye, Q. et al. Substantial gaps in evaluation and treatment of patients with hepatitis B in the US. J. Hepatol.76, 63–74 (2022). CASPubMed Google Scholar
Zhao, C. & Nguyen, M. H. Hepatocellular carcinoma screening and surveillance: practice guidelines and real-life practice. J. Clin. Gastroenterol.50, 120–133 (2016). CASPubMed Google Scholar
Huang, D. Q., Mathurin, P., Cortez-Pinto, H. & Loomba, R. Global epidemiology of alcohol-associated cirrhosis and HCC: trends, projections and risk factors. Nat. Rev. Gastroenterol. Hepatol.20, 37–49 (2023). PubMed Google Scholar
Tan, D. J. H. et al. Clinical characteristics, surveillance, treatment allocation, and outcomes of non-alcoholic fatty liver disease-related hepatocellular carcinoma: a systematic review and meta-analysis. Lancet Oncol.23, 521–530 (2022). PubMedPubMed Central Google Scholar
Simmons, O. et al. Predictors of adequate ultrasound quality for hepatocellular carcinoma surveillance in patients with cirrhosis. Aliment. Pharmacol. Ther.45, 169–177 (2017). CASPubMed Google Scholar
Marrero, J. A. et al. Diagnosis, staging, and management of hepatocellular carcinoma: 2018 practice guidance by the American Association for the Study of Liver Diseases. Hepatology68, 723–750 (2018). PubMed Google Scholar
Kim, J. H. et al. Modified PAGE-B score predicts the risk of hepatocellular carcinoma in Asians with chronic hepatitis B on antiviral therapy. J. Hepatol.69, 1066–1073 (2018). PubMed Google Scholar
Kanwal, F. & Singal, A. G. Surveillance for hepatocellular carcinoma: current best practice and future direction. Gastroenterology157, 54–64 (2019). PubMed Google Scholar
Davila, J. A. et al. Utilization of surveillance for hepatocellular carcinoma among hepatitis C virus-infected veterans in the United States. Ann. Intern. Med.154, 85–93 (2011). PubMed Google Scholar
Goldberg, D. S. et al. Identifying barriers to hepatocellular carcinoma surveillance in a national sample of patients with cirrhosis. Hepatology65, 864–874 (2017). PubMed Google Scholar
Tran, S. A. et al. Rate of hepatocellular carcinoma surveillance remains low for a large, real-life cohort of patients with hepatitis C cirrhosis. BMJ Open Gastroenterol.5, e000192 (2018). PubMedPubMed Central Google Scholar
Nguyen, M. H. et al. Gaps in hepatocellular carcinoma surveillance in a United States cohort of insured patients with cirrhosis. Curr. Med. Res. Opin.38, 2163–2173 (2022). PubMed Google Scholar
Yeo, Y. H. et al. Surveillance of patients with cirrhosis remains suboptimal in the United States. J. Hepatol.75, 856–864 (2021). PubMed Google Scholar
Zhao, C. et al. Poor adherence to hepatocellular carcinoma surveillance: a systematic review and meta-analysis of a complex issue. Liver Int.38, 503–514 (2018). PubMed Google Scholar
Wang, C. et al. Poor adherence and low persistency rates for hepatocellular carcinoma surveillance in patients with chronic hepatitis B. Medicine95, e4744 (2016). PubMedPubMed Central Google Scholar
Singal, A. G. et al. Failure rates in the hepatocellular carcinoma surveillance process. Cancer Prev. Res.5, 1124–1130 (2012). Google Scholar
Zhang, W. et al. Awareness and knowledge of nonalcoholic fatty liver disease among office employees in Beijing, Cchina. Dig. Dis. Sci.64, 708–717 (2019). PubMed Google Scholar
Jun, D. W. et al. A study of the awareness of chronic liver diseases among Korean adults. Korean J. Hepatol.17, 99–105 (2011). PubMedPubMed Central Google Scholar
Farvardin, S. et al. Patient-reported barriers are associated with lower hepatocellular carcinoma surveillance rates in patients with cirrhosis. Hepatology65, 875–884 (2017). PubMed Google Scholar
Singal, A. G. et al. Patient-reported barriers are associated with receipt of hepatocellular carcinoma surveillance in a multicenter cohort of patients with cirrhosis. Clin. Gastroenterol. Hepatol.19, 987–995.e1 (2021). PubMed Google Scholar
Rodriguez Villalvazo, Y. et al. Effect of travel distance and rurality of residence on initial surveillance for hepatocellular carcinoma in VA primary care patient with cirrhosis. Health Serv. Res.55, 103–112 (2020). PubMed Google Scholar
