Evolution from WHO to EASL and mRECIST for hepatocellular carcinoma: considerations for tumor response assessment

References

• Ferlay J, Shin HR, Bray F, et al. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 2010;127(12):2893-917
   PubMed Web of Science ®Google Scholar
• Sherman M. Hepatocellular carcinoma: epidemiology, surveillance, and diagnosis. Semin Liver Dis 2010;30(1):3-16
   PubMed Web of Science ®Google Scholar
• Lau WY, Lai EC. Hepatocellular carcinoma: current management and recent advances. Hepatobiliary Pancreat Dis Int 2008;7(3):237-57
   PubMed Web of Science ®Google Scholar
• Cabibbo G, Craxi A. Hepatocellular cancer: optimal strategies for screening and surveillance. Dig Dis 2009;27(2):142-7
   PubMed Web of Science ®Google Scholar
• Shields A, Reddy KR. Hepatocellular carcinoma: current treatment strategies. Curr Treat Options Gastroenterol 2005;8(6):457-66
   PubMedGoogle Scholar
• Llovet JM, Bruix J. Systematic review of randomized trials for unresectable hepatocellular carcinoma: chemoembolization improves survival. Hepatology 2003;37(2):429-42
   PubMed Web of Science ®Google Scholar
• Llovet JM, Ricci S, Mazzaferro V, et al. Sorafenib in advanced hepatocellular carcinoma. N Engl J Med 2008;359(4):378-90
   PubMed Web of Science ®Google Scholar
• Cheng AL, Kang YK, Chen Z, et al. Efficacy and safety of sorafenib in patients in the Asia-Pacific region with advanced hepatocellular carcinoma: a phase III randomised, double-blind, placebo-controlled trial. Lancet Oncol 2009;10(1):25-34
   PubMed Web of Science ®Google Scholar
• Takayasu K, Arii S, Ikai I, et al. Prospective cohort study of transarterial chemoembolization for unresectable hepatocellular carcinoma in 8510 patients. Gastroenterology 2006;131(2):461-9
   PubMed Web of Science ®Google Scholar
• Lau WY, Ho S, Leung TW, et al. Selective internal radiation therapy for nonresectable hepatocellular carcinoma with intraarterial infusion of 90yttrium microspheres. Int J Radiat Oncol Biol Phys 1998;40(3):583-92
   PubMed Web of Science ®Google Scholar
• Salem R, Lewandowski RJ, Mulcahy MF, et al. Radioembolization for hepatocellular carcinoma using Yttrium-90 microspheres: a comprehensive report of long-term outcomes. Gastroenterology 2010;138(1):52-64
   PubMed Web of Science ®Google Scholar
• Schuetze SM, Baker LH, Benjamin RS, Canetta R. Selection of response criteria for clinical trials of sarcoma treatment. Oncologist 2008;13(Suppl 2):32-40
   PubMedGoogle Scholar
• Miller AB, Hoogstraten B, Staquet M, Winkler A. Reporting results of cancer treatment. Cancer 1981;47(1):207-14
   PubMed Web of Science ®Google Scholar
• Therasse P, Arbuck SG, Eisenhauer EA, et al. New guidelines to evaluate the response to treatment in solid tumors. European Organization for Research and Treatment of Cancer, National Cancer Institute of the United States, National Cancer Institute of Canada. J Natl Cancer Inst 2000;92(3):205-16
   PubMed Web of Science ®Google Scholar
• Bruix J, Sherman M, Llovet JM, et al. Clinical management of hepatocellular carcinoma. Conclusions of the Barcelona-2000 EASL conference. European Association for the Study of the Liver. J Hepatol 2001;35(3):421-30
   PubMed Web of Science ®Google Scholar
• Lencioni R, Llovet JM. Modified RECIST (mRECIST) assessment for hepatocellular carcinoma. Semin Liver Dis 2010;30(1):52-60
   PubMed Web of Science ®Google Scholar
• Llovet JM, Di Bisceglie AM, Bruix J, et al. Design and endpoints of clinical trials in hepatocellular carcinoma. J Natl Cancer Inst 2008;100(10):698-711
   PubMedGoogle Scholar
• Warr D, McKinney S, Tannock I. Influence of measurement error on assessment of response to anticancer chemotherapy: proposal for new criteria of tumor response. J Clin Oncol 1984;2(9):1040-6
   PubMed Web of Science ®Google Scholar
• Eisenhauer EA, Therasse P, Bogaerts J, et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer 2009;45(2):228-47
   PubMed Web of Science ®Google Scholar
