(BQ) Part 1 book Gastrointestinal imaging presents the following contents: Pharynx and esophagus, stomach, small bowel, appendix, colon, anorectum, diffuse and vascular liver disease. Invite you to consult.
Gastrointestinal Imaging Rotations in Radiology Published and Forthcoming Books in the Rotations in Radiology Series Pediatric Radiology Janet R. Reid, Angelisa Paladin, William Davros, Edward Y. Lee, and Caroline Carrico Cardiac Imaging Charles S. White, Linda B. Haramati, Joseph Jen-Sho Chen, and Jeffrey M. Levsky Gastrointestinal Imaging Angela D. Levy, Koenraad J. Mortele, and Benjamin M. Yeh Chest Imaging Melissa Rosado de Christensen, Sanjeev Bhalla, Gerald Abbott, and Santiago Martinez-Jiminez Emergency Radiology Hani H Abujudeh Neuroradiology Zoran Rumboldt, Giulio Zuccoli, Clifford Eskey, Timothy Amrhein, and Benjamin Huang Rotations in Radiology Gastrointestinal Imaging Edited by Angela D. Levy, MD Professor of Radiology Department of Radiology Medstar Georgetown University Hospital Washington, DC Koenraad J. Mortele, MD Associate Professor of Radiology Harvard Medical School Department of Radiology Beth Israel Deaconess Medical Center Boston, Massachusetts Benjamin M. Yeh, MD Professor of Radiology UCSF Department of Radiology and Biomedical Imaging University of California, San Francisco San Francisco, California With Medical Illustrations by Heike Blum Medical Illustrator Müenster, Germany 1 Oxford University Press is a department of the University of Oxford It furthers the University’s objective of excellence in research, scholarship, and education by publishing worldwide Oxford New York Auckland Cape Town Dar es Salaam Hong Kong Karachi Kuala Lumpur Madrid Melbourne Mexico City Nairobi New Delhi Shanghai Taipei Toronto With offices in Argentina Austria Brazil Chile Czech Republic France Greece Guatemala Hungary Italy Japan Poland Portugal Singapore South Korea Switzerland Thailand Turkey Ukraine Vietnam Oxford is a registered trademark of Oxford University Press in the UK and certain other countries Published in the United States of America by Oxford University Press 198 Madison Avenue, New York, NY 10016 © Oxford University Press 2015 Original Artwork © H Blum All rights reserved No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, without the prior permission in writing of Oxford University Press, or as expressly permitted by law, by license, or under terms agreed with the appropriate reproduction rights organization Inquiries concerning reproduction outside the scope of the above should be sent to the Rights Department, Oxford University Press, at the address above You must not circulate this work in any other form and you must impose this same condition on any acquirer Library of Congress Cataloging-in-Publication Data Gastrointestinal imaging (Levy) Gastrointestinal imaging / edited by Angela D Levy, Koenraad J Mortele, Benjamin M Yeh p ; cm.—(Rotations in radiology) Includes bibliographical references and index ISBN 978–0–19–975942–2 (alk paper) I. Levy, Angela D., editor. II. Mortele, Koenraad J., editor. III. Yeh, Benjamin, editor. IV. Title. V. Series: Rotations in radiology [DNLM: 1. Digestive System Diseases—diagnosis. 2. Diagnosis, Differential 3. Diagnostic Imaging—methods. 4. Diagnostic Techniques, Digestive System WI 141] RC804.D52 616.3′0754—dc23 2014028627 This material is not intended to be, and should not be considered, a substitute for medical or other professional advice Treatment for the conditions described in this material is highly dependent on the individual circumstances And, while this material is designed to offer accurate information with respect to the subject matter covered and to be current as of the time it was written, research and knowledge about medical and health issues is constantly evolving and dose schedules for medications are being revised continually, with new side effects recognized and accounted for regularly Readers must therefore always check the product information and clinical procedures with the most up-to-date published product information and data sheets provided by the manufacturers and the most recent codes of conduct and safety regulation The publisher and the authors make no representations or warranties to readers, express or implied, as to the accuracy or completeness of this material Without limiting the foregoing, the publisher and the authors make no representations or warranties as to the accuracy or efficacy of the drug dosages mentioned in the material The authors and the publisher not accept, and expressly disclaim, any responsibility for any liability, loss or risk that may be claimed or incurred as a consequence of the use and/or application of any of the contents of this material 9 8 7 6 5 4 3 2 1 Printed in the United States of America on acid-free paper Dedication To my husband Asa, for his love and infinite support —ADL To Dejana, for her infinite love and support, and my four beautiful children, Charlotte, Christophe, Mabel and Mila, who make me proud every day and remind me of what is truly important in life —KJM To my wife, Dr. Z. Jane Wang, and our kids, who inspire us daily —BMY Disclosures The views expressed in Section 14, Multisystem Disorders and Syndromes, are those of the authors and not necessarily reflect the official policy or position of the Uniformed Services University of the Health Sciences, Department of the Air Force, Navy or Army; Department of Defense or the US Government Contents Prefacꕇ╇╇xv Contributors ╇╇╇xvii Section I: Pharynx and Esophagus Normal Anatomy and Imaging Techniques of the Pharynx and Esophagus ╇╇╇ Marc S. Levine Pharyngeal Disorders ╇╇╇7 Marc S. Levine Esophageal Motility Disorders ╇╇╇ 11 Marc S. Levine A Achalasia ╇╇╇11 B Diffuse Esophageal Spasm ╇╇╇ 13 C Gastroesophageal Reflux Disease ╇╇╇15 Pharyngeal and Esophageal Diverticula ╇╇╇16 Marc S. Levine A Zenkers and Killian-Jamieson Diverticula ╇╇╇16 B Thoracic Esophageal Diverticula ╇╇╇18 Infectious Esophagitis ╇╇╇21 Marc S. Levine A Candida Esophagitis ╇╇╇21 B Viral Esophagitis ╇╇╇22 Noninfectious Esophagitis ╇╇╇26 Marc S. Levine A Reflux Esophagitis/Peptic Scarring/ Barrett’s Esophagus ╇╇╇26 B Drug-induced Esophagitis ╇╇╇ 30 C Eosinophilic Esophagitis ╇╇╇31 Benign Esophageal Tumors ╇╇╇ 33 Marc S. Levine A Leiomyoma ╇╇╇33 B Fibrovascular Polyp ╇╇╇34 Section II: Stomach 11 Normal Anatomy and Imaging Techniques of the Stomach ╇╇╇ 51 Laura R. Carucci 12 Helicobacter Pylori and Peptic Ulcer Disease ╇╇╇55 Laura R. Carucci A Helicobacter Pylori Gastritis ╇╇╇55 B Gastric Ulcer ╇╇╇57 13 Other Inflammatory Conditions of the Stomach ╇╇╇61 Laura R. Carucci A Atrophic Gastritis ╇╇╇61 B Emphysematous Gastritis ╇╇╇63 C Ménétrier’s Disease ╇╇╇65 14 Benign Tumors of the Stomach ╇╇╇ 68 Laura R. Carucci A Gastric Polyps ╇╇╇68 B Gastrointestinal Stromal Tumor ╇╇╇ 70 C Lipoma ╇╇╇73 15 Malignant Tumors of the Stomach ╇╇╇ 76 Laura R. Carucci A Gastric Adenocarcinoma ╇╇╇76 B Malignant Gastric Stromal Tumors ╇╇╇ 79 C Gastric Lymphoma ╇╇╇82 D Gastric Metastases ╇╇╇84 