Teerasarntipan, T. et al. Physician- and patient-reported barriers to hepatocellular carcinoma surveillance: a nationwide survey. Medicine101, e30538 (2022). PubMed Google Scholar
Karlsen, T. H. et al. The EASL-Lancet Liver Commission: protecting the next generation of Europeans against liver disease complications and premature mortality. Lancet399, 61–116 (2022). PubMed Google Scholar
Walker, M. et al. Cirrhosis is under-recognised in patients subsequently diagnosed with hepatocellular cancer. Aliment. Pharmacol. Ther.43, 621–630 (2016). CASPubMedPubMed Central Google Scholar
Alexander, M. et al. Real-world data reveal a diagnostic gap in non-alcoholic fatty liver disease. BMC Med.16, 130 (2018). PubMedPubMed Central Google Scholar
Riazi, K. et al. The prevalence and incidence of NAFLD worldwide: a systematic review and meta-analysis. Lancet Gastroenterol. Hepatol.7, 851–861 (2022). PubMed Google Scholar
Le, M. H. et al. 2019 Global NAFLD prevalence — a systematic review and meta-analysis. Clin. Gastroenterol. Hepatol.20, 2809–2817.e28 (2021). PubMed Google Scholar
Simmons, O. L., Feng, Y., Parikh, N. D. & Singal, A. G. Primary care provider practice patterns and barriers to hepatocellular carcinoma surveillance. Clin. Gastroenterol. Hepatol.17, 766–773 (2019). PubMed Google Scholar
Tzartzeva, K. et al. Surveillance imaging and alpha fetoprotein for early detection of hepatocellular carcinoma in patients with cirrhosis: a meta-analysis. Gastroenterology154, 1706–1718.e1 (2018). CASPubMed Google Scholar
Tan, D. J. H. et al. UNOS down-staging criteria for liver transplantation of hepatocellular carcinoma: systematic review and meta-analysis of 25 studies. Clin. Gastroenterol. Hepatol.21, 1475–1484 (2022). PubMed Google Scholar
Reig, M. et al. BCLC strategy for prognosis prediction and treatment recommendation: the 2022 update. J. Hepatol.76, 681–693 (2022). PubMed Google Scholar
Del Poggio, P. et al. Factors that affect efficacy of ultrasound surveillance for early stage hepatocellular carcinoma in patients with cirrhosis. Clin. Gastroenterol. Hepatol.12, 1927–1933.e2 (2014). PubMed Google Scholar
Fetzer, D. T. et al. Screening and surveillance of hepatocellular carcinoma: an introduction to ultrasound liver imaging reporting and data system. Radiol. Clin. North Am.55, 1197–1209 (2017). PubMed Google Scholar
Tang, A. et al. Introduction to the liver imaging reporting and data system for hepatocellular carcinoma. Clin. Gastroenterol. Hepatol.17, 1228–1238 (2019). PubMed Google Scholar
Schoenberger, H. et al. Dynamic changes in ultrasound quality for hepatocellular carcinoma screening in patients with cirrhosis. Clin. Gastroenterol. Hepatol.20, 1561–1569 (2021). PubMedPubMed Central Google Scholar
Chong, N. et al. Association between ultrasound quality and test performance for HCC surveillance in patients with cirrhosis: a retrospective cohort study. Aliment. Pharmacol. Ther.55, 683–690 (2022). PubMed Google Scholar
Atiq, O. et al. An assessment of benefits and harms of hepatocellular carcinoma surveillance in patients with cirrhosis. Hepatology65, 1196–1205 (2017). CASPubMed Google Scholar
Singal, A. G. et al. Benefits and harms of hepatocellular carcinoma surveillance in a prospective cohort of patients with cirrhosis. Clin. Gastroenterol. Hepatol.19, 1925–1932.e1 (2021). PubMed Google Scholar
Dale, W., Bilir, P., Han, M. & Meltzer, D. The role of anxiety in prostate carcinoma: a structured review of the literature. Cancer104, 467–478 (2005). PubMed Google Scholar
Tan, D. J. H. et al. Global burden of liver cancer in males and females: changing etiological basis and the growing contribution of NASH. Hepatology77, 1150–1163 (2022). PubMed Google Scholar
Ng, C. H., Huang, D. Q. & Nguyen, M. H. NAFLD versus MAFLD: prevalence, outcomes and implications of a change in name. Clin. Mol. Hepatol.28, 790–801 (2022). PubMedPubMed Central Google Scholar
Ng, C. H. et al. Examining the interim proposal for name change to steatotic liver disease in the US population. Hepatology77, 1712–1721 (2023). PubMed Google Scholar
