Imaging approach to hepatocellular carcinoma, cholangiocarcinoma, and metastatic colorectal cancer.

Liver imaging is a highly evolving field with new imaging contrast agents and modalities. Knowledge of the different imaging options and what they have to offer in primary and metastatic liver disease is essential for appropriate diagnosis, staging, and prognosis in patients. This review summarizes the major imaging modalities in liver neoplasms and provides specific discussion of imaging hepatocellular carcinoma, cholangiocarcinoma, and colorectal liver metastases. The final sections provide an overview of presurgical imaging relevant to planning hepatectomies and ablative procedures.

[1]  J. Vauthey,et al.  Uses and limitations of portal vein embolization for improving perioperative outcomes in hepatocellular carcinoma. , 2010, Seminars in oncology.

[2]  K. Okita,et al.  Management of hepatocellular carcinoma in Japan , 2006, Journal of Gastroenterology.

[3]  M. Ducreux,et al.  Evolution of missing colorectal liver metastases following inductive chemotherapy and hepatectomy , 2004, Journal of surgical oncology.

[4]  Christopher L Brace,et al.  Radiofrequency and microwave ablation of the liver, lung, kidney, and bone: what are the differences? , 2009, Current problems in diagnostic radiology.

[5]  J. Soto,et al.  Malignant hilar and perihilar biliary obstruction: use of MR cholangiography to define the extent of biliary ductal involvement and plan percutaneous interventions. , 2001, Radiology.

[6]  K. Abe,et al.  Gd-EOB-DTPA enhanced MRI for hepatocellular carcinoma: quantitative evaluation of tumor enhancement in hepatobiliary phase. , 2005, Magnetic resonance in medical sciences : MRMS : an official journal of Japan Society of Magnetic Resonance in Medicine.

[7]  Hirokazu Okada,et al.  Guidelines on the use of iodinated contrast media in patients with kidney disease 2012: digest version , 2013, Japanese Journal of Radiology.

[8]  Michael Laniado,et al.  Diagnostic efficacy of gadoxetic acid (Primovist)-enhanced MRI and spiral CT for a therapeutic strategy: comparison with intraoperative and histopathologic findings in focal liver lesions , 2008, European Radiology.

[9]  K. Bae,et al.  Intravenous contrast medium administration and scan timing at CT: considerations and approaches. , 2010, Radiology.

[10]  Steven A Curley,et al.  Extended hepatectomy in patients with hepatobiliary malignancies with and without preoperative portal vein embolization. , 2002, Archives of surgery.

[11]  F. Lammert,et al.  EASL Clinical Practice Guidelines: management of cholestatic liver diseases. , 2009, Journal of hepatology.

[12]  W. Chapman,et al.  Fluorodeoxyglucose PET imaging in the evaluation of gallbladder carcinoma and cholangiocarcinoma , 2007, Journal of Gastrointestinal Surgery.

[13]  G. Gores,et al.  Diagnosis and management of primary sclerosing cholangitis , 2010, Hepatology.

[14]  J. Ellis,et al.  Contrast material-induced nephrotoxicity and intravenous low-osmolality iodinated contrast material: risk stratification by using estimated glomerular filtration rate. , 2013, Radiology.

[15]  Osama Mawlawi,et al.  Multimodality imaging: an update on PET/CT technology , 2009, European Journal of Nuclear Medicine and Molecular Imaging.

[16]  T. Gruenberger,et al.  Preoperative detection of colorectal liver metastases in fatty liver: MDCT or MRI? , 2011, European journal of radiology.

[17]  J. Kellum,et al.  Risk factors for radiocontrast nephropathy after emergency department contrast-enhanced computerized tomography. , 2013, Academic emergency medicine : official journal of the Society for Academic Emergency Medicine.

[18]  T. Serrano,et al.  Preoperative Staging of Patients with Liver Metastases of Colorectal Carcinoma. Does PET/CT Really Add Something to Multidetector CT? , 2011, Annals of Surgical Oncology.

