Assessment of liver tumor response to therapy: role of quantitative imaging.

Quantitative imaging is the analysis of retrieved numeric data from images with the goal of reducing subjective assessment. It is an increasingly important radiologic tool to assess treatment response in oncology patients. Quantification of response to therapy depends on the tumor type and method of treatment. Anatomic imaging biomarkers that quantify liver tumor response to cytotoxic therapy are based on temporal change in the size of the tumors. Anatomic biomarkers have been incorporated into the World Health Organization criteria and the Response Evaluation Criteria in Solid Tumors (RECIST) versions 1.0 and 1.1. However, the development of novel therapies with different mechanisms of action, such as antiangiogenesis or radioembolization, has required new methods for measuring response to therapy. This need has led to development of tumor- or therapy-specific guidelines such as the Modified CT Response Evaluation (Choi) Criteria for gastrointestinal stromal tumors, the European Association for Study of the Liver (EASL) criteria, and modified RECIST for hepatocellular carcinoma, among many others. The authors review the current quantification criteria used in the evaluation of treatment response in liver tumors, summarizing their indications, advantages, and disadvantages, and discuss future directions with newer methods that have the potential for assessment of treatment response. Knowledge of these quantitative methods is important to facilitate pivotal communication between oncologists and radiologists about cancer treatment, with benefit ultimately accruing to the patient.

[1]  M. Makuuchi,et al.  Response Evaluation Criteria in Cancer of the Liver (RECICL) proposed by the Liver Cancer Study Group of Japan (2009 Revised Version) , 2010, Hepatology research : the official journal of the Japan Society of Hepatology.

[2]  W. Peng,et al.  In vivo 1H magnetic resonance spectroscopy in evaluation of hepatocellular carcinoma and its early response to transcatheter arterial chemoembolization. , 2006, Chinese medical sciences journal = Chung-kuo i hsueh k'o hsueh tsa chih.

[3]  M. Yoshikawa,et al.  Comparison of CT findings with resected specimens after chemoembolization with iodized oil for hepatocellular carcinoma. , 2000, AJR. American journal of roentgenology.

[4]  J. Lee,et al.  18F‐fluorodeoxyglucose uptake on positron emission tomography as a prognostic predictor in locally advanced hepatocellular carcinoma , 2011, Cancer.

[5]  A. Benson,et al.  Radiographic response to locoregional therapy in hepatocellular carcinoma predicts patient survival times. , 2011, Gastroenterology.

[6]  A. Krasnow,et al.  Positron emission tomography for staging and assessment of tumor response of hepatic malignancies. , 2006, Seminars in interventional radiology.

[7]  M. van Glabbeke,et al.  New guidelines to evaluate the response to treatment in solid tumors , 2000, Journal of the National Cancer Institute.

[8]  L. Schwartz,et al.  New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). , 2009, European journal of cancer.

[9]  Vahid Yaghmai,et al.  Hepatic tumors: region-of-interest versus volumetric analysis for quantification of attenuation at CT. , 2012, Radiology.

[10]  A. Chandler,et al.  Reproducibility of CT perfusion parameters in liver tumors and normal liver. , 2011, Radiology.

[11]  Armando Manduca,et al.  Review of MR elastography applications and recent developments , 2012, Journal of magnetic resonance imaging : JMRI.

[12]  R. Wahl,et al.  From RECIST to PERCIST: Evolving Considerations for PET Response Criteria in Solid Tumors , 2009, Journal of Nuclear Medicine.

[13]  J. Bloem,et al.  RECIST revised: implications for the radiologist. A review article on the modified RECIST guideline , 2009, European Radiology.

[14]  Y. Kuo,et al.  In vivo proton magnetic resonance spectroscopy of large focal hepatic lesions and metabolite change of hepatocellular carcinoma before and after transcatheter arterial chemoembolization using 3.0‐T MR scanner , 2004, Journal of magnetic resonance imaging : JMRI.