Eslam, M. et al. MAFLD: a consensus-driven proposed nomenclature for metabolic associated fatty liver disease. Gastroenterology158, 1999–2014.e1 (2020). CASPubMed Google Scholar
Huang, D. Q. et al. Hepatocellular carcinoma incidence in alcohol-associated cirrhosis: systematic review and meta-analysis. Clin. Gastroenterol. Hepatol.21, 1169–1177 (2022). PubMed Google Scholar
Orci, L. A. et al. Incidence of hepatocellular carcinoma in patients with nonalcoholic fatty liver disease: a systematic review, meta-analysis, and meta-regression. Clin. Gastroenterol. Hepatol.20, 283–292.e10 (2022). PubMed Google Scholar
Kanwal, F. et al. Risk factors for HCC in contemporary cohorts of patients with cirrhosis. Hepatology77, 997–1005 (2022). Google Scholar
Ioannou, G. N., Green, P., Kerr, K. F. & Berry, K. Models estimating risk of hepatocellular carcinoma in patients with alcohol or NAFLD-related cirrhosis for risk stratification. J. Hepatol.71, 523–533 (2019). PubMedPubMed Central Google Scholar
Younossi, Z. et al. The global epidemiology of nonalcoholic fatty liver disease (NAFLD) and non-alcoholic steatohepatitis (NASH): a systematic review. Hepatology77, 1335–1347 (2019). Google Scholar
Huang, D. Q., El-Serag, H. B. & Loomba, R. Global epidemiology of NAFLD-related HCC: trends, predictions, risk factors and prevention. Nat. Rev. Gastroenterol. Hepatol.18, 223–238 (2021). PubMed Google Scholar
Vitale, A. et al. Epidemiological trends and trajectories of MAFLD-associated hepatocellular carcinoma 2002-2033: the ITA.LI.CA database. Gut72, 141–152 (2023). PubMed Google Scholar
Karim, M. A. et al. Clinical characteristics and outcomes of nonalcoholic fatty liver disease-associated hepatocellular carcinoma in the United States. Clin. Gastroenterol. Hepatol.21, 670–680.e18 (2022). PubMed Google Scholar
Natarajan, Y. et al. Risk of cirrhosis and hepatocellular cancer in patients with NAFLD and normal liver enzymes. Hepatology72, 1242–1252 (2020). CASPubMed Google Scholar
Kanwal, F. et al. Risk of hepatocellular cancer in patients with non-alcoholic fatty liver disease. Gastroenterology155, 1828–1837.e2 (2018). PubMed Google Scholar
Sanyal, A. J. et al. Prospective study of outcomes in adults with nonalcoholic fatty liver disease. N. Engl. J. Med.385, 1559–1569 (2021). CASPubMedPubMed Central Google Scholar
Simon, T. G. et al. Cancer risk in patients with biopsy-confirmed nonalcoholic fatty liver disease: a population-based cohort study. Hepatology74, 2410–2423 (2021). CASPubMed Google Scholar
Cucchetti, A., Cescon, M., Erroi, V. & Pinna, A. D. Cost-effectiveness of liver cancer screening. Best Pract. Res. Clin. Gastroenterol.27, 961–972 (2013). PubMed Google Scholar
Loomba, R., Lim, J. K., Patton, H. & El-Serag, H. B. AGA clinical practice update on screening and surveillance for hepatocellular carcinoma in patients with nonalcoholic fatty liver disease: expert review. Gastroenterology158, 1822–1830 (2020). PubMed Google Scholar
Mózes, F. E. et al. Diagnostic accuracy of non-invasive tests for advanced fibrosis in patients with NAFLD: an individual patient data meta-analysis. Gut71, 1006–1019 (2022). PubMed Google Scholar
Loomba, R. & Adams, L. A. Advances in non-invasive assessment of hepatic fibrosis. Gut69, 1343–1352 (2020). CASPubMed Google Scholar
Vali, Y. et al. Enhanced liver fibrosis test for the non-invasive diagnosis of fibrosis in patients with NAFLD: a systematic review and meta-analysis. J. Hepatol.73, 252–262 (2020). PubMed Google Scholar
Loomba, R. et al. Liver stiffness thresholds to predict disease progression and clinical outcomes in bridging fibrosis and cirrhosis. Gut72, 581–589 (2023). CASPubMed Google Scholar
Teng, M. L., Tan, D. J. H., Ng, C. H. & Huang, D. Q. Hepatocellular carcinoma surveillance in non-alcoholic fatty liver disease — who and how? Clin. Mol. Hepatol.29, 404–407 (2023). PubMedPubMed Central Google Scholar
Huang, D. Q. et al. Type 2 diabetes, hepatic decompensation and hepatocellular carcinoma in patients with non-alcoholic fatty liver disease: an individual participant-level data meta-analysis. Lancet Gastroenterol. Hepatol.https://doi.org/10.1016/S2468-1253(23)00157-7 (2023).