16 Hernia and Volvulus ╇╇╇ 88 Laura R. Carucci A Hernia ╇╇╇88 B Volvulus ╇╇╇90 17 Miscellaneous Disorders of the Stomach ╇╇╇94 Laura R. Carucci A Gastric Varices ╇╇╇94 B Obstruction of the Gastric Outlet ╇╇╇ 96 C Gastric Diverticulum ╇╇╇99 D Gastric Bezoar ╇╇╇101 Esophageal Perforation ╇╇╇40 Marc S. Levine 18 Stomach Following Bariatric Surgery ╇╇╇103 Laura R. Carucci A Roux-en-Y Gastric Bypass ╇╇╇ 103 B Gastric Banding ╇╇╇106 C Gastric Sleeve ╇╇╇108 10 Esophageal Webs, Rings, and Varices ╇╇╇ 44 Marc S. Levine A Schatzki Ring ╇╇╇44 B Esophageal Varices ╇╇╇46 19 Other Postsurgical Changes ╇╇╇ 111 Laura R. Carucci A Fundoplication ╇╇╇111 B Billroth/Gastrojejunostomy ╇╇╇114 Esophageal Squamous Cell Carcinoma and Adenocarcinoma ╇╇╇36 Marc S. Levine CHAPTER 58 Veno-Occlusive Disorders Beatriz C Baranski Kaniak, Guilherme Moura da Cunha, Jin-Young Choi, and Claude B. Sirlin Definition Veno-occlusive disorders involve the obstruction of hepatic venous outflow Obstructions can occur in the suprahepatic inferior vena cava or hepatic veins (Budd-Chiari syndrome) or in the terminal hepatic venules or sinusoids (sinusoidal obstruction syndrome) Budd-Chiari syndrome may be primary (caused by intraluminal thrombosis; 75% of cases) or secondary (caused by invasion or compression by a tumor; 25% of cases) Demographic and Clinical Features General Features Primary Budd-Chiari syndrome and sinusoidal obstruction syndrome have similar clinical manifestations, such as abdominal pain, hepatomegaly, ascites, and fluid retention In contrast with other hepatic disorders, these disorders are unique in that they may cause portal hypertension prior to overt hepatic parenchymal dysfunction Primary Budd-Chiari syndrome and sinusoidal obstruction syndrome can occur in all ethnicities and at any age Both genders may be affected Primary Budd-Chiari Syndrome Primary Budd-Chiari syndrome has a prevalence of about in 1 million individuals, with an annual incidence of about in 10 million In western nations, the most common predisposing conditions include myeloproliferative and other hematologic disorders, pregnancy, postpartum state, use of oral contraceptives, and genetic hypercoagulability disorders Radiation, bone marrow transplantation, chemotherapeutic drugs, systemic venoinvasive infections (aspergillosis), and autoimmune diseases (Behỗets disease) can also be associated with Budd-Chiari syndrome Membranous (congenital) webs of the inferior vena cava are the most common cause of Budd-Chiari syndrome in Asia Predisposing factors are not discovered in 20% to 50% of patients The clinical picture in Budd-Chiari syndrome is defined by the location, extent, and acuteness of the venous outflow obstruction and on the remaining primary and collateral circulation The syndrome can be fulminant, 354 acute, subacute, chronic, or even asymptomatic In the uncommon fulminant form, liver failure is the most common presentation In the acute and subacute forms, portal hypertension is the most common manifestation In the chronic form (80%), portal hypertension, hepatomegaly, jaundice, and progression to cirrhosis (20%) and end-stage liver disease can be observed; renal impairment is observed in 50% of cases The classic triad of Budd-Chiari syndrome (abdominal pain, ascites, and hepatomegaly) is observed most commonly in the fulminant and acute forms In addition to hepatic venous or inferior vena cava occlusion, 10% to 20% of affected patients develop superimposed obstruction of the extrahepatic portal vein, presumably as a consequence of blood stasis in the portal vein in the setting of a hypercoagulable state Prognosis depends not only on the severity of the Budd-Chiari syndrome but also on the underlying predisposing condition or conditions Overall, the average 10-year survival rate in patients with primary Budd-Chiari syndrome is about 70% Sinusoidal Obstruction Syndrome Sinusoidal obstruction syndrome is a rare toxin-mediated condition occurring most commonly as a complication of hematopoietic stem cell transplantation and less commonly as a complication of solid organ transplantation It can also occur after chemotherapy in nontransplant settings, as a result of high-dose radiation therapy, and from accidental poisoning with food, drinks, or herbal medications contaminated with pyrrolizidine alkaloids The incidence and natural history of sinusoidal obstruction syndrome are variable and depend on its cause and other factors After stem cell transplantation, the incidence of sinusoidal obstruction syndrome ranges from 5% to 70% depending on the conditioning (preparatory) regimen given prior to the transplant, patient factors, and criteria used to diagnose the condition Sinusoidal obstruction syndrome usually occurs within weeks after transplant with tender hepatomegaly, ascites, fluid retention, and hyperbilirubinemia The condition may resolve completely within to weeks or advance rapidly to multiorgan failure (renal failure, encephalopathy, and pulmonary insufficiency) and death Patients who recover rarely develop cirrhosis By comparison, sinusoidal obstruction syndrome associated Ve n o - O c c l u s i v e D i s o r d e r s with chemotherapy for colorectal hepatic metastases is usually asymptomatic Its clinical relevance is that it may increase morbidity and liver failure after the surgical resection of hepatic metastases Therefore identification of sinusoidal obstruction syndrome is important for determining the timing of hepatic resection and the planning of further chemotherapy Currently the diagnosis of sinusoidal obstruction syndrome is based on clinical and laboratory findings, with liver biopsy reserved for equivocal cases Imaging is used to exclude biliary obstruction and tumor infiltration of the liver as the cause for the patient’s presentation, but imaging with conventional contrast agents does not reliably diagnose sinusoidal obstruction syndrome Recent investigations suggest that MRI with hepatocyte-specific agents may permit the noninvasive diagnosis of sinusoidal obstruction syndrome, as described further on If the results of recent investigations are confirmed, the role of imaging in the evaluation and management of this disorder may expand Pathophysiology disease with liver failure ultimate may occur Large regenerative nodules develop in arterialized areas of the liver that are deprived of portal perfusion but well drained by hepatic venous collaterals These nodules are multiple, variable in size (diameters ranging from less than 5 mm to more than 4 cm), and benign; they not undergo malignant transformation These liver abnormalities may be uneven in distribution depending on the sites of venous obstruction; areas of the liver drained by unoccluded hepatic veins typically undergo compensatory hypertrophy If all major hepatic veins are occluded but the inferior vena cava remains patent, the central portion of the liver (mainly the caudate lobe) characteristically hypertrophies, in part owing to preserved venous drainage through multiple small caudate lobe