• Bogaerts J, Ford R, Sargent D, et al. Individual patient data analysis to assess modifications to the RECIST criteria. Eur J Cancer 2009;45(2):248-60
   PubMed Web of Science ®Google Scholar
• Moskowitz CS, Jia X, Schwartz LH, Gonen M. A simulation study to evaluate the impact of the number of lesions measured on response assessment. Eur J Cancer 2009;45(2):300-10
   PubMed Web of Science ®Google Scholar
• Varela M, Real MI, Burrel M, et al. Chemoembolization of hepatocellular carcinoma with drug eluting beads: efficacy and doxorubicin pharmacokinetics. J Hepatol 2007;46(3):474-81
   PubMed Web of Science ®Google Scholar
• Sato K, Lewandowski RJ, Bui JT, et al. Treatment of unresectable primary and metastatic liver cancer with yttrium-90 microspheres (TheraSphere): assessment of hepatic arterial embolization. Cardiovasc Intervent Radiol 2006;29(4):522-9
   PubMed Web of Science ®Google Scholar
• Lencioni R, Cioni D, Crocetti L, et al. Early-stage hepatocellular carcinoma in patients with cirrhosis: long-term results of percutaneous image-guided radiofrequency ablation. Radiology 2005;234(3):961-7
   PubMed Web of Science ®Google Scholar
• Sala M, Llovet JM, Vilana R, et al. Initial response to percutaneous ablation predicts survival in patients with hepatocellular carcinoma. Hepatology 2004;40(6):1352-60
   PubMed Web of Science ®Google Scholar
• Llovet JM, Real MI, Montana X, et al. Arterial embolisation or chemoembolisation versus symptomatic treatment in patients with unresectable hepatocellular carcinoma: a randomised controlled trial. Lancet 2002;359(9319):1734-9
   PubMed Web of Science ®Google Scholar
• Bruix J, Sherman M. Management of hepatocellular carcinoma. Hepatology 2005;42(5):1208-36
   PubMed Web of Science ®Google Scholar
• EASL-EORTC clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol 2012;56(4):908-43
   PubMed Web of Science ®Google Scholar
• Memon K, Kulik L, Lewandowski RJ, et al. Radiographic response to locoregional therapy in hepatocellular carcinoma predicts patient survival times. Gastroenterology 2011;141(2):526-35; 535 e521-522
   PubMed Web of Science ®Google Scholar
• Forner A, Ayuso C, Varela M, et al. Evaluation of tumor response after locoregional therapies in hepatocellular carcinoma: are response evaluation criteria in solid tumors reliable? Cancer 2009;115(3):616-23
   PubMed Web of Science ®Google Scholar
• Riaz A, Memon K, Miller FH, et al. Role of the EASL, RECIST, and WHO response guidelines alone or in combination for hepatocellular carcinoma: radiologic-pathologic correlation. J Hepatol 2011;54(4):695-704
   PubMed Web of Science ®Google Scholar
• Sato Y, Watanabe H, Sone M, et al. Tumor response evaluation criteria for HCC (hepatocellular carcinoma) treated using TACE (transcatheter arterial chemoembolization): RECIST (response evaluation criteria in solid tumors) version 1.1 and mRECIST (modified RECIST): JIVROSG-0602. Ups J Med Sci 2013;118(1):16-22
   PubMed Web of Science ®Google Scholar
• Edeline J, Boucher E, Rolland Y, et al. Comparison of tumor response by Response Evaluation Criteria in Solid Tumors (RECIST) and modified RECIST in patients treated with sorafenib for hepatocellular carcinoma. Cancer 2012;118(1):147-56
   PubMed Web of Science ®Google Scholar
• Salvaggio G, Furlan A, Agnello F, et al. Hepatocellular carcinoma enhancement on contrast-enhanced CT and MR imaging: response assessment after treatment with sorafenib: preliminary results. Radiol Med 2014;119(4):215-21
   PubMed Web of Science ®Google Scholar
• Gillmore R, Stuart S, Kirkwood A, et al. EASL and mRECIST responses are independent prognostic factors for survival in hepatocellular cancer patients treated with transarterial embolization. J Hepatol 2011;55(6):1309-16
   PubMed Web of Science ®Google Scholar
• Shim JH, Lee HC, Kim SO, et al. Which response criteria best help predict survival of patients with hepatocellular carcinoma following chemoembolization? A validation study of old and new models. Radiology 2012;262(2):708-18
