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Noninvasive Imaging of Liver Transplant Complications
Noninvasive Imaging of Liver Transplant Complications Wael E.A. Saad, MBBCh,* Edward Lin, MD,† Margaret Ormanoski, DO,‡ Michael D. Darcy, MD,§ and Deborah J. Rubens, MD‡ Noninvasive cross-sectional imaging modalities include ultrasound, computerized tomography, and magnetic resonance imaging. Each of these imaging methods has unique applications for vascular imaging. This article will review the technical parameters of each of the 3 modalities, including specialized vascular techniques. The main vascular transplant complications will then be discussed with respect to the diagnostic criteria and applicability of each of the relevant modalities. Transplant complications including hepatic artery stenosis and thrombosis, stenosis and thrombosis of the portal vein or inferior vena cava, and hepatic vein stenosis will be discussed. Sequelae of hepatic artery stenosis including biliary necrosis will also be reviewed briefly. Tech Vasc Interventional Rad 10:191-206 © 2007 Elsevier Inc. All rights reserved. KEYWORDS liver transplant, Doppler ultrasound, magnetic resonance angiography, computed tomographic angiography, complications, stenosis
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maging modalities used to diagnose and monitor and treat postliver transplant complications include the major cross-sectional modalities of Doppler ultrasound (US), computed axial tomography (CT), and magnetic resonance imaging (MRI). Ultrasound is the initial imaging modality of choice because it is readily available, portable to the bedside, and offers real-time imaging and guidance. CT and MRI are used for problem solving when US imaging is suboptimal (ie, very slow flowing hepatic vessels) or to image vessels outside the view of US, which may be obscured by bowel or fluid collections. Each modality has its strengths and weaknesses, and also varying diagnostic efficacy depending on the institutional and community resources. To understand the complementary role each plays, it is important first to review their individual imaging techniques and diagnostic criteria.
*Vascular Interventional Radiology Section, Department of Imaging Sciences, University of Rochester Medical Center, Rochester, NY. †Department of Imaging Sciences, University of Rochester Medical Center, Rochester, NY. ‡Body and Cross-Sectional Imaging Section, Department of Imaging Sciences, University of Rochester Medical Center, Rochester, NY. §Interventional Radiology Section, Mallinckrodt Institute of Radiology, Washington University, St Louis, MO. Address reprint requests to Wael E.A. Saad, MBBCh, Vascular Interventional Radiology Section, Department of Imaging Sciences, University of Rochester Medical Center, 601 Elmwood Ave, Box 648, Rochester, NY 14618. E-mail: [email protected].
1089-2516/07/$-see front matter © 2007 Elsevier Inc. All rights reserved. doi:10.1053/j.tvir.2007.09.014
Imaging Techniques Doppler Ultrasonography Doppler ultrasonography provides an accurate, versatile, and rapid assessment of the hepatic and portal vasculature. It can be performed perioperatively or at the bedside. The quality of the scan depends on the size of the patient, available acoustic windows, transducer type and frequency, and experience of the sonographer. Larger patients are more technically challenging to scan than thinner patients. The presence of surgical dressings may also limit the acoustic window. A curved transducer is commonly used to evaluate the vasculature with color and spectral analysis. Transducer frequencies typically range from 3.5 to 5 MHz, although lower frequencies may be used with larger patients. Because resolution and Doppler sensitivity improve with higher frequencies, the highest possible frequency transducer should be used to optimize the examination. Scanning is performed through a combination of transabdominal, subcostal, and intercostal windows. The patient is placed in the supine position for transabdominal and subcostal scanning, and in the left lateral decubitus position for intercostal scanning. The different approaches allow optimal visualization and assessment of each hepatic and portal vessel, with respect to location and direction of flow. For example, the intercostal approach often provides the best window to evaluate the vessels within the posterior segment of the right hepatic lobe.1 The subcostal approach provides good visualization of the prox191
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Computed Tomography and Angiography
Figure 1 Normal. (A) Doppler ultrasound evaluation of the intrahepatic arteries with normal spectral wave form analysis in an adult liver transplant recipient. Right hepatic artery (RHA) evaluation showing an arterial resistive index (RI) of 0.73. (B) Left hepatic artery (LHA) evaluation showing an arterial resistive index (RI) of 0.60.
imal hepatic veins as they empty into the inferior vena cava (IVC). Complete evaluation of the hepatic and portal vessels includes color and spectral Doppler analysis. Color Doppler provides information regarding the presence and direction of flow, as well as the location of turbulent flow in a poststenotic segment. Spectral analysis provides the direction, velocity, and phasicity of flow. Scanning parameters should be optimized while performing the examination. These parameters include the location of the focal zone, the depth of field, the 2-dimensional (2D) gain, the pulse repetition frequency, the wall filter, and the Doppler angle.1 The sonographer should be aware of how these factors may affect the sensitivity and quality of the scan. For instance, because color information is superimposed on a 2D image, a high 2D gain will suppress color and vice versa.1 The pulse repetition frequency should also be decreased to the lowest possible setting before aliasing occurs. If flow is difficult to detect within vessels, the wall filter can also be decreased. During spectral analysis, scanning should be per-
Computed tomography (CT) has made significant advances over the past 2 decades, beginning with the singleslice helical CT in the early 1990s to the development of multiple-slice helical CT scanners 10 years later. CT is a rapid imaging modality and provides an excellent anatomical overview with high spatial resolution. The use of intravenous contrast allows improved tissue contrast, tumor characterization, and evaluation of the vasculature. CT angiography (CTA) has replaced conventional angiography as the primary imaging modality in preoperative evaluation and planning for hepatic resection or liver transplantation and postsurgical evaluation. Contrast uptake by the liver and opacification of vessels depends on numerous factors including the volume of contrast administered, iodine content, site of injection, cardiovascular circulation time, and vascular supply to the liver. Due to the biphasic nature of the hepatic blood supply, the timing of the scan is critical in capturing information regarding the enhancement of the hepatic parenchyma and vasculature. The 3 phases of blood flow to the liver are the (1) arterial phase, (2) redistribution phase, and (3) equilibrium phase.2 The arterial phase begins approximately 20 seconds after the injection of contrast and lasts approximately 10 to 15 seconds. The attenuation of the abdominal aorta rapidly reaches a peak immediately following completion of the contrast injection, and the attenuation of the liver attains approximately one-half of the aorta’s attenuation.2 During the redistribution phase, the attenuation within the aorta rapidly diminishes and the attenuation of the liver remains constant or slowly increases secondary to the addition of contrast through the portal circulation. The equilibrium phase describes the gradual diminishment and equalization of contrast within the aorta and liver secondary to renal excretion.2 Contrast is typically administered by a mechanical pump through an 18- to 20- gauge intravenous line. Nonionic contrast is injected at a rate ranging from 1 to 5 mL/sec, and an iodine concentration of 300 mg/mL for nonarterial and 300 to 350 mg/mL for arterial studies. Faster injection times are needed for arterial studies. A biphasic study should include 3 separate scans: a noncontrast, an arterial phase, and portal venous phase scan. The arterial phase scan should begin 20 to 25 seconds after injection, and the portal venous phase scan should begin 50 to 60 seconds after injection.2 Five-millimeter slice thickness is sufficient for evaluation of the liver parenchyma. Thinner slices with a thickness of 1-1.5 mm and reconstruction interval of 1 mm are required for CTA studies.3 Three-dimensional (3D) angiogram reconstructions are created at a separate workstation. This postprocessing of original source data can be performed to produce multiplanar reformation (MPR) or maximal intensity projection (MIP) images. MPR displays only a selected plane inside a 3D volume. The selected plane may be either straight or curved. Because MPR relies on the operator to manually select the planes, MPR is prone to false-positive or negative findings.4 With MIP,
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Figure 2 Hepatic artery stenosis (HAS). (A) Doppler ultrasound evaluation of the main hepatic artery (MHA) with spectral wave form analysis in an adult liver transplant recipient. The MHA evaluation shows an arterial resistive index (RI) of 0.38. (B) Same Doppler evaluation as A. The left hepatic artery (LHA) evaluation showing an arterial resistive index (RI) of 0.42. (C) Digital subtraction angiogram of the hepatic artery of the same patient showing a long segment anastomotic stenosis (arrowheads).
only the highest-attenuation voxels within a selected volume or slab are displayed. Another technique, called a sliding thin slab MIP, produces multiple consecutive MIP, created from a thin slab MPR, which is moved along the course of the vessel.5 A thin slab MIP is therefore created from every selected thin slab MPR, and is sometimes advantageous when background attenuation is high.
