Graft complications following orthotopic liver transplantation: Role of non-invasive cross-sectional imaging techniques

European Journal of Radiology 85 (2016) 1271–1283

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Graft complications following orthotopic liver transplantation: Role of non-invasive cross-sectional imaging techniques Piero Boraschi ∗ , Maria Clotilde Della Pina, Francescamaria Donati 2nd Unit of Radiology—Department of Diagnostic Radiology, Vascular and Interventional Radiology, and Nuclear Medicine, Pisa University Hospital, Via Paradisa 2, 56124 Pisa, Italy

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Article history: Received 1 March 2016 Received in revised form 10 April 2016 Accepted 13 April 2016 Keywords: Liver transplantation Graft complications Multidetector CT MR imaging MR cholangiography Contrast-enhanced MR cholangiography

a b s t r a c t Orthotopic liver transplantation is the treatment of choice in adult patients with endstage liver disease. Survival of both graft and patient has progressively improved over time due to improvements in surgical and medical treatment. However, post-transplant complications still have a significant impact on morbidity and mortality associated with transplant surgery. The most common adverse events of the graft include vascular (arterial and venous stenosis and thrombosis), biliary (leakage, strictures, stones) and parenchymal complications (hepatitis virus C infection, HCC recurrence, liver abscesses). The diagnosis of these adverse events is often challenging because of the low specificity of clinical and biologic findings. Different diagnostic algorithms have been proposed for the detection of graft complications and, in this setting, radiological evaluation plays a key role in differential diagnosis of graft complications and the exclusion of other adverse events. Ultrasound examination is established the first-line method of identifying adverse events in liver transplant recipients but a normal or a technically unsatisfactory study cannot exclude the presence of biliary, vascular and/or parenchymal complications. In these circumstances, before planning any treatment, multi-detector CT and/or MR imaging and MR cholangiography should be performed for the evaluation of vascular structures, biliary system, liver parenchyma and fluid collections. The aim of this review is to illustrate the role and state-of-the-art of non-invasive crosssectional imaging techniques in the diagnosis and management of complications which primarily affect the graft in patients after liver transplantation. © 2016 Elsevier Ireland Ltd. All rights reserved.

1. Introduction Liver transplantation is currently the preferred treatment for patients with acute or advanced chronic liver failure for whom no other treatment option is available [1,2]. Over the last decades, refinement of surgical techniques and advances in perioperative management has significantly improved the outcomes of liver transplantation. However, postoperative complications after ortothopic liver transplantation (OLT) still have a significant impact on the morbidity and mortality of recipients. The common adverse events include vascular (arterial and venous stenosis and thrombosis), biliary (leakage, strictures, stones) and parenchymal complications (hepatitis virus C infection, HCC recurrence, liver abscesses) [3].

∗ Corresponding author at: 2nd Unit of Radiology—Department of Diagnostic Radiology, Vascular and Interventional Radiology, and Nuclear Medicine, Pisa University Hospital, Via Paradisa 2, 56124 Pisa, Italy. E-mail addresses: [email protected], [email protected] (P. Boraschi). http://dx.doi.org/10.1016/j.ejrad.2016.04.008 0720-048X/© 2016 Elsevier Ireland Ltd. All rights reserved.

Postoperatively, the main goal of diagnostic imaging techniques is to identify early and late complications, thus influencing the management of recipients and significantly contributing to increase graft and patient survival [4]. Knowledge and prompt recognition of post-OLT complications with the most suitable imaging method are crucial for both graft and patient survival. A series of diagnostic and interventional imaging techniques are actually available for the evaluation of liver transplant recipients. Radiologists and clinicians should aware of capabilities and limits of each of them in order to optimize the diagnosis of adverse events, especially in the presence of life- and graft-threatening biliary and vascular complications. The purpose of this review is to illustrate the role and new developments of state-of-the-art non-invasive cross-sectional imaging techniques in assessing and managing complications primarily affecting the graft in patients previously undergoing orthotopic liver transplantation.