Kramer, J. R. et al. Effect of diabetes medications and glycemic control on risk of hepatocellular cancer in patients with nonalcoholic fatty liver disease. Hepatology75, 1420–1428 (2022). CASPubMed Google Scholar
Kanwal, F. et al. Effect of metabolic traits on the risk of cirrhosis and hepatocellular cancer in nonalcoholic fatty liver disease. Hepatology71, 808–819 (2020). PubMed Google Scholar
Cholankeril, G. et al. Longitudinal changes in fibrosis markers are associated with risk of cirrhosis and hepatocellular carcinoma in non-alcoholic fatty liver disease. J. Hepatol.78, 493–500 (2023). CASPubMed Google Scholar
Ioannou, G. N. Epidemiology and risk-stratification of NAFLD-associated HCC. J. Hepatol.75, 1476–1484 (2021). PubMed Google Scholar
Nemutlu, G., Hajjar, A. & Mueller, P. Which individuals with nonalcoholic fatty liver disease should undergo HCC surveillance? cost-effectiveness analysis. Hepatology76, S1–S1564 (2022). Google Scholar
Huang, D. Q. et al. Comparative efficacy of an optimal exam between ultrasound versus abbreviated MRI for HCC screening in NAFLD cirrhosis: a prospective study. Aliment. Pharmacol. Ther.55, 820–827 (2022). CASPubMedPubMed Central Google Scholar
McNeely, J. et al. Barriers and facilitators affecting the implementation of substance use screening in primary care clinics: a qualitative study of patients, providers, and staff. Addict. Sci. Clin. Pract.13, 8 (2018). PubMedPubMed Central Google Scholar
DiMartini, A. F., Leggio, L. & Singal, A. K. Barriers to the management of alcohol use disorder and alcohol-associated liver disease: strategies to implement integrated care models. Lancet Gastroenterol. Hepatol.7, 186–195 (2022). PubMed Google Scholar
Bucci, L. et al. Comparison between alcohol- and hepatitis C virus-related hepatocellular carcinoma: clinical presentation, treatment and outcome. Aliment. Pharmacol. Ther.43, 385–399 (2016). CASPubMed Google Scholar
Schutte, K. et al. Delayed diagnosis of HCC with chronic alcoholic liver disease. Liver Cancer1, 257–266 (2012). PubMedPubMed Central Google Scholar
Costentin, C. E. et al. Hepatocellular carcinoma is diagnosed at a later stage in alcoholic patients: results of a prospective, nationwide study. Cancer124, 1964–1972 (2018). PubMed Google Scholar
Costentin, C. E. et al. Geographical disparities of outcomes of hepatocellular carcinoma in France: the heavier burden of alcohol compared to hepatitis C. Dig. Dis. Sci.65, 301–311 (2020). CASPubMed Google Scholar
Seitz, H. K. et al. Alcoholic liver disease. Nat. Rev. Dis. Prim.4, 16 (2018). PubMed Google Scholar
Keyes, K. M. et al. Stigma and treatment for alcohol disorders in the United States. Am. J. Epidemiol.172, 1364–1372 (2010). CASPubMedPubMed Central Google Scholar
Im, G. Y. et al. Provider attitudes and practices for alcohol screening, treatment, and education in patients with liver disease: a survey from the American Association for the Study of Liver Diseases Alcohol-associated Liver Disease Special Interest Group. Clin. Gastroenterol. Hepatol.19, 2407–2416.e8 (2021). PubMed Google Scholar
Bataller, R., Arab, J. P. & Shah, V. H. Alcohol-associated hepatitis. N. Engl. J. Med.387, 2436–2448 (2022). CASPubMed Google Scholar
Jepsen, P. et al. Risk of hepatocellular carcinoma in Danish outpatients with alcohol-related cirrhosis. J. Hepatol.73, 1030–1036 (2020). PubMed Google Scholar
Parikh, N. D., Singal, A. G., Hutton, D. W. & Tapper, E. B. Cost-effectiveness of hepatocellular carcinoma surveillance: an assessment of benefits and harms. Am. J. Gastroenterol.115, 1642–1649 (2020). PubMedPubMed Central Google Scholar
Singal, A. K. & Mathurin, P. Diagnosis and treatment of alcohol-associated liver disease: a review. J. Am. Med. Assoc.326, 165–176 (2021). CAS Google Scholar
Kim, N. J., Vutien, P., Cleveland, E., Cravero, A. & Ioannou, G. N. Fibrosis stage-specific incidence of hepatocellular cancer after hepatitis c cure with direct-acting antivirals: a systematic review and meta-analysis. Clin. Gastroenterol. Hepatol.21, 1723–1738.e5 (2022). PubMed Google Scholar
Kanwal, F. et al. Risk of hepatocellular cancer in HCV patients treated with direct-acting antiviral agents. Gastroenterology153, 996–1005.e1 (2017). CASPubMed Google Scholar