[15]  Tim Meyer,et al.  EASL and mRECIST responses are independent prognostic factors for survival in hepatocellular cancer patients treated with transarterial embolization. , 2011, Journal of hepatology.

[16]  Y. Shin,et al.  Which response criteria best help predict survival of patients with hepatocellular carcinoma following chemoembolization? A validation study of old and new models. , 2012, Radiology.

[17]  K. Mekeel,et al.  Consensus and controversy in the management of hepatocellular carcinoma. , 2007, Journal of the American College of Surgeons.

[18]  R. D. Hunter,et al.  WHO Handbook for Reporting Results of Cancer Treatment , 1980 .

[19]  L. Schwartz,et al.  A theoretical approach to choosing the minimum number of multiple tumors required for assessing treatment response. , 2005, Journal of clinical epidemiology.

[20]  R. Reznek,et al.  CT assessment of tumour response to treatment: comparison of linear, cross-sectional and volumetric measures of tumour size. , 2000, The British journal of radiology.

[21]  D. Bluemke,et al.  Functional MR imaging assessment of tumor response after 90Y microsphere treatment in patients with unresectable hepatocellular carcinoma. , 2007, Journal of vascular and interventional radiology : JVIR.

[22]  J. Babb,et al.  Prediction of growth rate of solid renal masses: utility of MR imaging features--preliminary experience. , 2012, Radiology.

[23]  Vahid Yaghmai,et al.  Evaluation of hepatocellular carcinoma size using two-dimensional and volumetric analysis: effect on liver transplantation eligibility. , 2011, Academic radiology.

[24]  P. Prassopoulos,et al.  Treatment response classification of liver metastatic disease evaluated on imaging. Are RECIST unidimensional measurements accurate? , 2009, European Radiology.

[25]  Riccardo Lencioni,et al.  Modified RECIST (mRECIST) Assessment for Hepatocellular Carcinoma , 2010, Seminars in liver disease.

[26]  Jordi Rimola,et al.  Evaluation of tumor response after locoregional therapies in hepatocellular carcinoma , 2009, Cancer.

[27]  Vahid Yaghmai,et al.  Radiologic assessment of response to therapy: comparison of RECIST Versions 1.1 and 1.0. , 2011, Radiographics : a review publication of the Radiological Society of North America, Inc.

[28]  Y. Rolland,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 , 2012, Cancer.

[29]  A. D. Van den Abbeele,et al.  Revised RECIST guideline version 1.1: What oncologists want to know and what radiologists need to know. , 2010, AJR. American journal of roentgenology.

[30]  D. Tuveson,et al.  Effect of the tyrosine kinase inhibitor STI571 in a patient with a metastatic gastrointestinal stromal tumor. , 2001, The New England journal of medicine.

[31]  H. Rhim,et al.  Spectrum of CT findings after radiofrequency ablation of hepatic tumors. , 2008, Radiographics : a review publication of the Radiological Society of North America, Inc.

[32]  D. Bluemke,et al.  Role of diffusion-weighted imaging in estimating tumor necrosis after chemoembolization of hepatocellular carcinoma. , 2003, AJR. American journal of roentgenology.

[33]  C. Claussen,et al.  Diffusion-weighted MRI of advanced hepatocellular carcinoma during sorafenib treatment: initial results. , 2009, AJR. American journal of roentgenology.

[34]  Dieter Häussinger,et al.  Sorafenib in advanced hepatocellular carcinoma. , 2008, The New England journal of medicine.

[35]  E. Halpern,et al.  CT tumor measurement for therapeutic response assessment: comparison of unidimensional, bidimensional, and volumetric techniques initial observations. , 2002, Radiology.

[36]  D. Choi,et al.  Hepatocellular carcinoma treated with percutaneous radio-frequency ablation: evaluation with follow-up multiphase helical CT. , 2001, Radiology.

[37]  Keiko Miyazaki,et al.  Neuroendocrine tumor liver metastases: use of dynamic contrast-enhanced MR imaging to monitor and predict radiolabeled octreotide therapy response. , 2012, Radiology.