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2. Non-invasive imaging techniques in post-OLT complications In the postoperative period after liver transplantation complications primarily affecting the graft often shows a largely overlapping spectrum of clinical and laboratory findings [5]. Acute rejection is a serious adverse event following OLT and its final diagnosis is definitively established only by graft biopsy and histological analysis. On this basis, imaging techniques have the specific role of excluding the other complications, which can have clinical signs and symptoms very similar to those of acute rejection [6]. In particular, in the early post-OLT phase the differential diagnosis between organ rejection and biliary and/or vascular adverse events impairing the graft function is extremely difficult [7]. In order to obtain a prompt and effective treatment and to ensure the survival of the graft, the main objective of non-invasive imaging techniques is to identify or exclude vascular, biliary and parenchymal complications. In this setting Doppler ultrasound (US), multidetector computed tomography (MDCT), Magnetic Resonance Imaging (MRI) and MR cholangiography, and direct cholangiography are the main imaging diagnostic modalities that are currently utilized for this aim [8]. In Fig. 1 we show the algorithmic approach that is routinely used in our center for liver transplantation to assess post-OLT complications with the above imaging modalities. Whenever we suspect a complication in a liver transplant recipient for the presence of clinical symptoms and/or abnormal liver function tests results, the diagnostic work-up usually begins with the serology tests and a Doppler ultrasound, that can allow the contemporary evaluation of hepatic vasculature, biliary system and hepatic parenchyma. This technique represents the ideal initial imaging modality to detect post-operative complications of the transplanted liver since it is accessible, accurate, cost-effective, avoids the use of ionizing radiation, and can be easily performed at the patient’s bedside [9,10]. The results of US are highly reproducible when performed by expert operators and in a dedicated clinical scenario. If a complication is identified and no intervention is required, it is usually followed-up with serial US exams [11–14]. Although Doppler ultrasound is a non-invasive method of identifying adverse events in liver recipients, a normal US examination or a technically unsatisfactory US study cannot exclude the presence of biliary, vascular and/or parenchymal complications. In these circumstances and in the case of repeated US demonstration of an abnormality that can require therapeutic

management, further evaluation is advocated and multidetector computed tomography and/or MR imaging and MR cholangiography are usually performed.

3. Multidetector computed tomography Multidetector computed tomography imaging is accepted as a second line non-invasive diagnostic method in various complications after OLT. MDCT is a valuable examination to detect and evaluate complications because it provides non-invasive and rapid imaging of the entire abdomen including angiographic studies, liver parenchyma, biliary tract, and the other abdominal organs. MDCT is usually reserved for patients with clinical-laboratory and/or vascular abnormalities at Doppler US. Recent introduction of 64-section MDCT and the subsequent development of 256-section MDCT and dual energy CT have markedly changed the way of performing and evaluating CT imaging [15]. The current temporal resolution of modern CT scanners permits to obtain angiographic CT studies at the peak of arterial enhancement without motion or respiratory artifacts. Furthermore, the spatial resolution now available permits to obtain high quality three-dimensional reconstructions, including Maximum Intensity Projection (MIP) and Volume Rendering (VR) [16]. Some dualenergy CT (DECT) applications became available in the abdomen thanks to the recent advances in CT technology, especially the possibility of current scanners to simultaneously acquire images at two different energies [17,18]. DECT is based on different attenuation of photons with different energies by tissues. DECT can be obtained with two x-ray tubes operating at two different energies or with a single x-ray tube rapidly switching between two different energies or with detectors capable to discriminate different energies. With DECT it is now possible to calculate virtual unenhanced imaging set with consequent lower radiation exposure, improve visibility of iodine enhancing lesions at lower energy or increase temporal resolution in angiographic studies. A recent study demonstrated that DECT allowed CT angiographic studies using low concentration contrast media, vascular signal intensity being increased compared to single energy CT [19]. Post-processing of the imaging data sets using threedimensional reformatting techniques such as Maximum Intensity Projection (MIP) and Volume Rendering (VR) is needed to better recognize hepatic artery anatomy and most of vascular complications. MIP imaging extracts the highest attenuation voxels in a data

Fig. 1. Complications after liver transplantation: algorithmic approach. LFTs: liver function tests; US: ultrasound; MRCP: Magnetic Resonance Cholangiopancreatography; CT: computed tomography; ERC: endoscopic retrograde cholangiography; PTC: percutaneous transhepatic cholangiography; DSA: digital subtraction angiography.