Magnetic Resonance Imaging Magnetic resonance imaging (MRI) offers several benefits over US and CT, including improved contrast resolution, tissue and fluid characterization, and biliary and pancreatic duct and portal vein imaging without the use of intravenous contrast. Disadvantages include decreased spatial resolution compared with CT, longer scan times, and limitations by respiratory motion and susceptibility artifact. Tissue and fluid contrast are generated by differences in T1 and T2 values. In general, fat, protein, and subacute blood products result in T1 shortening and therefore high signal on T1weighted sequences. In contrast, fluid results in high signal and iron and fibrosis in low signal intensity on T2-weighted sequences. Because a full discussion of magnetic resonance imaging of the liver is beyond the scope of this article, dis-
cussion will focus on magnetic resonance cholangiopancreatography (MRCP) and magnetic resonance angiography (MRA). Magnetic resonance cholangiopancreatography. MRCP provides noninvasive imaging of the pancreatic and biliary ducts. MRCP is a relatively new technique, and protocols vary from institution to institution. Acquisition of MRCP relies on heavily T2-weighted imaging using fast spin echo (FSE) or single-shot fast spin echo techniques (SSFSE). FSE uses a series of rapid 180-degree rephasing pulses, resulting in multiple echoes. A different phase encoding gradient is used for each echo, thereby reducing the time of scanning. The echo train length defines the number of rephasing pulses, that is, the higher the echo train, the shorter the imaging time, and the more heavily T2-weighted the image. A sample parameter for FSE MRCP consists of a long echo train (ie, 32), a long repetition time (3-5 respiratory cycles, 8000-10,000 msec), a time to echo (TE) greater than 250 msec, 3 excitations, thin collimation, and fat saturation.6 Total imaging time is approximately 4 to 6 minutes.6 In SSFSE, the entire raw data are acquired using a single excitation pulse. Roughly half of the raw data are required to
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W.E.A. Saad et al. consists of a very long echo train (ie, 128), an infinite time to resonance (TR), a TE greater than 800 msec (which suppresses signal from extraductal structures and eliminates the need for fat saturation), 1 excitation, and thin and thick collimation.6 Total imaging time for both single- and multisection imaging is approximately 30 seconds.6 Single thick section acquisition is performed in multiple coronal and coronal oblique planes around a chosen axis anterior to the porta hepatis. Each section is approximately 20 mm thick and several planes are used to acquire a volume of data from the entire biliary and pancreatic ducts. Multisection acquisition is performed in the straight coronal plane using 5-mm-thick sections and 100% overlap. Maximal intensity projections (MIP) are often performed to provide a 3D image of the biliary and pancreatic ducts, similar to a conventional cholangiogram. MIP gives an overview of the biliary and pancreatic ducts and presents images in a manner more familiar to clinicians. However, volume averaging reduces spatial resolution and MIP reconstructions consequently do not replace careful evaluation of source images. Magnetic resonance angiography. MRA is typically performed with gadolinium contrast agents, using a T1-
Figure 3 Hepatic artery thrombosis (HAT) with normal resistive indices. (A) Doppler ultrasound evaluation of the Intrahepatic artery with spectral wave form analysis in an adult right lobe living related liver transplant recipient. The spectral wave form evaluation shows an arterial resistive index (RI) of 0.61. (B) Digital subtraction angiogram of a phrenic artery (white arrows) of the same patient showing collateral branches (most lateral white arrow) entering at the dome of the liver to reconstitute the intrahepatic arterial branches of the right lobe graft (arrowheads), indicating complete hepatic artery thrombosis with collaterals and a false-negative Doppler ultrasound.
obtain a full image using half-Fourier transform techniques. A different phase encoding step is ascribed to each echo. SSFSE significantly reduces imaging time (one breath hold) due to the long echo train and improves the signal to noise ratio. However, the decrease in overall signal results in decreased spatial resolution. A sample parater for SSFSE MRCP
Figure 4 High arterial resistive index (RI). (A) Doppler ultrasound evaluation of the main hepatic artery (MHA) with spectral wave form analysis in an adult liver transplant recipient 1 day after transplantation. The MHA evaluation shows an arterial resistive index (RI) of 0.99 with diastolic flow reversal. (B) Similar Doppler evaluation as A on the same patient 48 hours later. The MHA evaluation demonstrates a normalized arterial resistive index (RI) of 0.81.
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Figure 5 Hepatic artery stenosis (HAS), CTA versus conventional angiography. (A) Contrast-enhanced CT axial image with a magnified inset of the celiac axis. The images show a hepatic artery stenosis at the anastomosis (arrowheads). Ao, aorta (abdominal); CAx, celiac axis (celiac trunk); SA, splenic artery; CHA, common hepatic artery (native/recipient artery); NHA, native proper hepatic artery; GHA, graft proper hepatic artery. (B) Advanced vessel analysis of the above contrast-enhanced CT including a traced maximum intensity projection (MIP) in the upper half of the image. The analysis demonstrates the significant anastomotic stenosis again (arrowheads) and estimates it to be a 61% crosssectional area reduction. (C) Digital subtraction angiogram of the transplant hepatic artery of the same patient at a right-anterior-oblique (RAO) projection showing the same significant anastomotic stenosis (arrows). (D) Inversed (light background, dark vessels) maximum intensity projection (MIP) the above contrast-enhanced CT at a slightly obliqued coronal projection to simulate the DSA image of C. Very similarly to the DSA, the anastomotic stenosis is again noted (arrows).
weighted 3D gradient echo sequence and breath holding. Precontrast images are obtained, followed by a postcontrast volume, typically whatever can be acquired in a 20- to 30second breath hold. If a 3D acquisition is used, the plane of imaging is most often coronal. If a 2D acquisition is used,
axial imaging is common with thicker slices. In general 3D imaging is used for hepatic arterial imaging, while portal venous MRA can be done with either 2D or 3D acquisition, given the larger size of the vessel and less need for very thin slices for resolution.7 Patients who are unable to sustain a
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Figure 6 Hepatic artery anastomotic pseudoaneurysm. (A) Doppler ultrasound evaluation of the porta hepatis demonstrating a 2.0 ⫻ 2.5-cm saccular lesion (between arrowhead and arrow) with multidirectional flow. The arrowhead points to the sac portion with blood flow (red) going toward the transducer while the arrow points to the sac portion with blood flow (blue) going away from the transducer. These findings are consistent with an extrahepatic pseudoaneurysm of the hepatic artery. (B) Transverse Doppler ultrasound evaluation of the porta hepatis demonstrating the same pseudoaneurysm as in A (hollow arrowhead). The solid arrowhead points to the source hepatic artery (common hepatic artery). The arrow points to the neck where turbulent flow is noted. (C) Contrast-enhanced CT axial image at the level of the celiac axis of the same patient as in A and B. The images show the large pseudoaneurysm in the vicinity of the hepatic artery anastomosis (arrowhead). The hollow arrow points to the recipient hepatic artery. The solid arrow points to the distal/graft hepatic artery. L, liver; S, stomach. (D) Sagittal reformat of the contrast-enhanced CT of C. The images show the large pseudoaneurysm in the vicinity of the hepatic artery anastomosis (hollow arrowhead). The solid arrowhead points to the proximal/recipient hepatic artery. L, liver; Ao, aorta (abdominal); CAx, celiac axis (celiac trunk); SMA, superior mesenteric artery.
20-second breath hold for an entire coronal or axial volume may have portal venous imaging performed in 2 overlapping sequential axial acquisitions. Typical coronal 3D volume parameters include a TR/TE of 4.6 to 5/1.8 to 2, a slice thickness of 3 to 3.5 mm, a slab thickness of 96 to 112 mm, 24 to 32 partitions, matrix size of 150 ⫻ 256 or 200 ⫻ 512, field of view of 35 to 40 cm, and acquisition time of 19 to 23 seconds.8 The usual dose of gadolinium is 30 mL delivered at 3 to 5 mL/sec using a timing bolus or detection of a certain degree of enhancement by the scanner using real-time bolus monitoring software.7,8 The injection is followed by a 10-mL saline flush. The arterial phase image is derived by viewing an MIP reformat. Additional detail for small vessels can be obtained by subtracting the unenhanced volume from the enhanced volume. Portal phase imaging is performed with similar parameters
with a 20-second interscan delay following the end of each preceding scan.8 MRA is less accurate than CTA for detecting hepatic artery thromboses and stenoses due to less technically adequate examinations due to patient motion or inability to sustain a long enough breath hold. In addition the spatial resolution of CT exceeds that of MR, despite the enhanced soft tissue contrast of MR. Kim and coworkers concluded that MR is sensitive (100%) but not specific (74%) with a positive predictive value of only 29% in the detection of significant hepatic artery stenosis (HAS).8 MR significantly overestimated the presence of stenosis, with only 3 of 19 patients called positive for a 50% or greater stenosis on MRI actually having stenosis as compared with angiography, and of 5 patient’s arteries said to be occluded by MRI 4 actually had a stenosis on conventional angiography and 1 had no significant stenosis.
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Figure 7 Intrahepatic arterial pseudoaneurysm. (A) Digital subtraction angiogram of the transplant hepatic artery demonstrating a small intrahepatic pseudoaneurysm (large single arrowhead). Adjacent to the pseudoaneurysm is a narrowing of the segment of the involved right intrahepatic artery branch (arrowheads). (B) Contrast-enhanced CT axial image at the level of the celiac axis of the same patient as A. The images show the small pseudoaneurysm (see C for magnified details). (C) Magnified CT image (right) of the boxed area in B with an adjacent labeled line drawing (left). The small pseudoaneurysm (arrowhead) was missed and was considered a continuum of a normal caliber intrahepatic arterial branch. In actuality, the involved intrahepatic arterial segment (between the arrows) is narrowed as it passes between the biliary stent (seen en face) and the small (7 mm) pseudoaneurysm (arrowheads). Ao, aorta (abdominal); CAx, celiac axis (celiac trunk); SpA, splenic artery; CHA, common hepatic artery (native/recipient artery); IVC, inferior vena cava.
Diagnostic Criteria for Vascular Complications Hepatic Artery Stenosis and Thrombosis On Doppler ultrasound the normal hepatic artery has a low resistance waveform with continuous diastolic flow and a resistive index (as defined by peak systolic velocity minus end diastolic velocity all divided by peak systolic velocity) of between
0.60 and 0.80. It normally has a brisk, fairly vertical upstroke as well (Fig. 1). Dodd and coworkers used the threshold of a resistive index less than 0.50 in any of the hepatic vessels to diagnose either hepatic artery thrombosis or stenosis with a sensitivity of 60% and a specificity of 77%9 (Fig. 2). When the acceleration time of greater than 0.08 second was used for diagnosis, this yielded a sensitivity/specificity of 53% and 86%, respectively.9 The reason abnormal intrahepatic arterial flow is detected in the
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Figure 8 Arterioportal fistula by Doppler ultrasound. (A) Doppler ultrasound evaluation of the left hepatic artery (LHA) of a transplant recipient with a right hepatic artery to portal vein fistula. The LHA is not involved and has a normal wave form with an arterial resistive index (RI) of 0.81. (B) Doppler ultrasound evaluation of the right hepatic artery (RHA) of the same transplant recipient. The RHA is involved and has a reduced arterial resistive index (RI) of 0.37. The high diastolic flow reflects the reduced peripheral arterial resistance as the arterioportal fistula shunts blood without resistance from the hepatic artery to the portal vein. (C) Doppler ultrasound evaluation of the right portal vein (RPV) of the same transplant recipient. The RPV branch that is involved exhibits aliasing and turbulence (mottled coloring involving the entire color spectrum) (arrowhead). The remainder of the RPV demonstrates normal directional flow (Red: arrows). (D) Doppler ultrasound evaluation with spectral wave form analysis right at the arterioportal fistula of the same transplant recipient. The spectral wave form analysis demonstrates significant flow through the fistula at approximately 150 cm per second.