[19]  F. Rotellar,et al.  Laparoscopic staging in hilar cholangiocarcinoma: Is it still justified? , 2013, World journal of gastrointestinal oncology.

[20]  M. Büchler,et al.  [Surgical management of disappearing colorectal liver metastases]. , 2013, Der Chirurg; Zeitschrift fur alle Gebiete der operativen Medizen.

[21]  M. A. van den Bosch,et al.  Preoperative Imaging of Colorectal Liver Metastases After Neoadjuvant Chemotherapy: A Meta-Analysis , 2012, Annals of Surgical Oncology.

[22]  N. Ackerman,et al.  The blood supply of experimental liver metastases. I. The distribution of hepatic artery and portal vein blood to "small" and "large" tumors. , 1969, Surgery.

[23]  Steven G. Ross,et al.  Application and Evaluation of a Measured Spatially Variant System Model for PET Image Reconstruction , 2010, IEEE Transactions on Medical Imaging.

[24]  Hyeon Je Cho,et al.  Varying appearances of cholangiocarcinoma: radiologic-pathologic correlation. , 2009, Radiographics : a review publication of the Radiological Society of North America, Inc.

[25]  Masahiro Okada,et al.  Gd-EOB-DTPA-enhanced magnetic resonance images of hepatocellular carcinoma: correlation with histological grading and portal blood flow , 2010, European Radiology.

[26]  P. Malfertheiner,et al.  World Gastroenterology Organisation Guideline. Hepatocellular carcinoma (HCC): a global perspective. , 2010, Journal of gastrointestinal and liver diseases : JGLD.

[27]  H. Hussain,et al.  New OPTN/UNOS policy for liver transplant allocation: standardization of liver imaging, diagnosis, classification, and reporting of hepatocellular carcinoma. , 2013, Radiology.

[28]  A. Scarsbrook,et al.  Clinical impact of FDG PET-CT in patients with potentially operable metastatic colorectal cancer. , 2011, Clinical radiology.

[29]  F. Prat,et al.  Performance characteristics of magnetic resonance cholangiography in the staging of malignant hilar strictures , 2000, Gut.

[30]  Jeong Min Lee,et al.  Asian Pacific Association for the Study of the Liver consensus recommendations on hepatocellular carcinoma , 2010, Hepatology international.

[31]  B. I. Choi,et al.  Preoperative evaluation of Klatskin tumor: accuracy of spiral CT in determining vascular invasion as a sign of unresectability , 2000, Abdominal Imaging.

[32]  S. Curley,et al.  Hepatic insufficiency and mortality in 1,059 noncirrhotic patients undergoing major hepatectomy. , 2007, Journal of the American College of Surgeons.

[33]  C. Altehoefer,et al.  Breathhold unenhanced and gadolinium-enhanced magnetic resonance tomography and magnetic resonance cholangiography in hilar cholangiocarcinoma , 2001, International Journal of Colorectal Disease.

[34]  S. Tickoo,et al.  Combined hepatocellular and cholangiocarcinoma , 2002, Cancer.

[35]  Lihua Chen,et al.  Comparison of MRI with liver-specific contrast agents and multidetector row CT for the detection of hepatocellular carcinoma: a meta-analysis of 15 direct comparative studies , 2013, Gut.

[36]  T. Hwang,et al.  Malignant perihilar biliary obstruction: magnetic resonance cholangiopancreatographic findings , 2000, American Journal of Gastroenterology.

[37]  R. Freeman,et al.  Report of a national conference on liver allocation in patients with hepatocellular carcinoma in the United States , 2010, Liver transplantation : official publication of the American Association for the Study of Liver Diseases and the International Liver Transplantation Society.

[38]  N. Ackerman,et al.  The blood supply of experimental liver metastases. II. A microcirculatory study of the normal and tumor vessels of the liver with the use of perfused silicone rubber. , 1970, Surgery.