   PubMed Web of Science ®Google Scholar
• Jung ES, Kim JH, Yoon EL, et al. Comparison of the methods for tumor response assessment in patients with hepatocellular carcinoma undergoing transarterial chemoembolization. J Hepatol 2013;58(6):1181-7
   PubMed Web of Science ®Google Scholar
• Liu L, Wang W, Chen H, et al. EASL- and mRECIST-Evaluated Responses to Combination Therapy of Sorafenib with Transarterial Chemoembolization Predict Survival in Patients with Hepatocellular Carcinoma. Clin Cancer Res 2014;20(6):1623-31
   PubMed Web of Science ®Google Scholar
• Kim BK, Kim KA, Park JY, et al. Prospective comparison of prognostic values of modified response evaluation criteria in solid tumours with European Association for the Study of the Liver criteria in hepatocellular carcinoma following chemoembolisation. Eur J Cancer 2013;49(4):826-34
   PubMed Web of Science ®Google Scholar
• Georgiades C, Geschwind JF, Harrison N, et al. Lack of response after initial chemoembolization for hepatocellular carcinoma: does it predict failure of subsequent treatment? Radiology 2012;265(1):115-23
   PubMed Web of Science ®Google Scholar
• Sieghart W, Hucke F, Pinter M, et al. The ART of decision making: retreatment with transarterial chemoembolization in patients with hepatocellular carcinoma. Hepatology 2013;57(6):2261-73
   PubMed Web of Science ®Google Scholar
• Choi J, Shim JH, Shin YM, et al. Clinical significance of the best response during repeated transarterial chemoembolization in the treatment of hepatocellular carcinoma. J Hepatol 2014;60(6):1212-18
   PubMed Web of Science ®Google Scholar
• Riaz A, Miller FH, Kulik LM, et al. Imaging response in the primary index lesion and clinical outcomes following transarterial locoregional therapy for hepatocellular carcinoma. JAMA 2010;303(11):1062-9
   PubMed Web of Science ®Google Scholar
• Shim JH, Lee HC, Won HJ, et al. Maximum number of target lesions required to measure responses to transarterial chemoembolization using the enhancement criteria in patients with intrahepatic hepatocellular carcinoma. J Hepatol 2012;56(2):406-11
   PubMed Web of Science ®Google Scholar
• Kim BK, Kim SU, Kim MJ, et al. Number of target lesions for EASL and modified RECIST to predict survivals in hepatocellular carcinoma treated with chemoembolization. Clin Cancer Res 2013;19(6):1503-11
   PubMed Web of Science ®Google Scholar
• Raoul JL, Sangro B, Forner A, et al. Evolving strategies for the management of intermediate-stage hepatocellular carcinoma: available evidence and expert opinion on the use of transarterial chemoembolization. Cancer Treat Rev 2011;37(3):212-20
   PubMed Web of Science ®Google Scholar
• Hucke F, Sieghart W, Pinter M, et al. The ART-strategy: sequential assessment of the ART score predicts outcome of patients with hepatocellular carcinoma re-treated with TACE. J Hepatol 2014;60(1):118-26
   PubMed Web of Science ®Google Scholar
• Choi H. Response evaluation of gastrointestinal stromal tumors. Oncologist 2008;13(Suppl 2):4-7
   PubMed Web of Science ®Google Scholar
• Stroobants S, Goeminne J, Seegers M, et al. 18FDG-Positron emission tomography for the early prediction of response in advanced soft tissue sarcoma treated with imatinib mesylate (Glivec). Eur J cancer 2003;39(14):2012-20
   PubMed Web of Science ®Google Scholar
• Antoch G, Kanja J, Bauer S, et al. Comparison of PET, CT, and dual-modality PET/CT imaging for monitoring of imatinib (STI571) therapy in patients with gastrointestinal stromal tumors. J Nucl Med 2004;45(3):357-65
   PubMed Web of Science ®Google Scholar
• Choi H, Charnsangavej C, Faria SC, et al. Correlation of computed tomography and positron emission tomography in patients with metastatic gastrointestinal stromal tumor treated at a single institution with imatinib mesylate: proposal of new computed tomography response criteria. J Clin Oncol 2007;25(13):1753-9
   PubMed Web of Science ®Google Scholar