presence of thrombosis is due to collateral formation, which may be fairly rapid9,10 (Fig. 3). Absent arterial flow in all arteries on a technically adequate Doppler imaging study is nearly always indicative of thrombosis; however, false positives may occur due to severe hepatic edema, systemic hypotension, or in a suboptimal ultrasound study due to patient size or edema.11 A loss of diastolic flow or diastolic flow reversal has been implicated by Nolton and Sproat12 and by Garcia-Criado and coworkers13 as a sign of impending thrombosis, especially if it occurs in the main hepatic artery. In our experience this finding may reverse over time, sometimes requiring as long as a week to correct (Fig. 4). In other patients it may actually precede arterial thrombosis, so patients with loss of diastolic flow on spectral Doppler examination require close follow-up. The most specific sign of hepatic arterial stenosis is a focal velocity elevation of greater than 2 mo/sec, which, if present, is predictive 96% of the
time.9 However, the most common site of stenosis is at the arterial anastomosis, which is often difficult to image at ultrasound, as it is frequently obscured by bowel. In fact, in 20 cases of stenosis reported by Dodd and coworkers, only 1 patient had a focal velocity elevation of greater than 2 mo/sec detected in the hepatic artery.9 Thus the velocity elevation criterion is less useful in a screening examination. On CT or MRI, hepatic artery thrombosis is defined as nonvisualization of the hepatic artery (main or a branch) on arterial phase imaging. If collaterals are present, small intrahepatic arteries may still be visualized.14 HAS is identified as focal narrowing of a vessel by more than 50% diameter reduction.15 Because the vessel pathways are often in and out of the plane of image acquisition, stenoses are often better displayed on postprocessed images using either MIP or multiplanar reformats15 (Fig. 5). Stenoses
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Figure 9 Arterioportal fistula (APF) by contrast-enhanced CT. Contrast-enhanced CT axial image at the level of the upper abdomen of the same liver transplant recipient as Figure 8 with a right hepatic lobe APF. The images show an early and more avid enhancing right portal venous radical (solid arrowhead). This enhances more than the remainder of the portal vein (hollow arrowhead). In addition the hepatic segment (arrows) fed by the involved portal vein enhances ahead of the remainder of the hepatic parenchyma (see Figures 6 and 7, Chapter IV).
199 tend to be overestimated by CT as compared with conventional angiography.16 CTA has been calculated to overestimate HAS by approximately 13%.16 CTA has a sensitivity, specificity, and accuracy for detecting extrahepatic HAS of 88 to 100%, 89%, and 95%, respectively.16-18 The sensitivity of CTA in detecting extrahepatic HAS drops from 88 to 100% down to 83% for intrahepatic HAS.16 The positive and negative predictive values for CTA in this setting are 92% and 100%, respectively.18 The advantage of CTA over Doppler ultrasound is its 24-hour availability and that CTA is not operator dependent. However, CTA can be nondiagnostic in a minority of cases (4%), ranging from 0 to 9% of cases due to poor injection/scanning timing.15-18 In addition, the intravenous contrast load may not be tolerable for liver transplant recipients with hepatorenal syndrome (renal insufficiency). MRA is similarly suboptimal in patients with impaired renal function due to the risk of gadolinium-induced nephrogenic systemic fibrosis. This combined with a higher rate of suboptimal exams due to patient motion and inadequate breath holding make MR a less desirable imaging choice than US or CT.
Hepatic Artery Pseudoaneurysms Hepatic artery pseudoaneurysms occur most frequently at the anastomosis, and thus may be difficult to detect with US.13 Because pseudoaneurysms are extrahepatic they are often hidden behind bowel gas. In addition, sonographers may not visualize the entire extrahepatic main hepatic artery
Figure 10 Complete portal vein thrombosis (PVT). (A) Doppler ultrasound evaluation of a transplant recipient with complete thrombosis of the portal vein (P). The portal vein has no flow on color Doppler; however, the adjacent hepatic artery is visualized. This is consistent with portal vein thrombosis or very slow flow in the portal vein. (B) Power Doppler ultrasound evaluation of the same transplant recipient with complete thrombosis of the portal vein (P). The portal vein still does not light up on power Doppler; however, the surrounding arterial supply is visualized by color Doppler. This is consistent with portal vein thrombosis or very slow flow in the portal vein. (C) Contrast-enhanced CT of the same patient. The axial image is at the level of the celiac axis. The images show no enhancement of the portal vein (arrows). Around the thrombosed portal vein (P) is a slight rim of enhancement. The hepatic arteries enhance (arrowheads).
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Figure 11 Partial portal vein thrombosis (PVT). (A) Gray scale ultrasound evaluation of a transplant recipient with a shallow heterogeneous echogenic mass (arrowhead) along the wall of the main portal vein. This is consistent with chronic partial thrombosis of the portal vein (P). (B) Color Doppler ultrasound evaluation of a transplant recipient with the same thrombus (arrowhead) along the wall of the main portal vein. This is consistent with partial thrombosis of the portal vein. (C) Unenhanced CT axial image at the level of the upper abdomen of the same liver transplant recipient as in Figure 10A and B. The portal vein visualized is intrahepatic and not extrahepatic, however. The images demonstrate a high density portal vein thrombus (arrows).
and may overlook small pseudoaneurysms particularly if the hepatic artery is tortuous. A pseudoaneurysm is identified on US as a cystic structure in communication with the hepatic artery with a disorganized “to and fro” color and spectral Doppler pattern as the arterial blood flows into and out of the pseudoaneurysm (Fig. 6A, B). In a prospective study comparing US to CTA, US detected 13% of aneurysms while CTA detected 78%. CT or MRI performed in the arterial phase show a brightly enhancing round mass adjacent to a hepatic artery, enhancing with the same intensity as the adjacent arterial blood (Fig. 6C, D). One reason for false a false-negative CTA examination is very small pseudoaneurysm, particularly if it compresses an adjacent artery and narrows it to the extent that the radiologist would see the small pseudoaneurysm as a continuum of a normal caliber artery (Fig. 7), that is, missing both abnormalities, the outpouching, and adjacent luminal narrowing.
Hepatic Artery to Portal Vein Fistula This may occur as a complication of a pseudoaneurysm11 or as a result of liver biopsy.14,19,20 Biopsy-induced shunts occur in as many as 50% of patients if scanned at 1 week post biopsy, but drop to 10% thereafter as most close spontaneously.21,22 On US the inflowing hepatic arterial resistive index
will be lower than the contralateral normal vessel on the opposite side. In addition, reversed flow in particular portal vein radicals (considered a rare finding), arterialized portal vein waveform as well as a focus of turbidity with aliasing at the site of the arterioportal fistula can also be seen20,23-25 (Fig. 8). On CT the portal vein may show early enhancement in the arterial phase of injection before the enhancement of the main portal vein, or enhancement of the portal vein before enhancement of the mesenteric and splenic veins14,20 (Fig. 9; also see Figures 6 and 7 in this issue, pages 196-199. A less common sign includes transient wedge-shaped parenchymal enhancement during the hepatic arterial phase of injection20 (Fig. 9; also see Figures 6 and 7 in this issue, pages 196-199.
Portal Vein Thrombosis This is a relatively rare complication, occurring in 1 to 3% of patients,14,26 but seen more commonly with redundant vessels or trauma to the vessel at surgery.11 On US there is either total absence of flow in the portal vein on color Doppler (Fig. 10), or a mass filling in a portion of the portal vein and partially occluding it (Fig. 11). The CT or MR appearance is similar when contrast is used. The vessel is either absent or there is a nonenhancing mass occupying a portion of the vein (Fig. 10). On noncontrast CT the portal vein thrombus can
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Figure 12 Portal vein stenosis. (A) Gray scale ultrasound evaluation of the main portal vein at the anastomosis demonstrating a significant stenosis at the anastomosis (arrows). A part of this apparent narrowing is possibly a diameter mismatch between the recipient and graft portal veins; however, the dynamic findings of B-D indicate a hemodynamically significant portal vein stenosis. (B) Doppler ultrasound evaluation of the main portal vein at the anastomosis demonstrating a significant stenosis at the anastomosis (arrows). There is turbulent high velocity flow with aliasing at and distal to the anastomotic portal vein stenosis. (C) Doppler ultrasound evaluation of the portal vein of the same transplant recipient proximal to the anastomotic stenosis. The spectral wave form analysis shows a velocity of approximately 40 cm per second (41 cm/sec) proximal to the anastomosis. (D) Doppler ultrasound evaluation of the portal vein of the same transplant recipient distal to the anastomotic stenosis. The spectral wave form analysis shows a velocity of approximately 186 cm per second (185 cm/sec) distal to the anastomosis. This computes to a 4.5-fold increase in velocity from 40 cm/sec to 185 cm/sec. The threshold for calling a significant stenosis is a velocity greater than 125 cm/sec and a velocity increase of more than 3-fold.
have increased attenuation relative to the surrounding liver (Fig. 11C). However, with contrast enhancement, the portal vein thrombus becomes relatively less dense (Fig. 10C). Acutely the vessel is distended. As the thrombus becomes more chronic the vessel narrows and scars and the thrombus becomes more echogenic on US. Acute portal vein compression due to hematoma or biloma may produce symptoms similar to thrombosis, and cause nonvisualization of the main portal vein on US.
uation of the portal vein (Fig. 12). On US the predictive features include a focal velocity greater than 125 cm/sec or a 3-fold increase in velocity with a sensitivity of 73% and a specificity of 95 to 100%, respectively27 (Fig. 12C, D). Portal venography with pressure measurements remains the most reliable examination (gold standard). When a clinically significant stenosis is present, there is a greater than 5-mm gradient measured across the lesion on direct arterial portography.14
Portal Vein Stenosis
Hepatic Vein Thrombosis or Stenosis
Focal narrowing of the portal vein on US, CT, or MRI may represent discrepancy between donor and recipient portal vein size, or may indicate a true stenosis.14 Diameter discrepancy by CT or MRI may be overcalled as portal vein stenoses. Ultrasound may provide the most dynamic noninvasive eval-
Doppler examinations in a patient with hepatic vein stenosis will show decreased mean velocities in both the hepatic veins and portal vein. The hepatic vein wave form will be significantly dampened when there is an outflow obstruction.28 Typically the Doppler waveform in a nor-
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Figure 13 Hepatic vein stenosis. (A) Doppler ultrasound evaluation of the middle hepatic vein demonstrates a normal posttransplant biphasic spectral wave form with a mean velocity of 25 to 30 cm per second. (B) Doppler ultrasound evaluation of the right hepatic vein at the stenosis demonstrates aliasing. The spectral wave form shows a mean velocity of 100 cm per second. (C) Doppler ultrasound evaluation of the right hepatic vein proximal to the stenosis demonstrates a monophasic (flattened) spectral wave form with a mean velocity of 10 cm per second.
mal hepatic vein is triphasic, but after transplantation the waveform is often biphasic even without any other signs or symptoms of flow obstruction29 (Fig. 13A). However, when significant stenosis develops the waveform usually degrades to a monophasic pattern (Fig. 13C). Other findings may include reversal of hepatic vein flow, accelerated flow with aliasing just beyond the stenosis (Fig. 13B), and visualization of the stenosis on gray scale imaging. By CT, direct visualization of the stenosis can be seen (Fig. 14). In addition, perfusion abnormalities can also be noted, although they are nonspecific.