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set and project them in a two dimensional image. MIP imaging permits to better visualize vasculature system and to evaluate small intra-parenchymal branches in the liver. The major limitation of MIP reconstructions is that vascular calcifications can obscure vascular lumen. On the other hand, VR analyzes the content of each voxel and assigns a specific color and transparency to the voxel; respect to axial images, VR can accentuate small abnormalities. Of importance, bones do not interfere with the visualization of vasculature; this is useful in anatomic regions where bones and vessels are very close and when visualization of relationships between different tissues is important [16]. Abdomen MDCT scans should include baseline and quadriphasic hepatic scanning after bolus monitoring technique (double arterial phase with a delay of 10 and 20 s after reaching 100 UH threshold, the portal-venous phase with a delay of 60–70 s and the last phase at 180 s after the injection beginning). Non-ionic contrast material must be injected intravenously via a power injector (100–130 ml according to the patient body weight) at a flow-rate of 4–5 ml/s. Images should be reconstructed with a thickness of 1 mm or less [20]. According to the European Society of Urogenital Radiology (ESUR) guidelines, iso- or low-osmolar non-ionic contrast media should be used in order to reduce the incidence of contrast medium induced nephropathy (CIN); in patients at high risk of CIN (GFR less than 45 ml/min in combination with risk factors such as diabetes, age over 70 years, hypotension, dehydration) adequate hydration

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(normal saline intravenously 6 h before and after contrast medium) and elimination of nephrotoxic drugs should be considered [21]. On MDCT images in the post-operative period after OLT we can frequently observe some abdominal findings, such as small amounts of free intra-abdominal fluid or hematomas in the perihepatic region (especially in the hepatic hilum or adjacent to the anastomosis), the presence of periportal edema, right pleural effusion and small bowel edema. Periportal and porta hepatis lowattenuation zones are very common in this setting and probably reflect lymphedema and lymphangiectasia in most of the cases. The correlation with clinical and laboratory tests is important to avoid the misinterpretation of these normal findings visible on MDCT performed immediately after OLT and typically resolved within a few weeks [22]. The most common post-transplant vascular complication is hepatic artery thrombosis (HAT), occurring in 2–12% of cases, between 15 and 132 days after OLT. In liver transplant patient the celiac axis of donor is anastomosed to hepatic artery of recipient at the bifurcation in the right and left artery or at the takeoff of gastro-duodenal artery. Since the hepatic artery is the exclusive blood supply for biliary tract, the HAT can rapidly cause ischemia and necrosis of the biliary epithelium. In the early stages majority of patients show mild alteration of liver function tests; the prompt recognition of HAT is essential to avoid biliary leaks, bilomas, anastomotic biliary strictures, liver abscesses and finally the need of retrasplantation. MDCT is generally performed to confirm or identify HAT, recognizable as hepatic artery amputation or filling

Fig. 2. Hepatic arterial occlusion after OLT. Axial contrast-enhanced CT shows abrupt interruption of hepatic artery (a). Axial CT MIP (b, c) and VR (d) reconstructions confirm the hepatic artery occlusion. Common bile duct (CBD) stenting was previously performed.

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defect within the hepatic artery, usually at the site of the vascular anastomosis (Fig. 2). In general, MDCT is superior to MR angiography in term of rapidity and image quality in particular in patients clinically compromised. CT imaging is also ideal to evaluate the presence of areas of infarction and biloma in association with biliary necrosis. Ischemic areas can also be seen on CT images as wedge-shaped ipodense areas; larger areas can liquefy and become infected. Although surgical revascularization has traditionally been the principal treatment for early HAT, endovascular interventions have demonstrated high success rates, including fibrinolysis, angioplasty, or stent placement [23]. Hepatic artery stenosis (HAS) is the second most frequent vascular complication after OLT, and occurs in general in the first three months after liver transplantation at the anastomotic site. Risk factors include rejection, caliber differences between donor and recipient artery, clamp injury and injury associated with the cold preservation of the organ. There are not concordant data about a possible implication of trans-arterial chemoembolization (TACE) on the hepatic artery injury and the consequent arterial complication after OLT [24,25]. Patients can have from mild alteration of liver function tests secondary to ischemia to severe graft dysfunction. In order to avoid the development of HAT, the early diagnosis of this disease entity is fundamental and MDCT with 3D reconstruction is essential to evaluate the severity and the extent of HAS [26] (Fig. 3). Studies have shown good correlation between MDCT and angiography in the detection of vascular lesions with sensitivity of 100% and specificity of 89% [27]. Surgical options for HAS include resection with re-anastomosis and interposition of artery