• Benjamin RS, Choi H, Macapinlac HA, et al. We should desist using RECIST, at least in GIST. J Clin Oncol 2007;25(13):1760-4
   PubMed Web of Science ®Google Scholar
• Ronot M, Bouattour M, Wassermann J, et al. Alternative response criteria (Choi, European Association for the Study of the Liver, and Modified Response Evaluation Criteria in Solid Tumors [RECIST]) versus RECIST 1.1 in patients with advanced hepatocellular carcinoma treated with sorafenib. Oncologist 2014;19(4):394-402
   PubMed Web of Science ®Google Scholar
• Faivre S, Zappa M, Vilgrain V, et al. Changes in tumor density in patients with advanced hepatocellular carcinoma treated with sunitinib. Clin Cancer Res 2011;17(13):4504-12
   PubMed Web of Science ®Google Scholar
• Yeo DM, Choi JI, Lee YJ, et al. Comparison of RECIST, mRECIST, and Choi criteria for early response evaluation of hepatocellular carcinoma after transarterial chemoembolization using drug-eluting beads. J Comput Assist Tomogr 2014;38(3):391-7
   PubMed Web of Science ®Google Scholar
• Weng Z, Ertle J, Zheng S, et al. Choi criteria are superior in evaluating tumor response in patients treated with transarterial radioembolization for hepatocellular carcinoma. Oncol Lett 2013;6(6):1707-12
   PubMed Web of Science ®Google Scholar
• Torizuka T, Tamaki N, Inokuma T, et al. Value of fluorine-18-FDG-PET to monitor hepatocellular carcinoma after interventional therapy. J Nucl Med 1994;35(12):1965-9
   PubMed Web of Science ®Google Scholar
• Paudyal B, Oriuchi N, Paudyal P, et al. Early diagnosis of recurrent hepatocellular carcinoma with 18F-FDG PET after radiofrequency ablation therapy. Oncol Rep 2007;18(6):1469-73
   PubMed Web of Science ®Google Scholar
• Higashi T, Hatano E, Ikai I, et al. FDG PET as a prognostic predictor in the early post-therapeutic evaluation for unresectable hepatocellular carcinoma. Eur J Nucl Med Mol Imaging 2010;37(3):468-82
   PubMed Web of Science ®Google Scholar
• Wahl RL, Jacene H, Kasamon Y, Lodge MA. From RECIST to PERCIST: evolving Considerations for PET response criteria in solid tumors. J Nucl Med 2009;50(Suppl 1):122S-50S
   PubMed Web of Science ®Google Scholar
• Kubota K, Yamanishi T, Itoh S, et al. Role of diffusion-weighted imaging in evaluating therapeutic efficacy after transcatheter arterial chemoembolization for hepatocellular carcinoma. Oncol Rep 2010;24(3):727-32
   PubMed Web of Science ®Google Scholar
• Dong S, Ye XD, Yuan Z, et al. Relationship of apparent diffusion coefficient to survival for patients with unresectable primary hepatocellular carcinoma after chemoembolization. Eur J Radiol 2012;81(3):472-7
   PubMed Web of Science ®Google Scholar
• Vandecaveye V, Michielsen K, De Keyzer F, et al. Chemoembolization for hepatocellular carcinoma: 1-month response determined with apparent diffusion coefficient is an independent predictor of outcome. Radiology 2014;270(3):747-57
   PubMed Web of Science ®Google Scholar
• Lee YK, Kim SU, Kim do Y, et al. Prognostic value of alpha-fetoprotein and des-gamma-carboxy prothrombin responses in patients with hepatocellular carcinoma treated with transarterial chemoembolization. BMC Cancer 2013;13:5
   PubMed Web of Science ®Google Scholar
• Arai T, Kobayashi A, Ohya A, et al. Assessment of treatment outcomes based on tumor marker trends in patients with recurrent hepatocellular carcinoma undergoing trans-catheter arterial chemo-embolization. Int J Clin Oncol 2013. [Epub ahead of print]
   Web of Science ®Google Scholar
• Kawaoka T, Aikata H, Murakami E, et al. Evaluation of the mRECIST and alpha-fetoprotein ratio for stratification of the prognosis of advanced-hepatocellular-carcinoma patients treated with sorafenib. Oncology 2012;83(4):192-200
   PubMed Web of Science ®Google Scholar
• Personeni N, Bozzarelli S, Pressiani T, et al. Usefulness of alpha-fetoprotein response in patients treated with sorafenib for advanced hepatocellular carcinoma. J Hepatol 2012;57(1):101-7
   PubMed Web of Science ®Google Scholar