Inferior Vena Cava Thrombosis or Stenosis This is also a rare complication occurring in less than 1% of cases.11 The appearance of thrombosis is similar to that in the portal vein, with a space-occupying mass obliterating (in the case of complete thrombosis) or narrowing (in partial thrombosis) either the colorized portion of the vessel on color Doppler, or the contrasted lumen on CT or MR (Fig. 15). Stenosis most frequently occurs at the anastomosis. Ultrasound will show a focal narrowing with a 3- to 4-fold increase in velocity as compared with the prestenotic segment. If the stenosis is in the suprahepatic por-
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203 diagnosed by cholangiography; however, they can be identified on US, CT, or MRI as focal biliary duct dilation proximal to the area of stricture. Anastomotic strictures occur from post surgical scarring, whereas nonanastomotic strictures occur more proximally in the liver due to ischemia as a consequence of hepatic artery stenosis or thrombosis. These strictures often start at the hilum and progress to the intrahepatic bile ducts.14 With severe injury, the epithelium sloughs due to biliary necrosis. By US the biliary tree is markedly dilated and the lumen filled with debris (Fig. 18). The lumen itself may not be visible, only the periportal increased echogenicity, which may or may not conform to the normal biliary branching pattern (Fig. 19). On CT the biliary tree is dilated and irregular and of decreased attenuation as compared with the enhancing hepatic parenchyma (Fig. 18).
Summary
Figure 14 Hepatic vein stenosis. Contrast-enhanced CT axial image at the level of the upper abdomen in a liver transplant recipient with a “piggyback” caval anastomosis. The donor/graft inferior vena cava (IVC) is indicated by the hollow arrowhead. The native/recipient IVC is indicated by the solid arrowhead. The images show a right hepatic vein stenosis as it enters the IVC (between arrows).
tion of the vessel, there may be reversed flow or dampened waveforms with absent phasicity in the hepatic veins11 (Fig. 16). Chong and coworkers used the venous pulsatility index, defined as the peak venous velocity minus the minimum venous velocity all divided by the peak velocity.27 Normal vessels had an index of 0.75, while stenoses were associated with a low index, with a mean value of 0.39.27 Delayed stenoses may occur secondary to fibrosis. CT or MRI will show severe narrowing of the IVC at the point of stenosis, with only a minimal residual lumen (Figs. 16B and 17).
Noninvasive imaging of hepatic transplant complications is performed by all 3 major cross-sectional imaging modalities, US, CT, and MRI. Ultrasound is often used to screen for vascular abnormalities, including hepatic arterial stenosis and thrombosis, and the less common thromboses or stenoses of the portal vein, hepatic veins, and inferior vena cava. Precise anatomy of the vascular abnormalities is often better determined on CT or MR, especially when a focal stenosis occurs in the distal IVC, or in the hepatic artery proximal to the porta hepatis where it is difficult to image directly by US. CTA and MRA give detailed imaging of the small hepatic arteries, while US tends to give more physiologic data. All 3 modalites require angiographic correlation with pressure gradients across a stenosis to determine its physiologic significance. MRCP can be valuable to detect focal biliary abnormalities; however, direct cholangiography remains the gold standard for biliary complications.
Diagnostic Criteria for Biliary Complications Biliary complications are the most common transplant sequelae, occurring in up to 25% of allografts.11 Complications include leaks, strictures, biliary necrosis, and abscess formation. Leaks are most commonly confirmed with cholangiography. When imaged by US, CT, or MRI they are cystic fluid collections that lack enhancement on CT or MR, often located in the porta hepatic or adjacent to the liver, often at the T-tube site. Strictures are also most often
Figure 15 Partial inferior vena cava (IVC) thrombosis. Doppler ultrasound evaluation of an adult transplant recipient. This is transverse to the inferior vena cava. The IVC is mostly thrombosed (arrow). The residual patent lumen (blue, arrowhead) is seen.
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Figure 16 Inferior vena cava (IVC) stenosis. (A) Color Doppler ultrasound evaluation of the inferior vena cava (IVC). The transducer is along the longitudinal axis of the IVC. There is progressive narrowing of the IVC with a significant stenosis at the level of the arrowheads. (B) Axial MR image at the level of the upper abdomen shows a pinhole residual lumen (arrowhead) due to the significant stenosis seen in the Doppler examination of A. (C) Digital subtraction inferior vena-cavogram demonstrates the significant suprahepatic IVC stenosis (arrows) close to the IVC-right atrial (RA) junction. IVC, inferior vena cava; RRV, right renal vein; LRV, left renal vein.
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Figure 17 Inferior vena cava (IVC) stenosis. Contrast-enhanced CT axial image at the level of the upper abdomen in a liver transplant recipient. There is a significant IVC stenosis (arrow). Notice the ascites indicating graft dysfunction that may be due to graft outflow vein obstruction (the IVC stenosis).
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Figure 19 Biliary necrosis. Gray scale ultrasound image of an adult transplant recipient with hepatic artery thrombosis (HAT). The image demonstrates dilated bile ducts with nodular echogenic debris (arrows).
Figure 18 Central biliary necrosis. (A) Percutaneous transhepatic cholangiogram (PTC) showing disproportionate central biliary dilation (arrowheads) with irregular shaggy borders consistent with biliary necrosis (N) due to graft ischemia (dearterialization). The peripheral ducts (arrows) are spared at this moment in time. (B) Axial CT image at the level of the celiac axis of the same patient as in A showing dilated central bile ducts (arrowhead) with air within the central necrotic (N) ducts (arrow). (C) Gray scale ultrasound image depicting the same findings as in A and B on the same transplant recipient. There are irregular central necrotic (N) areas. The arrows point to dilated ducts (arrows).
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References 1. Kruskal JB, Newman PA, Sammons LG, et al: Optimizing Doppler and color flow US: application to hepatic sonography. Radiographics 24: 657-675, 2004 2. Merkle EM, Boll DT, Brambs HJ: Liver: normal anatomy, imaging techniques, and diffuse diseases, in Haaga LC Jr, Gilkeson RC (eds): Computed Tomography and Magnetic Resonance Imaging of the whole body. St. Louis, MO, Mosby, 2003, pp 1318-1339 3. Fishman EK: CT angiography: clinical applications in the abdomen. Radiographics 21:S3-S16, 2001 (RSNA Refresher course) 4. Nakanishi T: Evaluation of coronary artery stenoses using electronbeam CT and multiplanar reformation. J Comput Assist Tomogr 21: 121-127, 1997 5. Napel S, Rubin GD, Jeffrey RB Jr: STS-MIP: a new reconstruction technique for CT of the chest. J Comput Assist Tomogr 17:832-838, 1993 6. Vitellas KM, Keogan MT, Spritzer CE, et al: MR cholangiopancreatography of bile and pancreatic duct abnormalities with emphasis on the single-shot fast spin-echo technique. Radiographics 20:939-957; quiz 1107-1108, 2000 7. Leiner T: Magnetic resonance angiography of abdominal and lower extremity vasculature. Top Magn Reson Imaging 16:21-66, 2005 8. Kim BS, Kim TK, Jung DJ, et al: Vascular complications after living related liver transplantation: evaluation with gadolinium-enhanced three-dimensional MR angiography. AJR Am J Roentgenol 181:467474, 2003 9. Dodd GD 3rd, Memel DS, Zajko AB, et al: Hepatic artery stenosis and thrombosis in transplant recipients: Doppler diagnosis with resistive index and systolic acceleration time. Radiology 192:657-661, 1994 10. Rollins NK, Timmons C, Superina RA, et al: Hepatic artery thrombosis in children with liver transplants: false-positive findings at Doppler sonography and arteriography in four patients. AJR Am J Roentgenol 160:291-294, 1993 11. Crossin JD, Muradali D, Wilson SR: US of liver transplants: normal and abnormal. Radiographics 23:1093-1114, 2003 12. Nolten A, Sproat IA: Hepatic artery thrombosis after liver transplantation: Temporal accuracy of diagnosis with duplex US and the syndrome of impending thrombosis. Radiology 198:553-559, 1996 13. Garcia-Criado A, Gilabert R, Salmeron JM, et al: Significance of and contributing factors for a high resistive index on Doppler sonography of the hepatic artery immediately after surgery: prognostic implications for liver transplant recipients. AJR Am J Roentgenol 181:831-838, 2003 14. Quiroga S, Sebastia MC, Margarit C, et al: Complications of orthotopic liver transplantation: spectrum of findings with helical CT. Radiographics 21:1085-1102, 2001 15. Boraschi P, Donati F, Cossu MC, et al: Multi-detector computed tomog-