Calvaruso, V. et al. Incidence of hepatocellular carcinoma in patients with HCV-associated cirrhosis treated with direct-acting antiviral agents. Gastroenterology155, 411–421.e4 (2018). CASPubMed Google Scholar
Romano, A. et al. Newly diagnosed hepatocellular carcinoma in patients with advanced hepatitis C treated with DAAs: a prospective population study. J. Hepatol.69, 345–352 (2018). CASPubMed Google Scholar
Ogawa, E. et al. Association of direct-acting antiviral therapy with liver and nonliver complications and long-term mortality in patients with chronic hepatitis C. JAMA Intern. Med.183, 97–105 (2022). Google Scholar
Dang, H. et al. Cure with interferon-free direct-acting antiviral is associated with increased survival in patients with hepatitis C virus-related hepatocellular carcinoma from both east and west. Hepatology71, 1910–1922 (2020). CASPubMed Google Scholar
Shiha, G. et al. Incidence of HCC in chronic hepatitis C patients with advanced hepatic fibrosis who achieved SVR following DAAs: a prospective study. J. Viral Hepat.27, 671–679 (2020). CASPubMed Google Scholar
Tanaka, Y. et al. HCC risk post-SVR with DAAs in East Asians: findings from the REAL-C cohort. Hepatol. Int.14, 1023–1033 (2020). PubMed Google Scholar
Semmler, G. et al. HCC risk stratification after cure of hepatitis C in patients with compensated advanced chronic liver disease. J. Hepatol.76, 812–821 (2022). CASPubMed Google Scholar
DʼAmbrosio, R. et al. Incidence of liver- and non-liver-related outcomes in patients with HCV-cirrhosis after SVR. J. Hepatol.76, 302–310 (2022). PubMed Google Scholar
Degasperi, E. et al. Factors associated with increased risk of de novo or recurrent hepatocellular carcinoma in patients with cirrhosis treated with direct-acting antivirals for HCV infection. Clin. Gastroenterol. Hepatol.17, 1183–1191.e7 (2019). CASPubMed Google Scholar
Farhang Zangneh, H. et al. Cost effectiveness of hepatocellular carcinoma surveillance after a sustained virologic response to therapy in patients with hepatitis c virus infection and advanced fibrosis. Clin. Gastroenterol. Hepatol.17, 1840–1849.e16 (2019). PubMed Google Scholar
Kanda, T. et al. APASL HCV guidelines of virus-eradicated patients by DAA on how to monitor HCC occurrence and HBV reactivation. Hepatol. Int.13, 649–661 (2019). PubMed Google Scholar
Ioannou, G. N. et al. Development of models estimating the risk of hepatocellular carcinoma after antiviral treatment for hepatitis C. J. Hepatol.69, 1088–1098 (2018). PubMedPubMed Central Google Scholar
Ioannou, G. N. HCC surveillance after SVR in patients with F3/F4 fibrosis. J. Hepatol.74, 458–465 (2021). PubMed Google Scholar
Le, M. H. et al. Chronic hepatitis B prevalence among foreign-born and U.S.-born adults in the United States, 1999-2016. Hepatology71, 431–443 (2020). CASPubMed Google Scholar
Nguyen, M. H., Wong, G., Gane, E., Kao, J. H. & Dusheiko, G. Hepatitis B virus: advances in prevention, diagnosis, and therapy. Clin. Microbiol. Rev.33, e00046–19 (2020). PubMedPubMed Central Google Scholar
Tan, D. J. H. et al. Risk of hepatocellular carcinoma with tenofovir vs entecavir treatment for chronic hepatitis B virus: a reconstructed individual patient data meta-analysis. JAMA Netw. Open5, e2219407 (2022). PubMedPubMed Central Google Scholar
Chan, A. C. Y. et al. Impact of antiviral therapy on the survival of patients after major hepatectomy for hepatitis B virus-related hepatocellular carcinoma. Arch. Surg.146, 675–681 (2011). PubMed Google Scholar
GBD 2019 Hepatitis B Collaborators.Global, regional, and national burden of hepatitis B, 1990-2019: a systematic analysis for the Global Burden of Disease Study 2019. Lancet Gastroenterol. Hepatol.7, 796–829 (2022). Google Scholar
Yang, H. I. et al. Risk estimation for hepatocellular carcinoma in chronic hepatitis B (REACH-B): development and validation of a predictive score. Lancet Oncol.12, 568–574 (2011). PubMed Google Scholar
Lee, H. W. et al. Prediction of development of liver-related events by transient elastography in hepatitis B patients with complete virological response on antiviral therapy. Am. J. Gastroenterol.109, 1241–1249 (2014). CASPubMed Google Scholar
Wong, V. W. et al. Clinical scoring system to predict hepatocellular carcinoma in chronic hepatitis B carriers. J. Clin. Oncol.28, 1660–1665 (2010). CASPubMed Google Scholar