veins that enter the cava directly and in part from preferential portal perfusion of central versus peripheral hepatic parenchyma Globally the liver may be large, despite possible progression to cirrhosis Renal failure due to the activation of the renin-angiotensin pathways and excess sodium retention may also occur General Features Sinusoidal obstruction syndrome and Budd-Chiari syndrome have similar pathophysiologic features In both disorders, venous obstruction prevents blood from flowing out of the liver, leading to hepatic congestion, blood stagnation, and a subsequent increase in hepatic sinusoidal and portal vein pressures Portal hypertension ensues and is associated with development of protein-rich ascites and the formation of collateral venous channels Histologically, stagnant red blood cells distend and dilate the centrilobular sinusoids, causing compression of surrounding parenchyma and loss of hepatocytes The red blood cells eventually extravasate into the space of Disse and replace the disappearing hepatocytes Blood-filled lakes may develop in the centrilobular zone, with loss of recognizable hepatic parenchyma At the periphery of the injured areas, cholestatic changes and hemosiderin-laden macrophages may be present, but there is little if any inflammation Grossly the congested liver assumes a “nutmeg” appearance Sinusoidal Obstruction Syndrome In sinusoidal obstruction syndrome, drugs (e.g., those used to prepare patients for stem cell transplantation and some chemotherapy agents), radiation, or pyrrolizidine alkaloid‒contaminated food or drink induce toxin-mediated endothelial injury The injured sinusoidal endothelial cells dehisce into the sinusoidal lumen, embolize downstream, and cause nonthrombotic mechanical occlusion of hepatic sinusoids and terminal hepatic venules The endothelial injury also triggers the coagulation cascade and induces a local hypercoagulable state, leading to fibrin deposition within the lumen; this may exacerbate the occlusive process Although fibrin deposits may be evident, frank thrombus within the central veins is rare, in distinction to primary Budd-Chiari syndrome, in which it is characteristic Sinusoidal fibrosis may develop, but progression to cirrhosis is rare Liver involvement in sinusoidal obstruction syndrome tends to be diffuse and uniform Primary Budd-Chiari Syndrome Because primary Budd-Chiari syndrome is caused by intraluminal thrombosis, thrombus is characteristically present within central veins at histologic examination In chronic Budd-Chiari syndrome, reduced hepatic perfusion leads to centrilobular necrosis, followed by progressive fibrosis The fibrosis forms bridges between central veins, characteristically sparing the portal tracts and eventually resulting in a “venocentric cirrhosis” or “reversed-lobulation” pattern of cirrhosis End-stage liver Budd-Chiari Syndrome Imaging plays a fundamental role in the evaluation and management of Budd-Chiari syndrome Key imaging findings depend on the acuity of the disorder and the imaging modality In acute Budd-Chiari syndrome, ultrasound may reveal intraluminal thrombus as well as abnormal or absent venous waveforms in the affected hepatic veins (Figure 58-1), but no collateral vessels are seen Acutely thrombosed hepatic veins may be hyperattenuating at unenhanced CT and show absence of flow voids on spin-echo MRI and Imaging Features 355 356 Gastrointestinal Imaging (A) (B) Figure 58-1 A 25-year-old man with acute Budd-Chiari syndrome Color Doppler ultrasound images show absent flow in the middle hepatic vein (MHV) (A), and biphasic flow in the right hepatic vein (RHV) (B) The inferior vena cava is patent (arrows) absence of flow-related enhancement of gradient-echo MRI The thrombosed veins are more readily apparent as nonenhancing at contrast-enhanced CT and MRI Liver edema may cause smooth extrinsic narrowing of nonthrombosed inferior vena cava and hepatic veins Owing to hepatic congestion, the liver periphery is hypoattenuating at unenhanced CT and has high signal intensity on unenhanced T2-weighted MRI After the administration of contrast agents, the central portion of the liver and caudate enhance early while the periphery is relatively hypoenhanced (fan-shaped pattern); on more delayed images, the pattern reverses and there is relative hyperenhancement of the liver periphery (Figure 58-2) This temporal pattern has been attributed to marked elevation of parenchymal pressure with corresponding hypoperfusion and slow flow in the periphery of the liver Additionally, owing to the stagnation of contrast material within the sinusoids, the enhancing portions of the parenchyma may have a “nutmeg,” mottled, or mosaic appearance in the arterial and early venous phases Conventional catheter angiography may reveal smooth narrowing of the nonthrombosed inferior vena cava and hepatic veins, which is attributable to extrinsic compression of these vessels Imaging of chronic Budd-Chiari syndrome may show compensatory hypertrophy of the caudate lobe and relative atrophy of the periphery Despite progression to cirrhosis, the affected liver tends to be large and without the surface nodularity typically seen in other forms of cirrhosis Ultrasound may reveal hyperechogenic fibrous cords or membranes replacing the hepatic veins as well as multiple intrahepatic collateral vessels around the occluded veins Color Doppler ultrasound may show “bicolored hepatic veins,” reflecting opposing flow directions within adjacent perivenous collateral channels These small collateral vessels have a characteristic “spider web” appearance at conventional venography Edema and fibrosis may appear as diffusely hypodense liver at unenhanced CT and low hepatic parenchymal signal intensity on both T1- and T2-weighted MR images The enhancement differences between the caudate lobe and the periphery of the liver observed in acute Budd-Chiari syndrome become less noticeable in chronic stages because of the development of intrahepatic collateral channels Large regenerative nodules may measure up to 4 cm in diameter; they may be hyperattenuating at unenhanced CT, hyperintense at T1-weighted MRI, and hypointense at T2-weighted unenhanced MRI These nodules typically hyperenhance in the arterial phase and show enhancement similar to that of background liver in the venous phases (Figure 58-3) The nodules may grow and be mistaken for hepatocellular carcinoma or other malignant nodules The correct diagnosis can usually be established by the clinical setting (Budd-Chiari syndrome), characteristic unenhanced imaging features, and fading to isoenhancement rather than washout to hypoenhancement in venous phases Gadoxetate-enhanced MRI may be useful by demonstrating delayed uptake of the agent by the regenerative nodules Sinusoidal Obstruction Syndrome Conventional imaging findings of sinusoidal obstruction syndrome are nonspecific but include patent yet narrowed hepatic veins (Figure 58-4), hepatomegaly, periportal edema, ascites, and gallbladder wall thickening Doppler ultrasound