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raphy angiography of the hepatic artery in liver transplant recipient. Acta Radiol 46:455-461, 2005 Vignali C, Bargellini R, Cioni P, et al: Diagnosis and treatment of hepatic artery stenosis after orthotopic liver transplantation. Transpl Proc 36: 2771-2773, 2004 Piolanti M, Fabbro E, Pascali E, et al: CT angiography for the evaluation of adult orthotopic liver transplantation arterial complications. Radiol Med (Torino) 102:348-356, 2001 Brancatelli G, Katyal S, Federle MP, et al: Three-dimensional multi-slice helical computed tomography with volume rendering technique in the detection of vascular complications after liver transplantation. Transplantation 73:237-242, 2002 Saad WEA, Davies MG, Ryan CK, et al: Incidence of arterial injuries detected by angiography following percutaneous right-lobe ultrasound-guided core liver biopsies in human subjects. Am J Gastroenterol 101:2641-2645, 2006 Saad WEA, Davies MG, Rubens DJ, et al: Endoluminal management of arterio-portal fistulae in liver transplant recipients: a single center experience. Vasc Endovasc Surg 40:451-459, 2006 Hellekant C: Vascular complications following needle puncture of the liver. Acta Radiol Diagn 17:209-222, 1976 Hellekant C, Olint T: Vascular complications following needle puncture of the liver. An angiographic investigation in the rabbit. Acta Radiol Diagn 14:577-582, 1973 Chavan A, Harms J, Picjlmayr R, Galanski M: Transcatheter coil occlusion of an intrahepatic arterioportal fistula in a transplanted liver. Bildgebung 60:215-218, 1993 Strodel E, Eckhauser FE, Lemmer JH, Whitehouse M Jr, Williams DM: Presentation and perioperative management of arterioportal fistulas. Arch Surg 122:563-571, 1987 Glockner JF, Forauer AR: Vascular or ischemic complications after liver transplantation: pictorial essay. AJR Am J Roentgenol 173:1055-1059, 1999 Uzochukwu LN, Bluth EI, Smetherman DH, et al: Early postoperative hepatic sonography as a predictor of vascular and biliary complications in adult orthotopic liver transplant patients. AJR Am J Roentgenol 185: 1558-1570, 2005 Chong WK, Beland JC, Weeks SM: Sonographic evaluation of venous obstruction in liver transplants. AJR Am J Roentgenol 188:515-521, 2007 Egawa H, Tanaka K, Uemoto S, et al: Relief of hepatic vein stenosis by balloon angioplasty after living-related donor liver transplantation. Clin Transpl 7(4):306-311, 1993 Fujimoto M, Moriyasu F, Someda H, et al: Recovery of graft circulation following percutaneous transluminal angioplasty for stenotic venous complications in pediatric liver transplantation: assessment with Doppler ultrasound. Transpl Int 8(2):119-125, 1995
I
maging modalities used to diagnose and monitor and treat postliver transplant complications include the major cross-sectional modalities of Doppler ultrasound (US), computed axial tomography (CT), and magnetic resonance imaging (MRI). Ultrasound is the initial imaging modality of choice because it is readily available, portable to the bedside, and offers real-time imaging and guidance. CT and MRI are used for problem solving when US imaging is suboptimal (ie, very slow flowing hepatic vessels) or to image vessels outside the view of US, which may be obscured by bowel or fluid collections. Each modality has its strengths and weaknesses, and also varying diagnostic efficacy depending on the institutional and community resources. To understand the complementary role each plays, it is important first to review their individual imaging techniques and diagnostic criteria.
*Vascular Interventional Radiology Section, Department of Imaging Sciences, University of Rochester Medical Center, Rochester, NY. †Department of Imaging Sciences, University of Rochester Medical Center, Rochester, NY. ‡Body and Cross-Sectional Imaging Section, Department of Imaging Sciences, University of Rochester Medical Center, Rochester, NY. §Interventional Radiology Section, Mallinckrodt Institute of Radiology, Washington University, St Louis, MO. Address reprint requests to Wael E.A. Saad, MBBCh, Vascular Interventional Radiology Section, Department of Imaging Sciences, University of Rochester Medical Center, 601 Elmwood Ave, Box 648, Rochester, NY 14618. E-mail: [email protected].
1089-2516/07/$-see front matter © 2007 Elsevier Inc. All rights reserved. doi:10.1053/j.tvir.2007.09.014
Imaging Techniques Doppler Ultrasonography Doppler ultrasonography provides an accurate, versatile, and rapid assessment of the hepatic and portal vasculature. It can be performed perioperatively or at the bedside. The quality of the scan depends on the size of the patient, available acoustic windows, transducer type and frequency, and experience of the sonographer. Larger patients are more technically challenging to scan than thinner patients. The presence of surgical dressings may also limit the acoustic window. A curved transducer is commonly used to evaluate the vasculature with color and spectral analysis. Transducer frequencies typically range from 3.5 to 5 MHz, although lower frequencies may be used with larger patients. Because resolution and Doppler sensitivity improve with higher frequencies, the highest possible frequency transducer should be used to optimize the examination. Scanning is performed through a combination of transabdominal, subcostal, and intercostal windows. The patient is placed in the supine position for transabdominal and subcostal scanning, and in the left lateral decubitus position for intercostal scanning. The different approaches allow optimal visualization and assessment of each hepatic and portal vessel, with respect to location and direction of flow. For example, the intercostal approach often provides the best window to evaluate the vessels within the posterior segment of the right hepatic lobe.1 The subcostal approach provides good visualization of the prox191
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Figure 1 Normal. (A) Doppler ultrasound evaluation of the intrahepatic arteries with normal spectral wave form analysis in an adult liver transplant recipient. Right hepatic artery (RHA) evaluation showing an arterial resistive index (RI) of 0.73. (B) Left hepatic artery (LHA) evaluation showing an arterial resistive index (RI) of 0.60.
imal hepatic veins as they empty into the inferior vena cava (IVC). Complete evaluation of the hepatic and portal vessels includes color and spectral Doppler analysis. Color Doppler provides information regarding the presence and direction of flow, as well as the location of turbulent flow in a poststenotic segment. Spectral analysis provides the direction, velocity, and phasicity of flow. Scanning parameters should be optimized while performing the examination. These parameters include the location of the focal zone, the depth of field, the 2-dimensional (2D) gain, the pulse repetition frequency, the wall filter, and the Doppler angle.1 The sonographer should be aware of how these factors may affect the sensitivity and quality of the scan. For instance, because color information is superimposed on a 2D image, a high 2D gain will suppress color and vice versa.1 The pulse repetition frequency should also be decreased to the lowest possible setting before aliasing occurs. If flow is difficult to detect within vessels, the wall filter can also be decreased. During spectral analysis, scanning should be per-
Computed tomography (CT) has made significant advances over the past 2 decades, beginning with the singleslice helical CT in the early 1990s to the development of multiple-slice helical CT scanners 10 years later. CT is a rapid imaging modality and provides an excellent anatomical overview with high spatial resolution. The use of intravenous contrast allows improved tissue contrast, tumor characterization, and evaluation of the vasculature. CT angiography (CTA) has replaced conventional angiography as the primary imaging modality in preoperative evaluation and planning for hepatic resection or liver transplantation and postsurgical evaluation. Contrast uptake by the liver and opacification of vessels depends on numerous factors including the volume of contrast administered, iodine content, site of injection, cardiovascular circulation time, and vascular supply to the liver. Due to the biphasic nature of the hepatic blood supply, the timing of the scan is critical in capturing information regarding the enhancement of the hepatic parenchyma and vasculature. The 3 phases of blood flow to the liver are the (1) arterial phase, (2) redistribution phase, and (3) equilibrium phase.2 The arterial phase begins approximately 20 seconds after the injection of contrast and lasts approximately 10 to 15 seconds. The attenuation of the abdominal aorta rapidly reaches a peak immediately following completion of the contrast injection, and the attenuation of the liver attains approximately one-half of the aorta’s attenuation.2 During the redistribution phase, the attenuation within the aorta rapidly diminishes and the attenuation of the liver remains constant or slowly increases secondary to the addition of contrast through the portal circulation. The equilibrium phase describes the gradual diminishment and equalization of contrast within the aorta and liver secondary to renal excretion.2 Contrast is typically administered by a mechanical pump through an 18- to 20- gauge intravenous line. Nonionic contrast is injected at a rate ranging from 1 to 5 mL/sec, and an iodine concentration of 300 mg/mL for nonarterial and 300 to 350 mg/mL for arterial studies. Faster injection times are needed for arterial studies. A biphasic study should include 3 separate scans: a noncontrast, an arterial phase, and portal venous phase scan. The arterial phase scan should begin 20 to 25 seconds after injection, and the portal venous phase scan should begin 50 to 60 seconds after injection.2 Five-millimeter slice thickness is sufficient for evaluation of the liver parenchyma. Thinner slices with a thickness of 1-1.5 mm and reconstruction interval of 1 mm are required for CTA studies.3 Three-dimensional (3D) angiogram reconstructions are created at a separate workstation. This postprocessing of original source data can be performed to produce multiplanar reformation (MPR) or maximal intensity projection (MIP) images. MPR displays only a selected plane inside a 3D volume. The selected plane may be either straight or curved. Because MPR relies on the operator to manually select the planes, MPR is prone to false-positive or negative findings.4 With MIP,
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Figure 2 Hepatic artery stenosis (HAS). (A) Doppler ultrasound evaluation of the main hepatic artery (MHA) with spectral wave form analysis in an adult liver transplant recipient. The MHA evaluation shows an arterial resistive index (RI) of 0.38. (B) Same Doppler evaluation as A. The left hepatic artery (LHA) evaluation showing an arterial resistive index (RI) of 0.42. (C) Digital subtraction angiogram of the hepatic artery of the same patient showing a long segment anastomotic stenosis (arrowheads).
only the highest-attenuation voxels within a selected volume or slab are displayed. Another technique, called a sliding thin slab MIP, produces multiple consecutive MIP, created from a thin slab MPR, which is moved along the course of the vessel.5 A thin slab MIP is therefore created from every selected thin slab MPR, and is sometimes advantageous when background attenuation is high.