[39]  Jae Seung Kim,et al.  Clinical Role of 18F-FDG PET-CT in Suspected and Potentially Operable Cholangiocarcinoma: A Prospective Study Compared With Conventional Imaging , 2008, The American Journal of Gastroenterology.

[40]  John A Kellum,et al.  Acute Kidney Injury Network: report of an initiative to improve outcomes in acute kidney injury , 2007, Critical care.

[41]  Joon Koo Han,et al.  Gadoxetic Acid-Enhanced Magnetic Resonance Imaging for Differentiating Small Hepatocellular Carcinomas (≤2 cm in Diameter) From Arterial Enhancing Pseudolesions: Special Emphasis on Hepatobiliary Phase Imaging , 2010, Investigative radiology.

[42]  W. Jochum,et al.  Impact of integrated positron emission tomography and computed tomography on staging and management of gallbladder cancer and cholangiocarcinoma. , 2006, Journal of hepatology.

[43]  M. Gonen,et al.  Staging, Resectability, and Outcome in 225 Patients With Hilar Cholangiocarcinoma , 2001, Annals of surgery.

[44]  Carlo Catalano,et al.  Hepatocellular carcinoma in cirrhotic patients: prospective comparison of US, CT and MR imaging , 2013, European Radiology.

[45]  J. Bruix,et al.  Management of hepatocellular carcinoma: An update , 2011, Hepatology.

[46]  P. Mittal,et al.  Liver Imaging Reporting and Data System LI-RADS v2014 - A Pictorial Review of the Categories on CT and MRI , 2017 .

[47]  N. Ackerman,et al.  The blood supply of experimental liver metastases. V. Increased tumor perfusion with epinephrine. , 1980, American journal of surgery.

[48]  Antonio Rodríguez-Fernández,et al.  Fluorine-18 fluorodeoxyglucose PET in the preoperative staging of colorectal cancer , 2007, European Journal of Nuclear Medicine and Molecular Imaging.

[49]  Ackerman Nb,et al.  The blood supply of experimental liver metastases. II. A microcirculatory study of the normal and tumor vessels of the liver with the use of perfused silicone rubber. , 1970 .

[50]  J. Konishi,et al.  MR imaging of intrahepatic cholangiocarcinoma with pathologic correlation. , 2001, AJR. American journal of roentgenology.

[51]  Ann Harper,et al.  Optimizing staging for hepatocellular carcinoma before liver transplantation: A retrospective analysis of the UNOS/OPTN database , 2006, Liver transplantation : official publication of the American Association for the Study of Liver Diseases and the International Liver Transplantation Society.

[52]  Osamu Matsui,et al.  Hepatocellular carcinoma: signal intensity at gadoxetic acid-enhanced MR Imaging--correlation with molecular transporters and histopathologic features. , 2010, Radiology.

[53]  S. Kumano,et al.  Hypervascular hepatocellular carcinomas: detection with gadoxetate disodium-enhanced MR imaging and multiphasic multidetector CT , 2012, European Radiology.

[54]  T. Murakami,et al.  Hepatic metastases: detection with multi-detector row CT, SPIO-enhanced MR imaging, and both techniques combined. , 2006, Radiology.

[55]  Catherine Julié,et al.  Complete response of colorectal liver metastases after chemotherapy: does it mean cure? , 2006, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[56]  Steven S Raman,et al.  Radiofrequency ablation of hepatocellular carcinoma: treatment success as defined by histologic examination of the explanted liver. , 2005, Radiology.

[57]  Jesse S. Voss,et al.  Primary sclerosing cholangitis with equivocal cytology: Fluorescence in situ hybridization and serum CA 19‐9 predict risk of malignancy , 2013, Cancer cytopathology.

[58]  S. Curley,et al.  High-resolution computed tomography accurately predicts resectability in hilar cholangiocarcinoma. , 2007, American journal of surgery.

[59]  MRI versus 64-row MDCT for diagnosis of hepatocellular carcinoma. , 2009, World journal of gastroenterology.