may show bidirectional or reversed flow in hepatic veins as well as an elevated hepatic arterial resistive index (equal to or greater than 0.75) The edematous liver parenchyma is hypoattenuating at unenhanced CT and has heterogeneous signal intensity at unenhanced MRI The parenchyma enhances heterogeneously owing to arterioportal shunting, which develops in response to the sinusoidal obstruction The temporal Ve n o - O c c l u s i v e D i s o r d e r s (A) (B) (C) (D) Figure 58-2 Acute Budd-Chiari syndrome CT images acquired before contrast administration (A) and arterial (B), portal venous (C), and 3-minute delayed (D) images after contrast administration in a 28-year-old woman show diffuse peripheral edema and hypoattenuation due to congestion (asterisk in A), early enhancement of the central portion of the liver (B and C) with delayed enhancement of the congested periphery (D) The hepatic veins are occluded (arrows in C and D) enhancement pattern characteristic of Budd-Chiari syndrome—early enhancement of the central liver and caudate with delayed reversed enhancement—may be seen; visualization of patent hepatic veins permits differentiation (Figure 58-5) Recently diffuse reticular hypointensities on T1weighted hepatobiliary phase MR images using hepatocytespecific contrast agents have been observed in sinusoidal obstruction syndrome secondary to chemotherapy for colorectal liver metastases; preliminary studies suggest that this finding may have high specificity for the diagnosis of this disorder Differential Diagnosis ■ Cirrhosis due primary Budd-Chiari syndrome versus cirrhosis due to other causes: In most forms of cirrhosis, the liver has a nodular contour and is small ■ Regenerative nodules in primary Budd-Chiari syndrome versus regenerative nodules in other forms of cirrhosis: Regenerative nodules in other forms of cirrhosis are usually smaller and without arterial enhancement ■ Regenerative nodules in primary Budd-Chiari syndrome versus hepatocellular carcinoma nodules: Hepatocellular carcinoma nodules tend to wash out to hypoenhancement in venous phases Management/Clinical Issues Budd-Chiari Syndrome Treatment for Budd-Chiari syndrome is aimed at alleviating hepatic congestion It includes supportive medical therapy (diuretics, sodium restriction) and correction of hemodynamic abnormalities (anticoagulation medications, thrombolytic treatment, angioplasty with stent placement, transjugular intrahepatic portosystemic shunt, and venous shunt surgery) Liver transplantation is indicated in fulminant liver failure, failure of shunts, or progression to end-stage liver disease Patients with cirrhosis should be considered for hepatocellular carcinoma surveillance 357 (A) (B) (C) (D) (E) (F) (G) (H) Figure 58-3 Large regenerative nodule in chronic Budd-Chiari syndrome MR images acquired at 3T show a 14-mm large regenerative nodule in segment 8. Fat-saturated T1-weighted images were acquired before contrast administration (A) and in the arterial (B), portal venous (C), and 3-minute delayed (D) phases after the administration of extracellular contrast The nodule hyperenhances in the arterial phase (arrow in B) and subsequently fades to isointensity The nodule is hyperintense on T1-weighted images (A and E) and isointense on T2-weighted (F) and diffusion-weighted images acquired with b values of b = 0 (G) and 500 (H) s/mm2 Ve n o - O c c l u s i v e D i s o r d e r s Figure 58-4 A 24-year-old man with acute sinusoidal obstruction syndrome after bone marrow transplantation This double oblique reformatted CT image in the portal venous phase shows narrowed but patent hepatic veins and patent inferior vena cava Findings are consistent with but not diagnostic of sinusoidal obstruction syndrome Sinusoidal Obstruction Syndrome Therapy for sinusoidal obstruction syndrome is primarily supportive and includes alleviation of pain and maintenance of intravascular volume and renal perfusion while limiting third-space fluid accumulation Antithrombotic drugs are being investigated in clinical trials (A) Key Points ■ Budd-Chiari syndrome and sinusoidal obstruction syndrome are veno-occlusive diseases that affect hepatic venous outflow Both cause portal hypertension Budd-Chiari syndrome may progress to chronic liver disease and cirrhosis Sinusoidal obstruction syndrome associated with stem cell transplantation usually resolves spontaneously or advances rapidly to multiorgan failure and death; chronic liver disease with progression to cirrhosis usually does not occur Sinusoidal obstruction syndrome associated with chemotherapy for colorectal cancer metastases is usually asymptomatic but may contribute to postoperative hepatic failure if hepatic resection of metastases is performed ■ Suprahepatic inferior vena cava or hepatic veins are affected in Budd-Chiari syndrome and terminal hepatic venules or sinusoids are affected in sinusoidal obstruction syndrome ■ Primary Budd-Chiari syndrome is caused by intraluminal thrombosis whereas sinusoidal obstruction syndrome is caused by toxin-mediated injury to endothelial cells followed by dehiscence of injured cells into the sinusoids and nonthrombotic occlusion of the sinusoidal lumen ■ In Budd-Chiari syndrome, imaging studies show occlusion of hepatic veins and/or the inferior vena cava Acutely there is arterial-phase hyperenhancement of the central liver and caudate lobe with reversed venous-phase enhancement Chronically there is caudate lobe enlargement and development of intrahepatic collateral vessels (B) Figure 58-5 Sinusoidal obstruction syndrome after bone marrow transplantation (same patient as in Figure 58-4, 2 months later) CT images in the portal venous (A) and 3-minute delayed (B) phases show early central fan-shaped enhancement (arrow in A) with delayed reversal Appearance resembles that of Budd-Chiari syndrome but hepatic veins are patent (B) 359 360 Gastrointestinal Imaging Large hypervascular regenerative nodules are frequently observed in Budd-Chiari syndrome ■ In sinusoidal obstruction syndrome, conventional imaging findings are nonspecific and include patent but narrow hepatic veins, hepatomegaly, periportal edema, ascites, gallbladder wall thickening, elevation of the hepatic arterial resistive index at Doppler ultrasound, and heterogeneous enhancement at contrastenhanced CT or MRI The temporal enhancement pattern characteristic of acute Budd-Chiari syndrome may be observed, but hepatic veins are patent ■ Poor uptake of hepatocyte-specific contrast agents may be seen with sinusoidal obstruction syndrome ■ Further Reading Andrew SD Sinusoidal obstructive syndrome Alberta Bone and Marrow Transplant Program Canadian Blood and Marrow Transplant Group: 2–9 http://cbmtg.org/~ASSETS/DOCU MENT/ Guide/Sinusoidal%20Obstruction%20Syndrome.pdf Brancatelli G, Federele MP, Grazioli L, Golfieri R, Lencioni R Large regenerative nodules in Budd-Chiari syndrome and other vascular disorders of the liver: CT and MR imaging findings with clinicopathologic correlation AJR 2002;178(4):877–883 Cura M, Haskal