or vein graft. Recent studies highlight the use of endovascular treatments for HAS: percutaneous transluminal angioplasty (PTA) and stent placement have demonstrated promising results in terms of technical success and long term results [23,28]. Hepatic pseudoaneurysm represents an uncommon complication after OLT. Extrahepatic pseudoaneurysm occurs in general at the anastomotic site or arises as a complication of angioplasty, whereas intrahepatic pseudoaneurysm may be a result of liver biopsy or biliary procedures. MDCT and 3D reconstructions show a focal lesion with the enhancement pattern of arterial vessel (Fig. 4). Coil embolization is the treatment of choice when a rapid hemostasis is needed. On the other hand, superselective embolization techniques in patients with intrahepatic pseudoaneursysm permit preservation of arterial supply of the graft. Surgical management is generally reserved for complicated cases and when endovascular treatments fail [29]. Some Authors have proposed to perform MDCT in all patients in the first week after OLT: the rate of re-trasplantation for arterial complications was less in patients in whom MDCT was performed systematically 7–10 days after liver transplantation than in patients referred to CT on demand, especially because the early discover of HAS in asymptomatic patients permits early stenting or surgery preventing biliary ischemia and necrosis [30]. Portal vein complications are relatively rare (Figs. 5 and 6). In the majority of cases of liver transplantation, portal vein anastomosis is end-to-end between donor and recipient vessels; however, the exact knowledge of the surgical technique is essential because stenosis occurs at the anastomotic site. Factors associated with an

Fig. 3. Hepatic arterial stenosis after OLT. The presence of a tardus and parvus waveform within the right (a) and left (b) hepatic arteries correlates with the presence of hepatic artery stenosis. Axial contrast-enhanced CT (c) and MIP reconstruction (d) confirm the hepatic arterial stricture.

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tors. Coronal images are useful to demonstrate the extent of IVC thrombosis. Other post-transplant complications of the graft include liver hematoma and abscess [31]. Majority of hematomas are typically located near vascular anastomosis or in the perihepatic space and resolve spontaneously in few weeks (Fig. 4). Intrahepatic abscess is often secondary to superinfection of biloma or liver infarcted areas in patients with HAT or HAS. On CT images abscesses are typically hypovascular rounded lesions with thin rim enhancement. A complex fluid collection with air level can also suggest the presence of an abscess. HCC recurrence of liver graft usually represents a rare late complication that can be diagnosed on both multiphasic CT and MR imaging, showing typical arterial enhancement (wash-in), followed by portal venous phase wash-out.

4. MR imaging and MR cholangiography

Fig. 4. Hepatic arterial pseudoaneurysm after OLT. Axial contrast-enhanced CT (a) and MIP reconstruction (b) show hepatic arterial pseudoaneurysm following liver transplantation. Perivascular fluid-ematic collection is also present. CBD stent was placed few days before.

increased risk of portal vein complications are caliber discrepancies between portal vein diameters of the donor and recipient, hypercoagulable states, prolonged cold ischemia time. Portal vein stenosis may be treated with angioplasty, stent placement and surgery. Portal vein thrombosis occurs in 3% of liver transplantations and often occurs in the extrahepatic tract. MDCT typically shows nonenhancing filling defect of portal vein. Treatment options include angioplasty, surgical thrombectomy, and thrombolysis. Thrombosis or stenosis of inferior vena cava (IVC) occurs in the majority of cases at the anastomotic site. Anastomosis of the donor and recipient IVCs is typically end-to-end. IVC stenosis is caused by anastomotic narrowing; MDCT shows additional imaging features of portal hypertension and Budd-Chiari syndrome. Angioplasty and stent placement are good therapeutic options. IVC thrombosis is caused by hypercoagulable states and surgical fac-