Wong, G. L. et al. Liver stiffness-based optimization of hepatocellular carcinoma risk score in patients with chronic hepatitis B. J. Hepatol.60, 339–345 (2014). PubMed Google Scholar
Yuen, M. F. et al. Independent risk factors and predictive score for the development of hepatocellular carcinoma in chronic hepatitis B. J. Hepatol.50, 80–88 (2009). PubMed Google Scholar
Yang, H. I. et al. Nomograms for risk of hepatocellular carcinoma in patients with chronic hepatitis B virus infection. J. Clin. Oncol.28, 2437–2444 (2010). PubMed Google Scholar
Papatheodoridis, G. et al. PAGE-B predicts the risk of developing hepatocellular carcinoma in Caucasians with chronic hepatitis B on 5-year antiviral therapy. J. Hepatol.64, 800–806 (2016). CASPubMed Google Scholar
Papatheodoridis, G. V. et al. Hepatocellular carcinoma prediction beyond year 5 of oral therapy in a large cohort of Caucasian patients with chronic hepatitis B. J. Hepatol.72, 1088–1096 (2020). CASPubMed Google Scholar
Voulgaris, T., Papatheodoridi, M., Lampertico, P. & Papatheodoridis, G. V. Clinical utility of hepatocellular carcinoma risk scores in chronic hepatitis B. Liver Int.40, 484–495 (2020). PubMed Google Scholar
Yang, H. I. et al. REAL-B (Real-world effectiveness from the asia pacific rim liver consortium for HBV) risk score for the prediction of hepatocellular carcinoma in chronic hepatitis B patients treated with oral antiviral therapy. J. Infect. Dis.221, 389–399 (2019). Google Scholar
Poh, Z. et al. Real-world risk score for hepatocellular carcinoma (RWS-HCC): a clinically practical risk predictor for HCC in chronic hepatitis B. Gut65, 887–888 (2016). CASPubMed Google Scholar
Papatheodoridis, G. V. et al. Predictive performance of newer Asian hepatocellular carcinoma risk scores in treated Caucasians with chronic hepatitis B. JHEP Rep.3, 100290 (2021). PubMedPubMed Central Google Scholar
Chen, C. J. et al. Risk of hepatocellular carcinoma across a biological gradient of serum hepatitis B virus DNA level. J. Am. Med. Assoc.295, 65–73 (2006). CAS Google Scholar
Yu, J. H., Cho, S. G., Jin, Y.-J. & Lee, J.-W. The best predictive model for hepatocellular carcinoma in patients with chronic hepatitis B infection. Clin. Mol. Hepatol.28, 351–361 (2022). PubMed Google Scholar
Huang, D. Q. et al. Natural history and hepatocellular carcinoma risk in untreated chronic hepatitis B patients with indeterminate phase. Clin. Gastroenterol. Hepatol.20, 1803–1812.e5 (2022). CASPubMed Google Scholar
Chang, M.-L. & Liaw, Y.-F. Hepatitis B flares in chronic hepatitis B: Pathogenesis, natural course, and management. J. Hepatol.61, 1407–1417 (2014). PubMed Google Scholar
Kim, H. S. et al. Comparative performance of risk prediction models for hepatitis B-related hepatocellular carcinoma in the United States. J. Hepatol.76, 294–301 (2022). CASPubMed Google Scholar
Yu, J. H. et al. Prediction model for hepatocellular carcinoma risk in treatment-naive chronic hepatitis B patients receiving entecavir/tenofovir. Eur. J. Gastroenterol. Hepatol.31, 865–872 (2019). CASPubMed Google Scholar
Riveiro-Barciela, M. et al. Effectiveness and safety of entecavir or tenofovir in a spanish cohort of chronic hepatitis B patients: validation of the page-B score to predict hepatocellular carcinoma. Dig. Dis. Sci.62, 784–793 (2017). CASPubMed Google Scholar
Kennedy, N. A. et al. Optimisation of hepatocellular carcinoma surveillance in patients with viral hepatitis: a quality improvement study. Intern. Med. J.43, 772–777 (2013). CASPubMed Google Scholar
Singal, A. G. et al. Multicenter randomized clinical trial of a mailed outreach strategy for hepatocellular carcinoma surveillance. Clin. Gastroenterol. Hepatol.20, 2818–2825.e1 (2021). PubMed Google Scholar
Del Poggio, P. et al. A training program for primary care physicians improves the effectiveness of ultrasound surveillance of hepatocellular carcinoma. Eur. J. Gastroenterol. Hepatol.27, 1103–1108 (2015). PubMed Google Scholar
Beste, L. A. et al. Improved surveillance for hepatocellular carcinoma with a primary care-oriented clinical reminder. Clin. Gastroenterol. Hepatol.13, 172–179 (2015). PubMed Google Scholar