Z, Lopera J Diagnostic and interventional radiology for Budd-Chiari Syndrome RadioGraphics 2009;29(3): 669–681 Sahani DV, Samir A Abdominal Imaging Expert radiology series Maryland Heights, Mo: Saunders Elsevier, 2010 Valla D-C Primary Budd-Chiari syndrome J Hepatol 2009;50: 195–203 CHAPTER 59 Liver Transplantation Beatriz C Baranski Kaniak, Guilherme Moura da Cunha, Jin-Young Choi, and Claude B. Sirlin A Pre‒liver Transplantation Evaluation Definition Deceased-donor liver transplantation involves surgical replacement of a diseased liver by one from a recently deceased donor Living-donor liver transplantation involves surgical replacement of a diseased liver by part of a healthy liver from a living adult donor In the United States, deceased-donor transplantation is by far more common than living-donor liver transplantation Demographic and Clinical Features Liver transplantation is the only cure for many patients with end-stage liver disease, acute fulminant liver failure, hepatocellular carcinoma, and select other conditions Liver transplantation is a major intervention with huge costs, high morbidity, and nontrivial mortality; after surgery, it requires lifelong immunosuppression and clinical surveillance Moreover, owing to organ shortage, most patients on the liver transplantation waitlist not receive a liver transplant Currently, there are over 16,000 individuals in the liver transplantation waitlist in the United States, of whom about 3% are children and 97% are adults In 2010, a total of 6,291 liver transplantations were performed Overcoming the shortage of organs and mortality on the waitlist requires appropriate selection and prioritization of patients who will most likely benefit from liver transplantation The most common indications for liver transplantation in adults are end-stage liver disease with life-threatening or incapacitating complications (recurrent variceal hemorrhage, intractable ascites, refractory encephalopathy); acute fulminant hepatic failure (idiopathic, virus, drugs, toxins); and hepatocellular carcinoma Less common indications for liver transplantation are polycystic liver disease with decompensation, portal hypertension or intolerable quality of life; primary sclerosing cholangitis with recurrent episodes of cholangitis requiring hospitalization; severe hepatic metabolic disorders; and, in select cases, tumors other than hepatocellular carcinoma (e.g., hilar cholangiocarcinoma after neoadjuvant chemotherapy, unresectable neuroendocrine liver metastases) Patient enrollment onto the liver transplantation waitlist is done by a multidisciplinary selection committee and is based on a comprehensive medical and psychosocial evaluation Patients with active substance abuse (alcohol, drugs) or factors that adversely affect the technical feasibility of surgery (e.g., obesity, unfavorable anatomy, lack of vascular patency) are usually not considered If the transplant team determines that a patient is a good candidate for transplantation, he or she is added to the waiting list Each center has its own selection criteria and reserves the right to decline patients listed at other centers Centers monitor listed patients carefully until the transplantation is performed Patients who become too ill to undergo liver transplantation or develop contraindications to liver transplantation are de-listed Prioritization for liver transplantation is complex and depends on multiple factors In general, the highest priority is given to status candidates, defined as those with severe liver failure at risk of imminent death in the absence of a liver transplant Conditions associated with a status designation may include acute fulminant liver failure, primary nonfunction of a transplanted liver or hepatic artery thrombosis within week of a transplant, and chronic liver disease in its rapid terminal phases Except for status patients, priority is assigned using the Model for End-Stage Liver Disease (MELD) score for adults and the Pediatric End-Stage Liver Disease (PELD) score for children (under 18 years of age), stratified by ABO blood group and geographic region The MELD and PELD scores are calculated from three laboratory values (serum creatinine, total bilirubin, international normalized ratio [INR] for MELD; albumin, bilirubin, and INR for PELD) and are based on the estimated probability of death due to physiologic deterioration within 3 months if the patient does not receive a transplant If a liver becomes available to two patients in the same region with the same MELD or PELD scores and blood type, time on the waiting list becomes an important deciding factor The physiological MELD and PELD scores described above not take into account the risk of death due to cancer in patients with hepatocellular carcinoma Such 361 362 Gastrointestinal Imaging patients may also benefit from liver transplantation and, depending on the tumor stage, are assigned hepatocellular carcinoma exception points for transplantation prioritization The tumor stage is determined noninvasively by imaging studies and depends on the number and size of hepatocellular carcinoma nodules as well as the presence or absence of tumoral thrombosis Biopsy confirmation of hepatocellular carcinoma is not performed routinely, and the diagnosis usually is made based on imaging findings To qualify for hepatocellular carcinoma exception points, a tumor stage of T2 is required, defined as a single nodule between and 5 cm or two to three nodules each less than 3 cm in the absence of tumoral thrombosis The rationale for prioritizing stage T2 for liver transplantation is that patients with radiology-determined stage T2 cancer have a post‒liver transplantation prognosis similar to that of those who undergo liver transplantation based on physiologic MELD or PELD scores By comparison, patients with radiology-determined stage T3 (a single nodule greater than 5 cm or two to three nodules at least one of which is greater than 3 cm) or T4 (four or more nodules or the presence of tumoral thrombosis) tumors have high hepatocellular carcinoma recurrence rates after liver transplantation, presumably because extrahepatic metastases were present but undetected prior to surgery, while patients with radiology-determined stage T1 tumors (solitary nodule less than 2 cm) often have no cancer identified at explant pathology, presumably reflecting false-positive imaging findings For patients assigned hepatocellular carcinoma exception points, CT or MRI is performed every 3 months until transplantatopm, stage progression beyond transplantability, or death At each time point, if the tumor stage does not progress beyond T2, additional exception points are assigned, thereby moving the patient up in priority on the waitlist In some geographic regions, patients with hepatocellular carcinoma beyond stage T2 disease can receive hepatocellular carcinoma exception points if the cancer is successfully downstaged by ablative and/or embolic therapy Prioritization for liver transplantation based on factors other