During liver transplantation surgical reconstruction of the biliary tract can be performed with a choledochocholedochostomy or, less frequently, with a biliodigestive or choledochojejunostomy. In the first case a T tube is generally placed and intraopeative cholangiography is routinely performed at the end of the procedure. T-tube cholangiography is the examination of choice in the early post-OLT phase during which the T-tube remains in place. However, when it is removed three months after liver transplantation (or if it is not used at all), magnetic resonance cholangiography (MRC) represents the preferred non-invasive imaging technique in the assessment of biliary abnormalities after OLT. Despite recent technological innovations, this method consists of the acquisition of a heavily T2-weighted sequence, which allows to visualize the structures containing stationary or slow-moving fluids as very hyperintense areas over a low-signal back-ground, obtaining both overview and detailed representation of the biliary tract. After preliminary acquisition of T1- and T2-weighted sequences in the axial plane, two different MRC sequences are conventionally performed: 1) breath-hold, thick-collimation (40–60 mm), 2D SS-FSE T2-weighted sequence utilizing coronal/coronal oblique projections; 2) respiratory-triggered, thin-collimation (2.4 mm thk/-1.2 mm) 3D FRFSE T2-weighted sequence in the coronal plane, providing numerous single thin partitions as a source for multiplanar and volumetric reconstructions [32–34]. Several authors have reported very encouraging results as concerns as the MRC evaluation of biliary complications after OLT [35–41]. In a recent meta-analysis published by Jorgensen et al. [42], the authors concluded that MRC allows an excellent diagnostic accuracy for biliary obstruction in liver transplant patients, with a combined sensitivity and specificity of 96% and 94%, respectively. They also suggested that MRC may be a suitable non-invasive test in recipients with low to moderate suspicion for biliary obstruction, being able to prevent the unneeded possible risks of ERCP in this clinical settings. Besides, in a still more recent meta-analysis by Xu et al. [43], these authors confirmed that MRC is a highly accurate diagnostic technique for diagnosis of biliary complications and strictures in patients who have undergone OLT. The main advantage of conventional T2-weighted MRC [36] is that the bile ducts are non-invasively depicted in their normal state, both below and above obstruction sites. However, the disadvantage of conventional T2-weighted MRC [44,45] is that it lacks functional information and so, differentiation between obstructive and nonobstructive dilatation of the bile ducts is often extremely difficult. Depiction of anatomy and lesion detection can be inadequate in a non-dilated biliary system; besides, free fluid and leak in the vicinity obscures the biliary anatomy due to overlapping [46].

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Fig. 5. Portal vein stenosis after OLT. Compared to the portal velocity before the stenosis (a), Doppler US shows increased peak velocity after the portal narrowing (b). Coronal CT reconstructions confirm anastomotic portal vein stenosis (c, d).

Fig. 6. Portal vein thrombosis after OLT. Ultrasonography shows hyperechoic material within an expanded portal vein lumen (a, b). Axial (c, d) and coronal CT images confirm portal and superior mesenteric vein thrombosis (e, f).

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Fig. 8. Anastomotic biliary stricture in a patient with a choledocho-choledochal anastomosis. Axial T2-weighted image (a) shows dilation of pre-anastomotic biliary tract with a stricture at the anastomotic site. MIP reconstruction (b) of threedimensional thin-slab fast spin-echo T2-weighted images better demonstrates a circumscribed narrowing at the level of the surgical anastomosis associated with dilation of the pre-anastomotic biliary tract.

Fig. 7. Anastomotic leakage in a patient with hepatico-jejunostomy. Single-shot thick-slab MR cholangiogram (a) shows a fluid collection in the area of biliaryenteric anastomosis. Axial (b) and coronal (c) MIP reconstructions of Gd-EOB-DTPA enhanced LAVA sequence well exhibit extravasation of contrast material into the peri-anastomotic space compatible with anastomotic leak.