[60]  D. Collins,et al.  Combining diffusion-weighted MRI with Gd-EOB-DTPA-enhanced MRI improves the detection of colorectal liver metastases. , 2012, The British journal of radiology.

[61]  ndrea,et al.  Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis. , 1996, The New England journal of medicine.

[62]  M. A. van den Bosch,et al.  Accuracy of Multislice Liver CT and MRI for Preoperative Assessment of Colorectal Liver Metastases after Neoadjuvant Chemotherapy , 2011, Digestive Surgery.

[63]  G. Gores,et al.  The utility of CA 19-9 in the diagnoses of cholangiocarcinoma in patients without primary sclerosing cholangitis , 2000, American Journal of Gastroenterology.

[64]  P. Malfertheiner,et al.  Hepatocellular carcinoma (HCC): a global perspective. , 2010, Journal of clinical gastroenterology.

[65]  H. Bismuth,et al.  Intrahepatic cholangioenteric anastomosis in carcinoma of the hilus of the liver. , 1975, Surgery, gynecology & obstetrics.

[66]  M. Cova,et al.  Evidence of diagnostic enhancement pattern in hepatocellular carcinoma nodules ≤2 cm according to the AASLD/EASL revised criteria , 2013, Abdominal Imaging.

[67]  Markus Grube,et al.  Hepatic Uptake of the Magnetic Resonance Imaging Contrast Agent Gd-EOB-DTPA: Role of Human Organic Anion Transporters , 2010, Drug Metabolism and Disposition.

[68]  Jin‐Young Jang,et al.  Preoperative assessment of resectability of hepatic hilar cholangiocarcinoma: combined CT and cholangiography with revised criteria. , 2006, Radiology.

[69]  M. D'Angelica,et al.  Predictors of a true complete response among disappearing liver metastases from colorectal cancer after chemotherapy , 2010, Cancer.

[70]  R. Manfredi,et al.  [Malignant biliary hilar stenosis: MR cholangiography compared with direct cholangiography]. , 2001, La Radiologia medica.

[71]  Geoffrey E. Wile,et al.  Magnetic resonance imaging of the liver: sequence optimization and artifacts. , 2010, Magnetic resonance imaging clinics of North America.

[72]  Myeong-Jin Kim,et al.  Differentiation of early hepatocellular carcinoma from benign hepatocellular nodules on gadoxetic acid-enhanced MRI. , 2012, The British journal of radiology.

[73]  P. Meier,et al.  Hepatic uptake of the magnetic resonance imaging contrast agent gadoxetate by the organic anion transporting polypeptide Oatp1. , 1999, The Journal of pharmacology and experimental therapeutics.

[74]  K. Chandrakumaran,et al.  Detailed liver-specific imaging prior to pre-operative chemotherapy for colorectal liver metastases reduces intra-hepatic recurrence and the need for a repeat hepatectomy. , 2012, HPB : the official journal of the International Hepato Pancreato Biliary Association.

[75]  M. Tillich,et al.  Multiphasic helical CT in diagnosis and staging of hilar cholangiocarcinoma. , 1998, AJR. American journal of roentgenology.

[76]  Tae Un Kim,et al.  Significance of the “Delayed hyperintense portal vein sign” in the hepatobiliary phase MRI obtained with Gd‐EOB‐DTPA , 2012, Journal of magnetic resonance imaging : JMRI.

[77]  B. Siegel,et al.  Chemotherapy-Induced Normalization of FDG Uptake by Colorectal Liver Metastases Does Not Usually Indicate Complete Pathologic Response , 2007, Journal of Gastrointestinal Surgery.

[78]  J A Brink,et al.  Aortic and hepatic contrast medium enhancement at CT. Part I. Prediction with a computer model. , 1998, Radiology.

[79]  B. Davidson,et al.  Prospective study of contrast‐enhanced computed tomography, computed tomography during arterioportography, and magnetic resonance imaging for staging colorectal liver metastases for liver resection , 2004, The British journal of surgery.