than MELD/PELD score or hepatocellular carcinoma exception points usually requires an appeal to the regional review board by the transplant center responsible for the patient Imaging Features Imaging studies play a critical role in the preoperative evaluation of potential liver transplantation patients because they provide key anatomic information to guide the selection of patients and prevent or reduce postoperative complications The following imaging findings should be reported as they influence the selection of potential recipients of liver transplants and may alter prioritization and surgical planning: Arterial Findings ■ Arterial anatomy (arterial variants such as replaced or accessory hepatic arteries) ■ Arterial pathology ■ Severe atherosclerosis, mural calcification of thrombus, or stenosis of the abdominal aorta, celiac artery, or hepatic artery (may compromise inflow to the transplanted organ and may alert the surgeon to potential technical difficulties) ■ Poststenotic dilatation of hepatic artery (may alter surgical technique) ■ Aneurysms of splenic artery or other visceral arteries (high risk of rupture after liver transplantation; need to be addressed before or during surgery) Venous Findings ■ Bland portal vein thrombosis (need to define the degree and extent of the thrombus into the splenic or superior mesenteric veins, patency of confluences, and presence of mural calcifications or cavernous transformation) ■ Tumoral thrombosis (contraindication to liver transplantation) ■ Inferior vena cava patency and stenosis, especially in retransplants (may occur at either the suprahepatic or infrahepatic anastomosis) Biliary Findings ■ Major abnormalities of the extrahepatic duct (strictures, marked dilatation, and choledochal cysts; these may affect surgical technique and feasibility) Transjugular Portosystemic Shunt ■ The locations of the proximal and distal ends of the shunt must be reported Hepatocellular Carcinoma ■ The number and size of nodules must be reported, as well as the presence of tumoral thrombosis Nodules with features diagnostic of malignancy but atypical for hepatocellular carcinoma should also be reported, as these may represent cholangiocellular carcinomas or metastases and may require biopsy prior to liver transplantation Ascites ■ The presence and degree of ascites should be reported A large amount of ascites in the recipient improves accommodation of the transplanted liver in the abdominal cavity and may permit the use of a larger donor liver than would otherwise be possible L i v e r Tr a n s p l a n t a t i o n Surgical Technique The basic surgical techniques in deceased-donor liver transplantation involves three vascular and one biliary anastomosis: Caval: end to end, end to side, or side to side Portal vein: end to side ■ Hepatic artery: end to end ■ Bile duct: most commonly end to end; in patients with a diseased biliary tree due to primary sclerosing cholangitis or other cause, a choledochojejunostomy is performed ■ ■ Key Points ■ Liver transplantation is the treatment of choice for adult or pediatric patients with end-stage liver disease, acute liver failure, or hepatocellular carcinoma In the United States, deceased-donor liver transplantation is far more common than living-donor transplantation ■ A multidisciplinary selection committee at each transplant center selects suitable candidates and places them on the waitlist Highest priority is given to status patients In non‒status patients, prioritization is based on MELD (adults) and PELD (children) scores Patients with hepatocellular carcinoma are assigned hepatocellular carcinoma exception points if the tumor stage meets appropriate criteria ■ The goal of imaging studies is to assess hepatic vascular and biliary anatomy, variants, and patency; diagnose and stage hepatocellular carcinoma; and report relevant ancillary findings such as the presence and severity of ascites Further Reading Freeman RB, Weisner RH, Harper A, et al The new liver allocation system: moving toward evidence-based transplantation policy Liver Transpl 2002;8:851 Redvanly RD, Nelson RC, Stieber AC, Dodd GD 3rd Imaging in the preoperative evaluation of adult liver-transplant candidates: goals, merits of various procedures, and recommendations AJR 1995;164:611–617 Said A, Williams J, Holden J, et al Model for end stage liver disease score predicts mortality across a broad spectrum of liver disease J Hepatol 2004;40:897 McDiarmid SV, Goodrich NP, Harper AM, Merion RM Liver Transplantation for status 1: the consequences of good intentions Liver Transpl 2007;13:699–707 Teefey SA, Hildeboldt CC, Dehdashti F, et al Detection of primary hepatic malignancy in liver transplant candidates: prospective comparison of CT, MR imaging, US, and PET Radiology 2003;226:533–542 US Department of Health and Human Services Organ Pro curement and Transplantation Network UNet Pre-transplant Data base, 2010 http://optn.transplant.hrsa.gov/converge/ data/ Xu J, Kochanek KD, Murphy SL, Betzaida Tejada-Vera BS US Department of Health and Human Services, Centers for Disease Control and Prevention National Vital Statistics Reports 2010;58(19):1–136 B Post‒liver Transplantation Complications Definition Liver transplantation complications are conditions or events that occur after liver transplantation and cause morbidity or mortality Complications of liver transplantation include liver graft rejection, vascular complications, biliary complications, postoperative intra- or perihepatic collections, recurrence of underlying hepatic disease, and recurrence of hepatic malignancy Transplant complications not unique to liver transplantation (immunosuppression-related opportunistic infections and neoplasms) are not discussed in this section Demographic and Clinical Features Graft Rejection Hyperacute rejection, which may complicate the transplantation of other organs, is rarely observed after liver transplantation Acute rejection is the most common complication of liver transplantation It occurs in 20% to 60% of transplant recipients, usually between and 30 days posttransplant Manifestations include jaundice, abnormal liver serum chemistries, fever, abdominal pain, and graft dysfunction Diagnosis is made by liver biopsy Chronic cellular rejection Chronic rejection occurs in 1% to 5% of liver transplant recipients, starts at least 3 months after surgery, and is a major cause of late graft failure and late patient death in both adult and pediatric liver transplant recipients Clinically it manifests as jaundice, pruritus, and ultimately loss of liver synthetic function Diagnosis is made by liver biopsy Vascular Complications Vascular complications usually occur at anastomotic sites and may affect hepatic arteries, portal veins, hepatic veins, or the inferior vena cava Hepatic artery thrombosis, the most severe vascular complication, occurs in 4% to 12% of adult and 9% to 42% of pediatric liver transplant recipients, usually within 2 months after liver transplantation It has high fatality (up to 60%) and can cause