Magnetic Resonance Imaging Magnetic resonance imaging (MRI) offers several benefits over US and CT, including improved contrast resolution, tissue and fluid characterization, and biliary and pancreatic duct and portal vein imaging without the use of intravenous contrast. Disadvantages include decreased spatial resolution compared with CT, longer scan times, and limitations by respiratory motion and susceptibility artifact. Tissue and fluid contrast are generated by differences in T1 and T2 values. In general, fat, protein, and subacute blood products result in T1 shortening and therefore high signal on T1weighted sequences. In contrast, fluid results in high signal and iron and fibrosis in low signal intensity on T2-weighted sequences. Because a full discussion of magnetic resonance imaging of the liver is beyond the scope of this article, dis-
cussion will focus on magnetic resonance cholangiopancreatography (MRCP) and magnetic resonance angiography (MRA). Magnetic resonance cholangiopancreatography. MRCP provides noninvasive imaging of the pancreatic and biliary ducts. MRCP is a relatively new technique, and protocols vary from institution to institution. Acquisition of MRCP relies on heavily T2-weighted imaging using fast spin echo (FSE) or single-shot fast spin echo techniques (SSFSE). FSE uses a series of rapid 180-degree rephasing pulses, resulting in multiple echoes. A different phase encoding gradient is used for each echo, thereby reducing the time of scanning. The echo train length defines the number of rephasing pulses, that is, the higher the echo train, the shorter the imaging time, and the more heavily T2-weighted the image. A sample parameter for FSE MRCP consists of a long echo train (ie, 32), a long repetition time (3-5 respiratory cycles, 8000-10,000 msec), a time to echo (TE) greater than 250 msec, 3 excitations, thin collimation, and fat saturation.6 Total imaging time is approximately 4 to 6 minutes.6 In SSFSE, the entire raw data are acquired using a single excitation pulse. Roughly half of the raw data are required to
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W.E.A. Saad et al. consists of a very long echo train (ie, 128), an infinite time to resonance (TR), a TE greater than 800 msec (which suppresses signal from extraductal structures and eliminates the need for fat saturation), 1 excitation, and thin and thick collimation.6 Total imaging time for both single- and multisection imaging is approximately 30 seconds.6 Single thick section acquisition is performed in multiple coronal and coronal oblique planes around a chosen axis anterior to the porta hepatis. Each section is approximately 20 mm thick and several planes are used to acquire a volume of data from the entire biliary and pancreatic ducts. Multisection acquisition is performed in the straight coronal plane using 5-mm-thick sections and 100% overlap. Maximal intensity projections (MIP) are often performed to provide a 3D image of the biliary and pancreatic ducts, similar to a conventional cholangiogram. MIP gives an overview of the biliary and pancreatic ducts and presents images in a manner more familiar to clinicians. However, volume averaging reduces spatial resolution and MIP reconstructions consequently do not replace careful evaluation of source images. Magnetic resonance angiography. MRA is typically performed with gadolinium contrast agents, using a T1-
Figure 3 Hepatic artery thrombosis (HAT) with normal resistive indices. (A) Doppler ultrasound evaluation of the Intrahepatic artery with spectral wave form analysis in an adult right lobe living related liver transplant recipient. The spectral wave form evaluation shows an arterial resistive index (RI) of 0.61. (B) Digital subtraction angiogram of a phrenic artery (white arrows) of the same patient showing collateral branches (most lateral white arrow) entering at the dome of the liver to reconstitute the intrahepatic arterial branches of the right lobe graft (arrowheads), indicating complete hepatic artery thrombosis with collaterals and a false-negative Doppler ultrasound.
obtain a full image using half-Fourier transform techniques. A different phase encoding step is ascribed to each echo. SSFSE significantly reduces imaging time (one breath hold) due to the long echo train and improves the signal to noise ratio. However, the decrease in overall signal results in decreased spatial resolution. A sample parater for SSFSE MRCP
Figure 4 High arterial resistive index (RI). (A) Doppler ultrasound evaluation of the main hepatic artery (MHA) with spectral wave form analysis in an adult liver transplant recipient 1 day after transplantation. The MHA evaluation shows an arterial resistive index (RI) of 0.99 with diastolic flow reversal. (B) Similar Doppler evaluation as A on the same patient 48 hours later. The MHA evaluation demonstrates a normalized arterial resistive index (RI) of 0.81.
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Figure 5 Hepatic artery stenosis (HAS), CTA versus conventional angiography. (A) Contrast-enhanced CT axial image with a magnified inset of the celiac axis. The images show a hepatic artery stenosis at the anastomosis (arrowheads). Ao, aorta (abdominal); CAx, celiac axis (celiac trunk); SA, splenic artery; CHA, common hepatic artery (native/recipient artery); NHA, native proper hepatic artery; GHA, graft proper hepatic artery. (B) Advanced vessel analysis of the above contrast-enhanced CT including a traced maximum intensity projection (MIP) in the upper half of the image. The analysis demonstrates the significant anastomotic stenosis again (arrowheads) and estimates it to be a 61% crosssectional area reduction. (C) Digital subtraction angiogram of the transplant hepatic artery of the same patient at a right-anterior-oblique (RAO) projection showing the same significant anastomotic stenosis (arrows). (D) Inversed (light background, dark vessels) maximum intensity projection (MIP) the above contrast-enhanced CT at a slightly obliqued coronal projection to simulate the DSA image of C. Very similarly to the DSA, the anastomotic stenosis is again noted (arrows).
weighted 3D gradient echo sequence and breath holding. Precontrast images are obtained, followed by a postcontrast volume, typically whatever can be acquired in a 20- to 30second breath hold. If a 3D acquisition is used, the plane of imaging is most often coronal. If a 2D acquisition is used,
axial imaging is common with thicker slices. In general 3D imaging is used for hepatic arterial imaging, while portal venous MRA can be done with either 2D or 3D acquisition, given the larger size of the vessel and less need for very thin slices for resolution.7 Patients who are unable to sustain a
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Figure 6 Hepatic artery anastomotic pseudoaneurysm. (A) Doppler ultrasound evaluation of the porta hepatis demonstrating a 2.0 ⫻ 2.5-cm saccular lesion (between arrowhead and arrow) with multidirectional flow. The arrowhead points to the sac portion with blood flow (red) going toward the transducer while the arrow points to the sac portion with blood flow (blue) going away from the transducer. These findings are consistent with an extrahepatic pseudoaneurysm of the hepatic artery. (B) Transverse Doppler ultrasound evaluation of the porta hepatis demonstrating the same pseudoaneurysm as in A (hollow arrowhead). The solid arrowhead points to the source hepatic artery (common hepatic artery). The arrow points to the neck where turbulent flow is noted. (C) Contrast-enhanced CT axial image at the level of the celiac axis of the same patient as in A and B. The images show the large pseudoaneurysm in the vicinity of the hepatic artery anastomosis (arrowhead). The hollow arrow points to the recipient hepatic artery. The solid arrow points to the distal/graft hepatic artery. L, liver; S, stomach. (D) Sagittal reformat of the contrast-enhanced CT of C. The images show the large pseudoaneurysm in the vicinity of the hepatic artery anastomosis (hollow arrowhead). The solid arrowhead points to the proximal/recipient hepatic artery. L, liver; Ao, aorta (abdominal); CAx, celiac axis (celiac trunk); SMA, superior mesenteric artery.
20-second breath hold for an entire coronal or axial volume may have portal venous imaging performed in 2 overlapping sequential axial acquisitions. Typical coronal 3D volume parameters include a TR/TE of 4.6 to 5/1.8 to 2, a slice thickness of 3 to 3.5 mm, a slab thickness of 96 to 112 mm, 24 to 32 partitions, matrix size of 150 ⫻ 256 or 200 ⫻ 512, field of view of 35 to 40 cm, and acquisition time of 19 to 23 seconds.8 The usual dose of gadolinium is 30 mL delivered at 3 to 5 mL/sec using a timing bolus or detection of a certain degree of enhancement by the scanner using real-time bolus monitoring software.7,8 The injection is followed by a 10-mL saline flush. The arterial phase image is derived by viewing an MIP reformat. Additional detail for small vessels can be obtained by subtracting the unenhanced volume from the enhanced volume. Portal phase imaging is performed with similar parameters
with a 20-second interscan delay following the end of each preceding scan.8 MRA is less accurate than CTA for detecting hepatic artery thromboses and stenoses due to less technically adequate examinations due to patient motion or inability to sustain a long enough breath hold. In addition the spatial resolution of CT exceeds that of MR, despite the enhanced soft tissue contrast of MR. Kim and coworkers concluded that MR is sensitive (100%) but not specific (74%) with a positive predictive value of only 29% in the detection of significant hepatic artery stenosis (HAS).8 MR significantly overestimated the presence of stenosis, with only 3 of 19 patients called positive for a 50% or greater stenosis on MRI actually having stenosis as compared with angiography, and of 5 patient’s arteries said to be occluded by MRI 4 actually had a stenosis on conventional angiography and 1 had no significant stenosis.
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Figure 7 Intrahepatic arterial pseudoaneurysm. (A) Digital subtraction angiogram of the transplant hepatic artery demonstrating a small intrahepatic pseudoaneurysm (large single arrowhead). Adjacent to the pseudoaneurysm is a narrowing of the segment of the involved right intrahepatic artery branch (arrowheads). (B) Contrast-enhanced CT axial image at the level of the celiac axis of the same patient as A. The images show the small pseudoaneurysm (see C for magnified details). (C) Magnified CT image (right) of the boxed area in B with an adjacent labeled line drawing (left). The small pseudoaneurysm (arrowhead) was missed and was considered a continuum of a normal caliber intrahepatic arterial branch. In actuality, the involved intrahepatic arterial segment (between the arrows) is narrowed as it passes between the biliary stent (seen en face) and the small (7 mm) pseudoaneurysm (arrowheads). Ao, aorta (abdominal); CAx, celiac axis (celiac trunk); SpA, splenic artery; CHA, common hepatic artery (native/recipient artery); IVC, inferior vena cava.