T1-weighted contrast-enhanced MRC with intravenous administration of hepato-biliary contrast agents such as Mn-DPDP, Gd-BOPTA and Gd-EOB-DTPA [47] is a technique that has been recently introduced and may provide both anatomical and functional information on the biliary tract. The above mentioned contrast media are picked up by normal hepatocytes and eliminated at a various amount in the biliary system (3% to 5% for Gd-BOPTA, 20% for Mn-DPDP, 50% for Gd-EOBDTPA) [48]. This emerging diagnostic tool is performed using 3D breath-hold fatsuppressed T1-weighted gradient-echo sequences in the axial and coronal plane, and it is particularly helpful especially when utilizing Gd-EOB-DTPA, which allows acquisitions of both dynamic and hepato-biliary phases.

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Fig. 9. Anastomotic biliary stricture with lithiasis in a patient with hepatico-jejunostomy at 3.0-T device. Axial T2-weighted images (a) show dilation of the biliary system with concomitant stones at the level of the common and left hepatic ducts. Axial T1-weighted images (b) confirm the presence of calculi in the biliary tract. Coronal (c) and coronal/oblique (d) MIP reconstructions of three-dimensional thin-slab fast spin-echo T2-weighted images demonstrate dilation of the biliary system above the anastomosis with concomitant stones into the common hepatic duct at the level of the hepatico-jejunal anastomosis.

MR cholangiography well depicts the postoperative reconstruction of the biliary system and the different types of biliary anastomosis. Nevertheless, it can be limited in the visualization of the site of biliary-enteric anastomosis and also the possible cause of obstruction. Contrast-enhanced MRC may provide images with a higher resolution than those we can obtain using conventional T2-weighted MR cholangiography, and has the advantage of contrast agent into the biliary system and jejunal loop. Therefore, contrast- enhanced MRC can be useful to complement conventional T2-weighted MRC in demonstrating bile leakage or in evaluating biliary-enteric anastomosis and bile cast syndrome [49]. Finally, the recent innovation of 3.0-T device, including technical advances such as ultra-fast imaging sequences and parallel imaging techniques, provides improved image quality over that at 1.5-T. In particular, SNR at 3.0T is twice that at 1.5-T, with higher-resolution images in less time. Depiction of anatomy and lesion detection in a non-dilated biliary system is significantly better at 3.0-T, improving the evaluation of intrahepatic ductal disease [50]. Biliary tract adverse events are the most common complications after OLT and remain a major source of morbidity in liver transplant patients, with an incidence of 5%–32%. Complications such as bile leaks, anastomotic and non-anastomotic strictures, biliary stones, sludge and casts are encountered more commonly as a result of increased number of liver transplantations and the prolonged survival of transplant patients [51].

The prompt diagnosis and appropriate management of these adverse events are very important to ensure the survival of both the organ and the patient after OLT. Bile leakage represents the most frequent early biliary complication after OLT, occurring in 2%–25% of cases [52–55]. In liver transplant patients with both choledocho-choledochal (CC) and biliary-enteric anastomosis, rapid and correct localization of biliary leakage is helpful for guiding the more appropriate therapy. Contrast-enhanced MRC with intravenous administration of hepato-biliary contrast agents provides functional informations as concerns as biliary excretion and may be extremely helpful in localizing the bile leak, which is not generally possible at conventional T2 weighted MR cholangiography [56]. Indeed, using contrast-enhanced MRC we can demonstrate active biliary leakage by visualizing contrast media extravasation into the fluid collection and so we can also localize the anatomic site of the bile leak [56] (Fig. 7). Biliary strictures are the most frequent type of late biliary adverse events (5%–34% of liver transplant patients) [5,57], occur approximately five-eight months after OLT, and can be classified into anastomotic stricture (AST) and non-anastomotic stricture (NAS) according to their location [58]. Anastomotic strictures at the site of biliary anastomosis can occur in both choledocho-choledochal and choledocho-jejunal (CJ) type of biliary reconstruction [59]. In the CC strictures two-dimensional and 3D MR cholangiography show a circumscribed narrowing at the