[38]  Wen He,et al.  Computed tomography perfusion in evaluating the therapeutic effect of transarterial chemoembolization for hepatocellular carcinoma. , 2008, World journal of gastroenterology.

[39]  L. Klotz,et al.  Growth kinetics of renal masses: analysis of a prospective cohort of patients undergoing active surveillance. , 2011, European urology.

[40]  D. Sahani,et al.  Established and novel imaging biomarkers for assessing response to therapy in hepatocellular carcinoma. , 2013, Journal of hepatology.

[41]  Rebecca M. Lindell,et al.  Five-year lung cancer screening experience: CT appearance, growth rate, location, and histologic features of 61 lung cancers. , 2007, Radiology.

[42]  Axel Hoos,et al.  Guidelines for the Evaluation of Immune Therapy Activity in Solid Tumors: Immune-Related Response Criteria , 2009, Clinical Cancer Research.

[43]  A. Qayyum,et al.  MR spectroscopy of the liver: principles and clinical applications. , 2009, Radiographics : a review publication of the Radiological Society of North America, Inc.

[44]  L Pagliaro,et al.  Clinical management of hepatocellular carcinoma. Conclusions of the Barcelona-2000 EASL conference. European Association for the Study of the Liver. , 2001, Journal of hepatology.

[45]  J. Bruix,et al.  Molecular targeted therapies in hepatocellular carcinoma , 2008, Hepatology.

[46]  R. Salem,et al.  Does multidetector CT attenuation change in colon cancer liver metastases treated with 90Y help predict metabolic activity at FDG PET? , 2010, Radiology.

[47]  John M Buatti,et al.  Comparison of response evaluation criteria in solid tumors with volumetric measurements for estimation of tumor burden in pancreatic adenocarcinoma and hepatocellular carcinoma. , 2012, American journal of surgery.

[48]  Mickael Tanter,et al.  Viscoelastic shear properties of in vivo breast lesions measured by MR elastography. , 2005, Magnetic resonance imaging.

[49]  A. Padhani,et al.  Diffusion MR imaging for monitoring of treatment response. , 2011, Magnetic resonance imaging clinics of North America.

[50]  Myeong-Jin Kim,et al.  Response evaluation in patients with colorectal liver metastases: RECIST version 1.1 versus modified CT criteria. , 2012, AJR. American journal of roentgenology.

[51]  V. Goh,et al.  CT perfusion in oncologic imaging: a useful tool? , 2013, AJR. American journal of roentgenology.

[52]  Celia P. Corona-Villalobos,et al.  Intrahepatic cholangiocarcinoma treated with local-regional therapy: quantitative volumetric apparent diffusion coefficient maps for assessment of tumor response. , 2012, Radiology.

[53]  F. Zaccagna,et al.  Liver Metastases From Colorectal Cancer Treated With Conventional and Antiangiogenetic Chemotherapy: Evaluation With Liver Computed Tomography Perfusion and Magnetic Resonance Diffusion-Weighted Imaging , 2011, Journal of computer assisted tomography.

[54]  C. Claussen,et al.  Early MRI response monitoring of patients with advanced hepatocellular carcinoma under treatment with the multikinase inhibitor sorafenib , 2009, BMC Cancer.

[55]  Chiun Hsu,et al.  Dynamic contrast-enhanced magnetic resonance imaging biomarkers predict survival and response in hepatocellular carcinoma patients treated with sorafenib and metronomic tegafur/uracil. , 2011, Journal of hepatology.

[56]  Hirofumi Fujii,et al.  Radiologic measurements of tumor response to treatment: practical approaches and limitations. , 2008, Radiographics : a review publication of the Radiological Society of North America, Inc.

[57]  L. Schwartz,et al.  Imaging response assessment in oncology , 2006, Cancer imaging : the official publication of the International Cancer Imaging Society.