Diagnostic Criteria for Vascular Complications Hepatic Artery Stenosis and Thrombosis On Doppler ultrasound the normal hepatic artery has a low resistance waveform with continuous diastolic flow and a resistive index (as defined by peak systolic velocity minus end diastolic velocity all divided by peak systolic velocity) of between
0.60 and 0.80. It normally has a brisk, fairly vertical upstroke as well (Fig. 1). Dodd and coworkers used the threshold of a resistive index less than 0.50 in any of the hepatic vessels to diagnose either hepatic artery thrombosis or stenosis with a sensitivity of 60% and a specificity of 77%9 (Fig. 2). When the acceleration time of greater than 0.08 second was used for diagnosis, this yielded a sensitivity/specificity of 53% and 86%, respectively.9 The reason abnormal intrahepatic arterial flow is detected in the
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Figure 8 Arterioportal fistula by Doppler ultrasound. (A) Doppler ultrasound evaluation of the left hepatic artery (LHA) of a transplant recipient with a right hepatic artery to portal vein fistula. The LHA is not involved and has a normal wave form with an arterial resistive index (RI) of 0.81. (B) Doppler ultrasound evaluation of the right hepatic artery (RHA) of the same transplant recipient. The RHA is involved and has a reduced arterial resistive index (RI) of 0.37. The high diastolic flow reflects the reduced peripheral arterial resistance as the arterioportal fistula shunts blood without resistance from the hepatic artery to the portal vein. (C) Doppler ultrasound evaluation of the right portal vein (RPV) of the same transplant recipient. The RPV branch that is involved exhibits aliasing and turbulence (mottled coloring involving the entire color spectrum) (arrowhead). The remainder of the RPV demonstrates normal directional flow (Red: arrows). (D) Doppler ultrasound evaluation with spectral wave form analysis right at the arterioportal fistula of the same transplant recipient. The spectral wave form analysis demonstrates significant flow through the fistula at approximately 150 cm per second.
presence of thrombosis is due to collateral formation, which may be fairly rapid9,10 (Fig. 3). Absent arterial flow in all arteries on a technically adequate Doppler imaging study is nearly always indicative of thrombosis; however, false positives may occur due to severe hepatic edema, systemic hypotension, or in a suboptimal ultrasound study due to patient size or edema.11 A loss of diastolic flow or diastolic flow reversal has been implicated by Nolton and Sproat12 and by Garcia-Criado and coworkers13 as a sign of impending thrombosis, especially if it occurs in the main hepatic artery. In our experience this finding may reverse over time, sometimes requiring as long as a week to correct (Fig. 4). In other patients it may actually precede arterial thrombosis, so patients with loss of diastolic flow on spectral Doppler examination require close follow-up. The most specific sign of hepatic arterial stenosis is a focal velocity elevation of greater than 2 mo/sec, which, if present, is predictive 96% of the
time.9 However, the most common site of stenosis is at the arterial anastomosis, which is often difficult to image at ultrasound, as it is frequently obscured by bowel. In fact, in 20 cases of stenosis reported by Dodd and coworkers, only 1 patient had a focal velocity elevation of greater than 2 mo/sec detected in the hepatic artery.9 Thus the velocity elevation criterion is less useful in a screening examination. On CT or MRI, hepatic artery thrombosis is defined as nonvisualization of the hepatic artery (main or a branch) on arterial phase imaging. If collaterals are present, small intrahepatic arteries may still be visualized.14 HAS is identified as focal narrowing of a vessel by more than 50% diameter reduction.15 Because the vessel pathways are often in and out of the plane of image acquisition, stenoses are often better displayed on postprocessed images using either MIP or multiplanar reformats15 (Fig. 5). Stenoses
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Figure 9 Arterioportal fistula (APF) by contrast-enhanced CT. Contrast-enhanced CT axial image at the level of the upper abdomen of the same liver transplant recipient as Figure 8 with a right hepatic lobe APF. The images show an early and more avid enhancing right portal venous radical (solid arrowhead). This enhances more than the remainder of the portal vein (hollow arrowhead). In addition the hepatic segment (arrows) fed by the involved portal vein enhances ahead of the remainder of the hepatic parenchyma (see Figures 6 and 7, Chapter IV).
199 tend to be overestimated by CT as compared with conventional angiography.16 CTA has been calculated to overestimate HAS by approximately 13%.16 CTA has a sensitivity, specificity, and accuracy for detecting extrahepatic HAS of 88 to 100%, 89%, and 95%, respectively.16-18 The sensitivity of CTA in detecting extrahepatic HAS drops from 88 to 100% down to 83% for intrahepatic HAS.16 The positive and negative predictive values for CTA in this setting are 92% and 100%, respectively.18 The advantage of CTA over Doppler ultrasound is its 24-hour availability and that CTA is not operator dependent. However, CTA can be nondiagnostic in a minority of cases (4%), ranging from 0 to 9% of cases due to poor injection/scanning timing.15-18 In addition, the intravenous contrast load may not be tolerable for liver transplant recipients with hepatorenal syndrome (renal insufficiency). MRA is similarly suboptimal in patients with impaired renal function due to the risk of gadolinium-induced nephrogenic systemic fibrosis. This combined with a higher rate of suboptimal exams due to patient motion and inadequate breath holding make MR a less desirable imaging choice than US or CT.
Hepatic Artery Pseudoaneurysms Hepatic artery pseudoaneurysms occur most frequently at the anastomosis, and thus may be difficult to detect with US.13 Because pseudoaneurysms are extrahepatic they are often hidden behind bowel gas. In addition, sonographers may not visualize the entire extrahepatic main hepatic artery
Figure 10 Complete portal vein thrombosis (PVT). (A) Doppler ultrasound evaluation of a transplant recipient with complete thrombosis of the portal vein (P). The portal vein has no flow on color Doppler; however, the adjacent hepatic artery is visualized. This is consistent with portal vein thrombosis or very slow flow in the portal vein. (B) Power Doppler ultrasound evaluation of the same transplant recipient with complete thrombosis of the portal vein (P). The portal vein still does not light up on power Doppler; however, the surrounding arterial supply is visualized by color Doppler. This is consistent with portal vein thrombosis or very slow flow in the portal vein. (C) Contrast-enhanced CT of the same patient. The axial image is at the level of the celiac axis. The images show no enhancement of the portal vein (arrows). Around the thrombosed portal vein (P) is a slight rim of enhancement. The hepatic arteries enhance (arrowheads).
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Figure 11 Partial portal vein thrombosis (PVT). (A) Gray scale ultrasound evaluation of a transplant recipient with a shallow heterogeneous echogenic mass (arrowhead) along the wall of the main portal vein. This is consistent with chronic partial thrombosis of the portal vein (P). (B) Color Doppler ultrasound evaluation of a transplant recipient with the same thrombus (arrowhead) along the wall of the main portal vein. This is consistent with partial thrombosis of the portal vein. (C) Unenhanced CT axial image at the level of the upper abdomen of the same liver transplant recipient as in Figure 10A and B. The portal vein visualized is intrahepatic and not extrahepatic, however. The images demonstrate a high density portal vein thrombus (arrows).
and may overlook small pseudoaneurysms particularly if the hepatic artery is tortuous. A pseudoaneurysm is identified on US as a cystic structure in communication with the hepatic artery with a disorganized “to and fro” color and spectral Doppler pattern as the arterial blood flows into and out of the pseudoaneurysm (Fig. 6A, B). In a prospective study comparing US to CTA, US detected 13% of aneurysms while CTA detected 78%. CT or MRI performed in the arterial phase show a brightly enhancing round mass adjacent to a hepatic artery, enhancing with the same intensity as the adjacent arterial blood (Fig. 6C, D). One reason for false a false-negative CTA examination is very small pseudoaneurysm, particularly if it compresses an adjacent artery and narrows it to the extent that the radiologist would see the small pseudoaneurysm as a continuum of a normal caliber artery (Fig. 7), that is, missing both abnormalities, the outpouching, and adjacent luminal narrowing.
Hepatic Artery to Portal Vein Fistula This may occur as a complication of a pseudoaneurysm11 or as a result of liver biopsy.14,19,20 Biopsy-induced shunts occur in as many as 50% of patients if scanned at 1 week post biopsy, but drop to 10% thereafter as most close spontaneously.21,22 On US the inflowing hepatic arterial resistive index
will be lower than the contralateral normal vessel on the opposite side. In addition, reversed flow in particular portal vein radicals (considered a rare finding), arterialized portal vein waveform as well as a focus of turbidity with aliasing at the site of the arterioportal fistula can also be seen20,23-25 (Fig. 8). On CT the portal vein may show early enhancement in the arterial phase of injection before the enhancement of the main portal vein, or enhancement of the portal vein before enhancement of the mesenteric and splenic veins14,20 (Fig. 9; also see Figures 6 and 7 in this issue, pages 196-199. A less common sign includes transient wedge-shaped parenchymal enhancement during the hepatic arterial phase of injection20 (Fig. 9; also see Figures 6 and 7 in this issue, pages 196-199.
Portal Vein Thrombosis This is a relatively rare complication, occurring in 1 to 3% of patients,14,26 but seen more commonly with redundant vessels or trauma to the vessel at surgery.11 On US there is either total absence of flow in the portal vein on color Doppler (Fig. 10), or a mass filling in a portion of the portal vein and partially occluding it (Fig. 11). The CT or MR appearance is similar when contrast is used. The vessel is either absent or there is a nonenhancing mass occupying a portion of the vein (Fig. 10). On noncontrast CT the portal vein thrombus can
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Figure 12 Portal vein stenosis. (A) Gray scale ultrasound evaluation of the main portal vein at the anastomosis demonstrating a significant stenosis at the anastomosis (arrows). A part of this apparent narrowing is possibly a diameter mismatch between the recipient and graft portal veins; however, the dynamic findings of B-D indicate a hemodynamically significant portal vein stenosis. (B) Doppler ultrasound evaluation of the main portal vein at the anastomosis demonstrating a significant stenosis at the anastomosis (arrows). There is turbulent high velocity flow with aliasing at and distal to the anastomotic portal vein stenosis. (C) Doppler ultrasound evaluation of the portal vein of the same transplant recipient proximal to the anastomotic stenosis. The spectral wave form analysis shows a velocity of approximately 40 cm per second (41 cm/sec) proximal to the anastomosis. (D) Doppler ultrasound evaluation of the portal vein of the same transplant recipient distal to the anastomotic stenosis. The spectral wave form analysis shows a velocity of approximately 186 cm per second (185 cm/sec) distal to the anastomosis. This computes to a 4.5-fold increase in velocity from 40 cm/sec to 185 cm/sec. The threshold for calling a significant stenosis is a velocity greater than 125 cm/sec and a velocity increase of more than 3-fold.