Aberra, F. B., Essenmacher, M., Fisher, N. & Volk, M. L. Quality improvement measures lead to higher surveillance rates for hepatocellular carcinoma in patients with cirrhosis. Dig. Dis. Sci.58, 1157–1160 (2013). PubMed Google Scholar
Labenz, C. et al. Structured early detection of asymptomatic liver cirrhosis: results of the population-based liver screening program SEAL. J. Hepatol.77, 695–701 (2022). PubMed Google Scholar
Kudo, M. Japan’s successful model of nationwide hepatocellular carcinoma surveillance highlighting the urgent need for global surveillance. Liver Cancer1, 141–143 (2012). CASPubMedPubMed Central Google Scholar
Liao, S.-H. et al. Long-term effectiveness of population-wide multifaceted interventions for hepatocellular carcinoma in Taiwan. J. Hepatol.75, 132–141 (2021). PubMed Google Scholar
Kudo, M. et al. Management of hepatocellular carcinoma in Japan: JSH consensus statements and recommendations 2021 update. Liver Cancer10, 181–223 (2021). CASPubMedPubMed Central Google Scholar
Toyoda, H. et al. Outcome of hepatocellular carcinoma detected during surveillance: comparing USA and Japan. Clin. Gastroenterol. Hepatol.19, 2379–2388.e6 (2021). PubMed Google Scholar
Johnson, P. et al. Impact of disease stage and aetiology on survival in hepatocellular carcinoma: implications for surveillance. Br. J. Cancer116, 441–447 (2017). PubMedPubMed Central Google Scholar
Kuo, S.-C. et al. Optimal intervals of ultrasonography screening for early diagnosis of hepatocellular carcinoma in Taiwan. JAMA Netw. Open4, e2114680 (2021). PubMedPubMed Central Google Scholar
Alqahtani, S. A. et al. Poor awareness of liver disease among adults with NAFLD in the United States. Hepatol. Commun.5, 1833–1847 (2021). PubMedPubMed Central Google Scholar
Finberg, H. J. Whither (wither?) the ultrasound specialist? J. Ultrasound Med.23, 1543–1547 (2004). PubMed Google Scholar
Fetzer, D. T., Browning, T., Xi, Y., Yokoo, T. & Singal, A. G. Associations of ultrasound LI-RADS visualization score with examination, sonographer, and radiologist factors: retrospective assessment in over 10,000 examinations. AJR Am. J. Roentgenol.218, 1010–1020 (2022). PubMed Google Scholar
Parikh, N. D., Tayob, N. & Singal, A. G. Blood-based biomarkers for hepatocellular carcinoma screening: approaching the end of the ultrasound era? J. Hepatol.78, 207–216 (2023). CASPubMed Google Scholar
Oka, H., Tamori, A., Kuroki, T., Kobayashi, K. & Yamamoto, S. Prospective study of α-fetoprotein in cirrhotic patients monitored for development of hepatocellular carcinoma. Hepatology19, 61–66 (1994). CASPubMed Google Scholar
Lok, A. S. et al. Des-γ-carboxy prothrombin and α-fetoprotein as biomarkers for the early detection of hepatocellular carcinoma. Gastroenterology138, 493–502 (2010). CASPubMed Google Scholar
Marrero, J. A. et al. α-Fetoprotein, des-γ carboxyprothrombin, and lectin-bound α-fetoprotein in early hepatocellular carcinoma. Gastroenterology137, 110–118 (2009). CASPubMed Google Scholar
Singal, A. G. et al. GALAD demonstrates high sensitivity for HCC surveillance in a cohort of patients with cirrhosis. Hepatology75, 541–549 (2022). CASPubMed Google Scholar
Kumada, T. et al. High-sensitivity Lens culinaris agglutinin-reactive alpha-fetoprotein assay predicts early detection of hepatocellular carcinoma. J. Gastroenterol.49, 555–563 (2014). CASPubMed Google Scholar
Tayob, N., Kanwal, F., Alsarraj, A., Hernaez, R. & El-Serag, H. B. The performance of AFP, AFP-3, DCP as biomarkers for detection of hepatocellular carcinoma (HCC): a phase 3 biomarker study in the United States. Clin. Gastroenterol. Hepatol.21, 415–423 (2023). CASPubMed Google Scholar
Toyoda, H. et al. Staging hepatocellular carcinoma by a novel scoring system (BALAD score) based on serum markers. Clin. Gastroenterol. Hepatol.4, 1528–1536 (2006). CASPubMed Google Scholar
Fox, R. et al. Biomarker-based prognosis in hepatocellular carcinoma: validation and extension of the BALAD model. Br. J. Cancer110, 2090–2098 (2014). CASPubMedPubMed Central Google Scholar
Singal, A. G. et al. Doylestown plus and GALAD demonstrate high sensitivity for HCC detection in patients with cirrhosis. Clin. Gastroenterol. Hepatol.20, 953–955.e2 (2022). CASPubMed Google Scholar