fulminant hepatic necrosis and 363 364 Gastrointestinal Imaging graft failure, liver infarction and abscess formation, and ischemic cholangiopathy (see further on) Hepatic artery stenosis occurs in 11% to 13% of liver transplant recipients Manifestations depend on the severity of the stenosis and include elevated serum liver chemistries, graft dysfunction, and ischemic cholangiopathy (see further on) Post‒liver transplantation hepatic artery pseudoaneurysms are rare (0.3% to 1%) They may be intra- or extrahepatic and typically present within the first months after transplantation Portal venous thrombosis or stenosis occurs in 1% to 3% of liver transplant recipients Manifestations include abdominal pain, graft dysfunction, portal hypertension, and ascites Uncommonly, hepatic veins and/or the inferior vena cava become thrombosed or stenosed Affected patients may present with graft dysfunction, portal hypertension, Budd-Chiari syndrome, and lower extremity edema Biliary Complications Biliary complications develop in 25% of liver transplant recipients and include bile leaks at the T-tube exit site, anastomotic strictures, and ischemic cholangiopathy The time of onset after surgery is variable and depends in part on the nature and etiology of the complication T-tube site bile leaks manifest clinically within the first 3 months after transplantation with extrahepatic biloma formation Anastomotic strictures can occur at any time after liver transplantation Ischemic cholangiopathy is usually associated with hepatic artery stenosis or thrombosis and develops within 1 year after transplantation; manifestations include biliary necrosis, nonanastomotic strictures, bile leaks, bilomas, peribiliary abscesses, and sepsis Postoperative Fluid Collections Fluid collections are common within the first few weeks after surgery Collections usually are intra- or perihepatic; perihepatic collections are usually located at the site of vascular or biliary anastomoses Collections are most commonly bilomas but may be abscesses, seromas, hematomas, or infarctions Recurrence of Underlying Disease Reinfection of the liver with hepatitis C virus occurs in up to 90% of liver transplant recipients with a history of chronic hepatitis C infection and can advance to severe fibrosis or cirrhosis in as little as to 10 years; up to 25% will eventually require retransplantation With hepatitis B vaccination, clinically significant hepatitis B reinfection occurs infrequently (10% or less of patients) Recurrent nonalcoholic fatty disease (NAFLD) and nonalcoholic steatohepatitis (NASH) are common after liver transplantation, especially if NAFLD risk factors (diabetes, obesity, hypertriglyceridemia) persist Progression from isolated steatosis to NASH, cirrhosis, and end-stage liver disease has been demonstrated Hepatocellular Carcinoma The frequency of post‒liver transplantation hepatocellular carcinoma recurrence ranges from 10% to 60% and depends on the pathology-determined tumor stage and grade at the time of surgery as well as the presence of microvascular invasion Recurrences usually appear within 24 months after transplantation Median survival from the time of diagnosis is about 1 year Pathophysiology Graft Rejection Acute rejection Both cellular and humoral immune mechanisms may play a role Cellular rejection is characterized by peribiliary lymphocytic infiltration, whereas humoral rejection is characterized by vasculitis (endotheliitis) Hepatocellular swelling and cholestasis are uncommon Chronic Rejection Chronic rejection is dominated by vascular changes (fibrous intimal thickening), interstitial fibrosis, centrilobular hepatocyte swelling, and centrilobular cholestasis There is bile duct loss in at least 50% of portal tracts Vascular Complications Hepatic arterial, portal venous, and caval stenosis or thrombosis is usually caused by technical problems at the donor-recipient anastomosis (clamp injury, intimal injury due to perfusion catheters, anastomosis vessel redundancy), although hypercoagulability and external compression (hematoma, hepatic regeneration) may contribute to portal venous and caval obstructions The pathophysiologic consequences of vascular stenosis or thrombosis depend on their location and severity In hepatic artery thrombosis and hemodynamically significant hepatic artery stenosis, hepatic arterial flow is absent or reduced, thereby predisposing to hepatic infarction and, as described further on, ischemic cholangiopathy Portal vein thrombosis or stenosis may cause presinusoidal portal hypertension and global hepatic hypoperfusion, hepatocellular nutritional deficiency, and ultimately parenchymal atrophy; uncommonly hepatic infarction may occur Caval obstruction causes hepatic congestion or lower extremity edema, depending on its location Biliary Complications Anastomotic bile duct strictures are usually due to chronic focal ischemia and eventually fibrotic scarring Ischemic cholangiopathy is usually caused by hepatic artery thrombosis or stenosis, usually leading to multifocal biliary stricture formation These abnormalities may predispose to pyogenic cholangitis and the formation of peribiliary abscesses In severe cases, the biliary epithelium may slough and collect as dependent debris within dilated L i v e r Tr a n s p l a n t a t i o n biliary cavities Less commonly, intrahepatic strictures occur in the absence of hepatic arterial obstruction The etiology of such strictures has not been elucidated Recurrence of Underlying Disease In liver transplant recipients with a history of chronic hepatitis C, infection of the new liver occurs immediately and histologic features of viral hepatitis—such as acute and chronic inflammatory cellular infiltrates, fibrosis, and eventually cirrhosis—are common Recurrent hepatitis B infection is of relatively low incidence The pathophysiology of recurrent NAFLD and NASH is not well understood; similar mechanisms as in primary NAFLD and NASH likely play a role Additionally, immunosuppressive drugs promote insulin resistance and thereby may accelerate the progression of NAFLD and NASH in patients who have undergone liver transplantation Recurrent Hepatocellular Carcinoma Tumor recurrence is usually due to extrahepatic metastasis that was present but undiagnosed prior to liver transplantation; after surgery, the metastasis may grow in its extrahepatic location or locations or may spread hematogenously to the liver and then grow as a hepatic lesion Less commonly, post‒liver transplantation hepatocellular carcinoma is due to de novo tumor development related to recurrent liver disease Imaging Features Graft Rejection Acute or Chronic Rejection No imaging modality is sensitive or specific for the diagnosis of rejection The diagnosis is based on biopsy and histology interpretation Vascular Complications Ultrasound is the imaging modality of choice for the initial evaluation of vascular complications in patients who have undergone liver transplantation; it is performed routinely within 24 hours after surgery If