[58]  A. Chaudhari,et al.  Treatment Planning and Volumetric Response Assessment for Yttrium-90 Radioembolization: Semiautomated Determination of Liver Volume and Volume of Tumor Necrosis in Patients with Hepatic Malignancy , 2010, CardioVascular and Interventional Radiology.

[59]  Benoit Mory,et al.  Quantitative and volumetric European Association for the Study of the Liver and Response Evaluation Criteria in Solid Tumors measurements: feasibility of a semiautomated software method to assess tumor response after transcatheter arterial chemoembolization. , 2012, Journal of vascular and interventional radiology : JVIR.

[60]  A. Cucchetti,et al.  Hepatocellular carcinoma locoregional therapies for patients in the waiting list. Impact on transplantability and recurrence rate. , 2013, Journal of hepatology.

[61]  Tomy Varghese,et al.  Monitoring stiffness changes in lesions after radiofrequency ablation at different temperatures and durations of ablation. , 2005, Ultrasound in medicine & biology.

[62]  A. Manduca,et al.  Magnetic resonance elastography by direct visualization of propagating acoustic strain waves. , 1995, Science.

[63]  J. Bussink,et al.  Diffusion-weighted MR imaging in liver metastases of colorectal cancer: reproducibility and biological validation , 2013, European Radiology.

[64]  Namkug Kim,et al.  Malignant hepatic tumors: short-term reproducibility of apparent diffusion coefficients with breath-hold and respiratory-triggered diffusion-weighted MR imaging. , 2010, Radiology.

[65]  K. Gately,et al.  Clinical implication and prognostic significance of standardised uptake value of primary non-small cell lung cancer on positron emission tomography: analysis of 176 cases. , 2008, European journal of cardio-thoracic surgery : official journal of the European Association for Cardio-thoracic Surgery.

[66]  V. Paradis,et al.  Diffusion-weighted MR imaging for the regional characterization of liver tumors. , 2012, Radiology.

[67]  E. Eisenhauer,et al.  Review of phase II trial designs used in studies of molecular targeted agents: outcomes and predictors of success in phase III. , 2008, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[68]  Eric P Tamm,et al.  CT evaluation of the response of gastrointestinal stromal tumors after imatinib mesylate treatment: a quantitative analysis correlated with FDG PET findings. , 2004, AJR. American journal of roentgenology.

[69]  V. Goh,et al.  Novel oncologic drugs: what they do and how they affect images. , 2011, Radiographics : a review publication of the Radiological Society of North America, Inc.

[70]  S. Curley,et al.  Association of computed tomography morphologic criteria with pathologic response and survival in patients treated with bevacizumab for colorectal liver metastases. , 2009, JAMA.

[71]  Haesun Choi,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. , 2007, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[72]  H. Chalian,et al.  MDCT evaluation of the growth kinetics of serous and benign mucinous cystic neoplasms of the pancreas , 2011, Cancer imaging : the official publication of the International Cancer Imaging Society.

[73]  D. Collins,et al.  Advanced solid tumors treated with cediranib: comparison of dynamic contrast-enhanced MR imaging and CT as markers of vascular activity. , 2012, Radiology.

[74]  Zhengjia Chen,et al.  mRECIST and EASL responses at early time point by contrast-enhanced dynamic MRI predict survival in patients with unresectable hepatocellular carcinoma (HCC) treated by doxorubicin drug-eluting beads transarterial chemoembolization (DEB TACE). , 2013, Annals of oncology : official journal of the European Society for Medical Oncology.

[75]  F. Miller,et al.  Multimodality imaging following 90Y radioembolization: a comprehensive review and pictorial essay. , 2008, Radiographics : a review publication of the Radiological Society of North America, Inc.

[76]  K. Chayama,et al.  Evaluation of the mRECIST and α-Fetoprotein Ratio for Stratification of the Prognosis of Advanced-Hepatocellular-Carcinoma Patients Treated with Sorafenib , 2012, Oncology.