[80]  S. Cowper,et al.  Clinical and histological findings in nephrogenic systemic fibrosis. , 2008, European journal of radiology.

[81]  J B Fowlkes,et al.  Guidelines and Good Clinical Practice Recommendations for Contrast Enhanced Ultrasound (CEUS) in the Liver – Update 2012 , 2012, Ultraschall in der Medizin.

[82]  N. Hosten,et al.  Visualization of hepatic uptake transporter function in healthy subjects by using gadoxetic acid-enhanced MR imaging. , 2012, Radiology.

[83]  D. Gouma,et al.  Prognostic Impact of Preoperative Imaging Parameters on Resectability of Hilar Cholangiocarcinoma , 2013, HPB surgery : a world journal of hepatic, pancreatic and biliary surgery.

[84]  D. Iannitti,et al.  Hepatocellular carcinoma and cholangiocarcinoma: an update , 2014, Expert review of gastroenterology & hepatology.

[85]  J. Shindoh,et al.  Optimal morphologic response to preoperative chemotherapy: an alternate outcome end point before resection of hepatic colorectal metastases. , 2012, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[86]  I. Floriani,et al.  Staging of colorectal liver metastases after preoperative chemotherapy. Diffusion-weighted imaging in combination with Gd-EOB-DTPA MRI sequences increases sensitivity and diagnostic accuracy , 2013, European Radiology.

[87]  Doumit Daou,et al.  Respiratory motion handling is mandatory to accomplish the high-resolution PET destiny , 2008, European Journal of Nuclear Medicine and Molecular Imaging.

[88]  B. Gray,et al.  Vascularization of small liver metastases , 1989, The British journal of surgery.

[89]  S. Zangos,et al.  Staging of Klatskin tumours (hilar cholangiocarcinomas): comparison of MR cholangiography, MR imaging, and endoscopic retrograde cholangiography , 2006, European Radiology.

[90]  G. Everson,et al.  Impact of pretransplant diagnosis of hepatocellular carcinoma on cadveric liver allocation in the era of MELD , 2004, Liver transplantation : official publication of the American Association for the Study of Liver Diseases and the International Liver Transplantation Society.

[91]  Steven A Curley,et al.  Three Hundred and One Consecutive Extended Right Hepatectomies: Evaluation of Outcome Based on Systematic Liver Volumetry , 2009, Annals of surgery.

[92]  K. Boudjema,et al.  Liver Transplantation for Hepatocellular Carcinoma Without Preoperative Tumor Biopsy , 2008, Transplantation.

[93]  J. Shindoh,et al.  Kinetic growth rate after portal vein embolization predicts posthepatectomy outcomes: toward zero liver-related mortality in patients with colorectal liver metastases and small future liver remnant. , 2013, Journal of the American College of Surgeons.

[94]  L. Laasonen,et al.  Preoperative assessment of focal liver lesions: multidetector computed tomography challenges magnetic resonance imaging , 2005, Acta radiologica.

[95]  R. Hunt,et al.  World Gastroenterology Organisation Global Guidelines: GERD Global Perspective on Gastroesophageal Reflux Disease. , 2017, Journal of clinical gastroenterology.

[96]  K. Lindor,et al.  Utility of serum tumor markers, imaging, and biliary cytology for detecting cholangiocarcinoma in primary sclerosing cholangitis , 2008, Hepatology.

[97]  G. Garcia‐Tsao,et al.  Management and Treatment of Patients With Cirrhosis and Portal Hypertension: Recommendations From the Department of Veterans Affairs Hepatitis C Resource Center Program and the National Hepatitis C Program , 2009, The American Journal of Gastroenterology.

[98]  I. Endo,et al.  Importance of Complete Pathologic Response to Prehepatectomy Chemotherapy in Treating Colorectal Cancer Metastases , 2009, Annals of surgery.