Tayob, N. et al. Validation of the updated hepatocellular carcinoma early detection screening algorithm in a community-based cohort of patients with cirrhosis of multiple etiologies. Clin. Gastroenterol. Hepatol.19, 1443–1450.e6 (2021). CASPubMed Google Scholar
Chalasani, N. P. et al. Validation of a novel multitarget blood test shows high sensitivity to detect early stage hepatocellular carcinoma. Clin. Gastroenterol. Hepatol.20, 173–182.e7 (2022). CASPubMed Google Scholar
Lin, N. et al. A multi-analyte cell-free DNA-based blood test for early detection of hepatocellular carcinoma. Hepatol. Commun.6, 1753–1763 (2022). CASPubMedPubMed Central Google Scholar
Sun, N. et al. HCC EV ECG score: an extracellular vesicle-based protein assay for detection of early-stage hepatocellular carcinoma. Hepatology77, 774–788 (2023). PubMed Google Scholar
Singal, A. G. et al. International Liver Cancer Association (ILCA) white paper on biomarker development for hepatocellular carcinoma. Gastroenterology160, 2572–2584 (2021). PubMed Google Scholar
Johnson, P., Zhou, Q., Dao, D. Y. & Lo, Y. M. D. Circulating biomarkers in the diagnosis and management of hepatocellular carcinoma. Nat. Rev. Gastroenterol. Hepatol.19, 670–681 (2022). PubMed Google Scholar
Lee, Y. T., Fujiwara, N., Yang, J. D. & Hoshida, Y. Risk stratification and early detection biomarkers for precision HCC screening. Hepatology78, 319–362 (2022). PubMed Google Scholar
Kim, S. Y. et al. MRI with liver-specific contrast for surveillance of patients with cirrhosis at high risk of hepatocellular carcinoma. JAMA Oncol.3, 456–463 (2017). PubMedPubMed Central Google Scholar
Roberts, L. R. et al. Imaging for the diagnosis of hepatocellular carcinoma: a systematic review and meta-analysis. Hepatology67, 401–421 (2018). PubMed Google Scholar
An, J. Y. et al. Abbreviated MRI for hepatocellular carcinoma screening and surveillance. Radiographics40, 1916–1931 (2020). PubMed Google Scholar
Gupta, P. et al. Abbreviated MRI for hepatocellular carcinoma screening: a systematic review and meta-analysis. J. Hepatol.75, 108–119 (2021). PubMed Google Scholar
Park, H. J. et al. Abbreviated magnetic resonance imaging vs. ultrasound for surveillance of hepatocellular carcinoma in high-risk patients. Liver Int.42, 2080–2092 (2021). PubMed Google Scholar
GBD 2017 Cirrhosis Collaborators. The global, regional, and national burden of cirrhosis by cause in 195 countries and territories, 1990-2017: a systematic analysis for the global burden of disease study 2017. Lancet Gastroenterol. Hepatol.5, 245–266 (2020). Google Scholar
Mohammed, H. A. et al. Factors influencing surveillance for hepatocellular carcinoma in patients with liver cirrhosis. Liver Cancer6, 126–136 (2017). Google Scholar
Signorelli, I. V. et al. Socioeconomic disparities in access to a hepatocellular carcinoma screening program in Brazil. Clinics71, 361–364 (2016). PubMedPubMed Central Google Scholar
Palmer, L. B., Kappelman, M. D., Sandler, R. S. & Hayashi, P. H. Surveillance for hepatocellular carcinoma in a Medicaid cirrhotic population. J. Clin. Gastroenterol.47, 713–718 (2013). PubMedPubMed Central Google Scholar
Singal, A. G., Tiro, J., Li, X., Adams-Huet, B. & Chubak, J. Hepatocellular carcinoma surveillance among patients with cirrhosis in a population-based integrated health care delivery system. J. Clin. Gastroenterol.51, 650–655 (2017). CASPubMedPubMed Central Google Scholar
Chang, S. S. et al. Factors associated with nonadherence to surveillance for hepatocellular carcinoma among patients with hepatic C virus cirrhosis, 2000-2015. Medicine101, e31907 (2022). PubMedPubMed Central Google Scholar
Goldberg, D. S. et al. Hepatocellular carcinoma surveillance rates in commercially insured patients with noncirrhotic chronic hepatitis B. J. Viral Hepat.22, 727–736 (2015). CASPubMedPubMed Central Google Scholar
Tran, S., Jeong, D., Henry, L., Cheung, R. C. & Nguyen, M. H. Initial evaluation, long-term monitoring, and hepatocellular carcinoma surveillance of chronic hepatitis B in routine practice: a nationwide US study. Am. J. Gastroenterol.116, 1885–1895 (2021). PubMed Google Scholar
Lazarus, J. V. et al. Advancing the global public health agenda for NAFLD: a consensus statement. Nat. Rev. Gastroenterol. Hepatol.19, 60–78 (2021). PubMed Google Scholar