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level of the surgical anastomosis that can be associated or not with dilatation of the pre-anastomotic biliary tract [60] (Fig. 8). Axial T1and T2-weighted images show a regular thickening of the anastomotic biliary wall with a typical ring-shaped hypointensity [60]; calculi can be often appreciable in the pre-anastomotic biliary tract (Fig. 9). Kinner et al. [58] evaluated the diagnostic performance of MRCP for the detection of biliary strictures after OLT according to the type of surgical reconstruction, concluding that post-OLT biliary stenoses can be properly identified by MRCP in recipients with CC; nevertheless, in patients with a bilio-digestive anastomosis the diagnostic performance of MRCP is reduced due to the less precise delineation of the anastomotic site. However, clear demonstration of the patency of the bilio-digestive anastomosis can be provided by contrast agent filling of the jejunal loop on contrast-enhanced MRC (Fig. 10); the differentiation between non-obstructive versus obstructive dilatation of the biliary tract may be arduous on conventional T2-weighted MRC since this technique does not provide functional information [48,49]. Alternatively, high concentration of hepato-biliary contrast agents in the bile ducts enables functional imaging of the biliary excretion since contrast-enhanced MRC may provide an indication of excretory function on the basis of the reference values of contrast media for biliary excretion [48,49]. Among biliary strictures, the most troublesome are the ischemic-type biliary lesions (ITBL), that are non-anastomotic intra- or extra-hepatic stenoses and dilatations involving electively the biliary system of the transplant. Microcirculatory problems related to graft preservation factors or immunogenic injury are the main pathogenic mechanisms that have been advocated for these lesions [61]. Using MRC, most of ITBL show a lengthy stricture that frequently involves the right and left hepatic ducts and the hepatic bifurcation, which is a prevalent localization for ischemic injures after OLT [41]. Another characteristic MR feature of ITBL is represented by wall thickening of the graft extra-hepatic biliary ducts, that can be associated to biliary sludge, stones or casts formation [34,40]. All these biliary findings can be better demonstrated at 3.0-T device [50] (Fig. 11). Actually, patients with obvious abnormalities on MRC generally have advanced disease and severe irreversible pathologic changes. Recently, Wang et al. [62] suggest that diffusion-weighted MR imaging (DWI) could sensitively detect the early injured bile ducts of ITBL without morphologic abnormality on MRC. In this study, the incidence of hyperintensity of bile ducts on DWI (82.9%, 29/35) was obviously higher in the ITBL patients than that in the control group of patients (5.0%, 1/20). Hyperintensity of the bile ducts of ITBL on DWI is assumed to reflect edematous inflammation injury, mainly caused by the impairment of blood supply to the peribiliary vascular plexus [62]. Furthermore, preliminary experiences suggest that contrastenhanced MRC using Gd-EOB-DTPA may provide both anatomical and functional information of ITBLs in liver transplant recipients. In fact, times of contrast agent excretion seem to be in correlation with different degrees of biliary obstruction. At least, patients undergoing OLT for primary sclerosing cholangitis can develop multiple biliary strictures alternating with dilation of bile ducts after liver transplantation. Sensitivity of MRCP is lower than that of ERCP in the identification of early alterations, but this non-invasive technique is helpful for detecting typical signs of biliary involvement in patients with a known diagnosis, in order to monitor the progress of these changes [50]. MRCP shows beaded bile ducts or we can observe a “pruned tree” appearance of the biliary system with multiple stenoses alternating with normal or slightly dilated ducts; in particular, distal arborisation and intrahepatic bile ducts variations can be more easily detected at 3.0-T device [50] (Fig. 12). Endoluminal bile duct obstruction, in the form of biliary stones, sludge and casts, can virtually occur at any time after OLT. Numer-

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Fig. 10. Patency of the bilio-digestive anastomosis at 3.0-T device. Single-shot thickslab MR cholangiogram (a) and MIP reconstruction (b) of three-dimensional thinslab fast spin-echo T2-weighted images show dilation of the biliary system without visualization of the hepatico-jejunostomy. Coronal MIP reconstructions (c) of GdEOB-DTPA enhanced LAVA sequences demonstrate the patency of the anastomosis with outflow of contrast-enhanced bile in the jejunal loop at 20 min.

ous published studies have shown that MRC is as effective as ERCP in diagnosing common bile duct stones, although the possibilities of MRI in identifying calculi of a few millimeters in size are still to be fully proven [63].