ultrasound is abnormal, contrast-enhanced CT or less commonly MRI may be done for further evaluation Ultrasound imaging may show an intraluminal filling defect in the hepatic artery or may fail to identify a normal artery along its expected course Doppler ultrasound shows abnormal flow (resistive flow proximal to a stenosis, turbulent flow at a stenosis, tardus parvus waveform distal to a stenosis) or flow may be absent Contrast-enhanced CT or MRI confirms the arterial obstruction (Figure 59-1) and may also depict ischemic areas in the hepatic parenchyma Post‒liver transplantation pseudoaneurysms are similar in appearance to those occurring in other settings Figure 59-1 Posttransplant hepatic artery thrombosis in a 60-year-old man with posttransplant hepatic artery thrombosis Oblique reformatted gadoxetate-enhanced MR image acquired at 3T in the hepatic arterial phase 3 months after liver transplantation shows occlusion of the common hepatic artery (arrow) Portal vein thrombosis has similar imaging findings as described for acute bland thrombosis; portal vein stenosis appears as focal narrowing of the vein with abnormal velocities on Doppler ultrasound In hepatic venous or caval thrombosis or stenosis, imaging may show absence of flow or filling defects within the lumen of the affected veins A persistent monophasic wave pattern at Doppler ultrasound suggests a downstream stenosis Biliary Complications Ultrasound, CT, and MRI may depict bilomas, biliary strictures, biliary dilatations, and ductal calculi In addition, contrast-enhanced CT and MRI may reveal associated peribiliary perfusional alterations MRI with magnetic resonance cholangiopancreatography tends to demonstrate strictures more clearly than ultrasound or CT The multifocal structuring associated with ischemic cholangiopathy resembles that of primary sclerosing cholangitis and HIV cholangiopathy Intrahepatic cavitation from biliary necrosis may be seen adjacent to or along the expected course of bile ducts (Figure 59-2) These cavities may become infected and/or can compress portal veins Accumulation of hepatocyte-specific contrast material within these cavities on hepatobiliary-phase MR images indicates communication with the biliary tree The optimal delay time for detection of bile leaks has not been determined but may be longer than the delays usually recommended for the detection and characterization of liver lesions (Figure 59-3) Postoperative Fluid Collections Postoperative collections appear as complex cystic masses without internal vascularity and may represent bilomas, seromas, hematomas, abscesses, or parenchymal necrosis 365 366 Gastrointestinal Imaging (A) (B) (C) Figure 59-2 Posttransplant ischemic cholangiopathy and biloma formation in the same patient as in Figure 59-1 Gadoxetate-enhanced MR images in the arterial (A) and 20-minute hepatobiliary (B) phase show intrahepatic cavitation of the central bile ducts but no biliary excretion into the cavities A more delayed image at hours after contrast injection shows intracavitary filling (arrow in C), confirming communication with the biliary tree A diagnosis was made of ischemic cholangiopathy with biliary necrosis and bile duct cavitation secondary to hepatic artery thrombosis Accumulation of hepatocyte-specific contrast material within these collections indicates communication with the biliary tree and is diagnostic of bile leak with biloma formation Management/Clinical Issues Liver transplant recipients are monitored closely clinically and with laboratory tests to help identify rejection or infection during the first weeks after transplantation After the early post‒liver transplantation period, less frequent follow-up is required Immunosuppressive therapy to control or prevent rejection is initiated intravenously immediately following surgery The majority of patients require lifelong immunosuppressive therapy Patients routinely undergo ultrasound within 24 hours after surgery to assess the patency of the vascular and biliary anastomoses and detect postoperative collections If ultrasound reveals abnormalities, a CT and, less frequently, a MRI is performed for more complete evaluation Management then depends on the type and severity Figure 59-3 Posttransplant recurrence of hepatocellular carcinoma (HCC) in a 61-year-old woman 3 years after liver transplantation for HCC CT image through the lung bases shows innumerable thoracic metastases L i v e r Tr a n s p l a n t a t i o n of the complication Patients with hepatic artery thrombosis may require immediate retransplantation After the immediate posttransplant imaging evaluation, imaging is usually reserved for the evaluation of clinical symptoms or laboratory abnormalities Patients with cancer pretransplant may undergo imaging surveillance to detect recurrence Key Points ■ Common complications after liver transplantation are acute rejection, vascular and biliary compromise, postoperative fluid collections, recurrence of underlying liver disease, and recurrence of cancer ■ Vascular complications usually occur at anastomotic sites; the most severe vascular complication is hepatic artery thrombosis ■ Biliary complications include bile leaks, anastomotic strictures, and ischemic cholangiopathy Ischemic cholangiopathy is usually due to arterial obstruction (hepatic artery thrombosis or stenosis); its imaging appearance resembles that of primary sclerosing cholangitis and HIV cholangiopathy Further Reading Chong WK, Beland JC, Weeks SM Sonographic evaluation of venous obstruction in liver transplants AJR 2007; 188: 515–521 Freeman RB, Gish RG, Harper A, et al Model for end-stage liver disease (MELD) exception guidelines: results and recommendations from the MELD exception study group and conference (MESSAGE) for the approval of patients who need liver transplantation with diseases not considered by the standard MELD formula Liver Transpl 2006;12(3):S128–S136, Kim YS, Lim HK, Rhim H, Lee WJ, Joh JW, Park CK Recurrence of hepatocellular carcinoma after liver transplantation: patterns and prognostic factors based on clinical and radiologic features AJR 2006;189:352–358 Post DJ, Douglas DD, Mulligan DC Immunosuppression in liver transplantation Liver Transpl 2005;11:1307–1314 US Department of Health and Human Services Organ Procurement and Transplantation Network UNet database, 2010 http://optn.transplant.hrsa.gov/converge/data/ 367 ... Varices ╇╇╇46 19 Other Postsurgical Changes ╇╇╇ 11 1 Laura R. Carucci A Fundoplication ╇╇╠11 1 B Billroth/Gastrojejunostomy ╇╇╠11 4 Esophageal Squamous Cell Carcinoma and Adenocarcinoma ╇╇╇36... double-contrast radiography of the pharynx Radiology 19 84 ;15 1 :12 3 12 6 Ekberg O, Nylander G Double contrast examination of the pharynx Gastrointest Radiol 19 85 ;10 :263–2 71 Gordon AR, Levine MS, Redfern RO, et ... postirradiation edema from recurrent tumor AJR 19 93 ;16 1 :12 05 12 08 Rubesin SE, Glick SN The tailored double-contrast pharyngogram Crit Rev Diagn Imaging 19 88;28 :13 3 17 9 Rubesin SE, Laufer I Pictorial review: principles