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Fig. 11. Ischemic type biliary lesion (ITBL) studied at both 1.5-T MRC and 3.0-T MRC six months after OLT. Single-shot thick-slab MR cholangiogram at 1.5-T (a) demonstrates a stenosis at the level of hepatic bifurcation and hepatic ducts with an irregular dilation of the intrahepatic biliary system; the extrahepatic biliary tree of the graft is not visualized. Single-shot thick-slab MR cholangiogram (b) and MIP reconstruction (b) of three-dimensional thin-slab fast spin-echo T2-weighted images at 3.0-T better demonstrate irregular dilation of the intrahepatic biliary system, showing also the more peripheral ducts. Axial T2-weighted images at 1.5-T device (d) well exhibit the presence of circumferential biliary wall thickening, even if a better delineation of this feature and a higher image quality can be appreciable in the same type of T2-weighted sequence at 3.0-T (e). The presence of endoluminal casts is also well evident on axial T1-weighted LAVA sequence (f). On diffusion-weighted MR imaging with different b-values (g) the liver parenchyma appears inhomogeneous with areas of persistent high signal intensity in all b-value acquisitions, associated to focal hyperintensity of bile ducts.

On conventional T2-weighted MR cholangiography the presence of pneumobilia is an element that can compromise the correct diagnosis of lithiasis. The differential diagnosis between stones and pneumobilia is usually performed on axial T2-weighted sequences. Calculi are generally identified as endoluminal areas of signal void surrounded by high intensity of bile in the dependent portion of the duct, whereas pneumobilia is typically characterized by low signal intensity in the nondependent portion of the bile duct [32]. Besides, on conventional T2-weighted MRC flow

artifacts are sometimes observed in the central portion of choledochal duct as thin area of low signal intensity [64]. These flow artefacts are not commonly recognized on contrast-enhanced T1weighted MR cholangiography, that may be helpful in providing an increased diagnostic confidence in the differential diagnosis between stones and pneumobilia. Furthermore, Kinner et al. [65] showed that adding non-enhanced T1-weighted sequences to conventional T2-weighted MRCP the diagnostic performance of MRI for the diagnosis of biliary cast syndrome after OLT is significantly

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Fig. 12. Recurrence of primary sclerosing cholangitis in a transplant patient with hepatico-jejunostomy studied at 3.0-T device. Thick (a) and thin slab MIP reconstruction (b) of three-dimensional thin-slab fast spin-echo T2-weighted images show multifocal stenosis with intervening dilation affecting the intrahepatic biliary system. MIP reconstructions (c) of Gd-EOB-DTPA enhanced LAVA images poorly visualize the intrahepatic biliary system, but are very accurate to depict the irregularities of the extrahepatic biliary tract. On diffusion-weighted MR imaging with different b-values (d) the liver parenchyma appears markedly inhomogeneous with areas of persistent high signal intensity in all b-value acquisitions; multiple enlarged lymph nodes are also evident in the hepatic hilum.

improved since biliary cast is hyperintense on T1-weighted images (Fig. 9). Another common occurrence after OLT is represented by sphincter of Oddi dysfunction (SOD) that is reported to be up to 7% in liver transplant recipients. The pathogenesis of SOD is attributed to the denervation of the sphincter during liver transplantation. On MRCP we can observe a significant dilatation of both recipient and donor bile duct in the absence of cholangiographic evidence of obstruction; a protrusion of the enlarged ampullary region into the duodenal lumen is sometimes associated. In these cases, contrastenhanced MRC can be added to T2-weighted MR cholangiography in order to obtain functional information on the degree of biliary obstruction and increase the diagnostic accuracy of MR imaging, particularly in patients with biochemical abnormalities that could be treated endoscopically with or without stenting. Conflict of interest All the authors declare that they have no conflict of interest. Authors’ contributions All authors have made substantial contributions to all of the following: (1) the conception and design of the study, or acquisition of data, or analysis and interpretation of data,

(2) drafting the article or revising it critically for important intellectual content, (3) final approval of the version to be submitted.

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