have increased attenuation relative to the surrounding liver (Fig. 11C). However, with contrast enhancement, the portal vein thrombus becomes relatively less dense (Fig. 10C). Acutely the vessel is distended. As the thrombus becomes more chronic the vessel narrows and scars and the thrombus becomes more echogenic on US. Acute portal vein compression due to hematoma or biloma may produce symptoms similar to thrombosis, and cause nonvisualization of the main portal vein on US.
uation of the portal vein (Fig. 12). On US the predictive features include a focal velocity greater than 125 cm/sec or a 3-fold increase in velocity with a sensitivity of 73% and a specificity of 95 to 100%, respectively27 (Fig. 12C, D). Portal venography with pressure measurements remains the most reliable examination (gold standard). When a clinically significant stenosis is present, there is a greater than 5-mm gradient measured across the lesion on direct arterial portography.14
Portal Vein Stenosis
Hepatic Vein Thrombosis or Stenosis
Focal narrowing of the portal vein on US, CT, or MRI may represent discrepancy between donor and recipient portal vein size, or may indicate a true stenosis.14 Diameter discrepancy by CT or MRI may be overcalled as portal vein stenoses. Ultrasound may provide the most dynamic noninvasive eval-
Doppler examinations in a patient with hepatic vein stenosis will show decreased mean velocities in both the hepatic veins and portal vein. The hepatic vein wave form will be significantly dampened when there is an outflow obstruction.28 Typically the Doppler waveform in a nor-
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Figure 13 Hepatic vein stenosis. (A) Doppler ultrasound evaluation of the middle hepatic vein demonstrates a normal posttransplant biphasic spectral wave form with a mean velocity of 25 to 30 cm per second. (B) Doppler ultrasound evaluation of the right hepatic vein at the stenosis demonstrates aliasing. The spectral wave form shows a mean velocity of 100 cm per second. (C) Doppler ultrasound evaluation of the right hepatic vein proximal to the stenosis demonstrates a monophasic (flattened) spectral wave form with a mean velocity of 10 cm per second.
mal hepatic vein is triphasic, but after transplantation the waveform is often biphasic even without any other signs or symptoms of flow obstruction29 (Fig. 13A). However, when significant stenosis develops the waveform usually degrades to a monophasic pattern (Fig. 13C). Other findings may include reversal of hepatic vein flow, accelerated flow with aliasing just beyond the stenosis (Fig. 13B), and visualization of the stenosis on gray scale imaging. By CT, direct visualization of the stenosis can be seen (Fig. 14). In addition, perfusion abnormalities can also be noted, although they are nonspecific.
Inferior Vena Cava Thrombosis or Stenosis This is also a rare complication occurring in less than 1% of cases.11 The appearance of thrombosis is similar to that in the portal vein, with a space-occupying mass obliterating (in the case of complete thrombosis) or narrowing (in partial thrombosis) either the colorized portion of the vessel on color Doppler, or the contrasted lumen on CT or MR (Fig. 15). Stenosis most frequently occurs at the anastomosis. Ultrasound will show a focal narrowing with a 3- to 4-fold increase in velocity as compared with the prestenotic segment. If the stenosis is in the suprahepatic por-
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203 diagnosed by cholangiography; however, they can be identified on US, CT, or MRI as focal biliary duct dilation proximal to the area of stricture. Anastomotic strictures occur from post surgical scarring, whereas nonanastomotic strictures occur more proximally in the liver due to ischemia as a consequence of hepatic artery stenosis or thrombosis. These strictures often start at the hilum and progress to the intrahepatic bile ducts.14 With severe injury, the epithelium sloughs due to biliary necrosis. By US the biliary tree is markedly dilated and the lumen filled with debris (Fig. 18). The lumen itself may not be visible, only the periportal increased echogenicity, which may or may not conform to the normal biliary branching pattern (Fig. 19). On CT the biliary tree is dilated and irregular and of decreased attenuation as compared with the enhancing hepatic parenchyma (Fig. 18).
Summary
Figure 14 Hepatic vein stenosis. Contrast-enhanced CT axial image at the level of the upper abdomen in a liver transplant recipient with a “piggyback” caval anastomosis. The donor/graft inferior vena cava (IVC) is indicated by the hollow arrowhead. The native/recipient IVC is indicated by the solid arrowhead. The images show a right hepatic vein stenosis as it enters the IVC (between arrows).
tion of the vessel, there may be reversed flow or dampened waveforms with absent phasicity in the hepatic veins11 (Fig. 16). Chong and coworkers used the venous pulsatility index, defined as the peak venous velocity minus the minimum venous velocity all divided by the peak velocity.27 Normal vessels had an index of 0.75, while stenoses were associated with a low index, with a mean value of 0.39.27 Delayed stenoses may occur secondary to fibrosis. CT or MRI will show severe narrowing of the IVC at the point of stenosis, with only a minimal residual lumen (Figs. 16B and 17).
Noninvasive imaging of hepatic transplant complications is performed by all 3 major cross-sectional imaging modalities, US, CT, and MRI. Ultrasound is often used to screen for vascular abnormalities, including hepatic arterial stenosis and thrombosis, and the less common thromboses or stenoses of the portal vein, hepatic veins, and inferior vena cava. Precise anatomy of the vascular abnormalities is often better determined on CT or MR, especially when a focal stenosis occurs in the distal IVC, or in the hepatic artery proximal to the porta hepatis where it is difficult to image directly by US. CTA and MRA give detailed imaging of the small hepatic arteries, while US tends to give more physiologic data. All 3 modalites require angiographic correlation with pressure gradients across a stenosis to determine its physiologic significance. MRCP can be valuable to detect focal biliary abnormalities; however, direct cholangiography remains the gold standard for biliary complications.
Diagnostic Criteria for Biliary Complications Biliary complications are the most common transplant sequelae, occurring in up to 25% of allografts.11 Complications include leaks, strictures, biliary necrosis, and abscess formation. Leaks are most commonly confirmed with cholangiography. When imaged by US, CT, or MRI they are cystic fluid collections that lack enhancement on CT or MR, often located in the porta hepatic or adjacent to the liver, often at the T-tube site. Strictures are also most often
Figure 15 Partial inferior vena cava (IVC) thrombosis. Doppler ultrasound evaluation of an adult transplant recipient. This is transverse to the inferior vena cava. The IVC is mostly thrombosed (arrow). The residual patent lumen (blue, arrowhead) is seen.
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Figure 16 Inferior vena cava (IVC) stenosis. (A) Color Doppler ultrasound evaluation of the inferior vena cava (IVC). The transducer is along the longitudinal axis of the IVC. There is progressive narrowing of the IVC with a significant stenosis at the level of the arrowheads. (B) Axial MR image at the level of the upper abdomen shows a pinhole residual lumen (arrowhead) due to the significant stenosis seen in the Doppler examination of A. (C) Digital subtraction inferior vena-cavogram demonstrates the significant suprahepatic IVC stenosis (arrows) close to the IVC-right atrial (RA) junction. IVC, inferior vena cava; RRV, right renal vein; LRV, left renal vein.
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Figure 17 Inferior vena cava (IVC) stenosis. Contrast-enhanced CT axial image at the level of the upper abdomen in a liver transplant recipient. There is a significant IVC stenosis (arrow). Notice the ascites indicating graft dysfunction that may be due to graft outflow vein obstruction (the IVC stenosis).
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Figure 19 Biliary necrosis. Gray scale ultrasound image of an adult transplant recipient with hepatic artery thrombosis (HAT). The image demonstrates dilated bile ducts with nodular echogenic debris (arrows).
Figure 18 Central biliary necrosis. (A) Percutaneous transhepatic cholangiogram (PTC) showing disproportionate central biliary dilation (arrowheads) with irregular shaggy borders consistent with biliary necrosis (N) due to graft ischemia (dearterialization). The peripheral ducts (arrows) are spared at this moment in time. (B) Axial CT image at the level of the celiac axis of the same patient as in A showing dilated central bile ducts (arrowhead) with air within the central necrotic (N) ducts (arrow). (C) Gray scale ultrasound image depicting the same findings as in A and B on the same transplant recipient. There are irregular central necrotic (N) areas. The arrows point to dilated ducts (arrows).
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References 1. Kruskal JB, Newman PA, Sammons LG, et al: Optimizing Doppler and color flow US: application to hepatic sonography. Radiographics 24: 657-675, 2004 2. Merkle EM, Boll DT, Brambs HJ: Liver: normal anatomy, imaging techniques, and diffuse diseases, in Haaga LC Jr, Gilkeson RC (eds): Computed Tomography and Magnetic Resonance Imaging of the whole body. St. Louis, MO, Mosby, 2003, pp 1318-1339 3. Fishman EK: CT angiography: clinical applications in the abdomen. Radiographics 21:S3-S16, 2001 (RSNA Refresher course) 4. Nakanishi T: Evaluation of coronary artery stenoses using electronbeam CT and multiplanar reformation. J Comput Assist Tomogr 21: 121-127, 1997 5. Napel S, Rubin GD, Jeffrey RB Jr: STS-MIP: a new reconstruction technique for CT of the chest. J Comput Assist Tomogr 17:832-838, 1993 6. Vitellas KM, Keogan MT, Spritzer CE, et al: MR cholangiopancreatography of bile and pancreatic duct abnormalities with emphasis on the single-shot fast spin-echo technique. Radiographics 20:939-957; quiz 1107-1108, 2000 7. Leiner T: Magnetic resonance angiography of abdominal and lower extremity vasculature. Top Magn Reson Imaging 16:21-66, 2005 8. Kim BS, Kim TK, Jung DJ, et al: Vascular complications after living related liver transplantation: evaluation with gadolinium-enhanced three-dimensional MR angiography. AJR Am J Roentgenol 181:467474, 2003 9. Dodd GD 3rd, Memel DS, Zajko AB, et al: Hepatic artery stenosis and thrombosis in transplant recipients: Doppler diagnosis with resistive index and systolic acceleration time. Radiology 192:657-661, 1994 10. Rollins NK, Timmons C, Superina RA, et al: Hepatic artery thrombosis in children with liver transplants: false-positive findings at Doppler sonography and arteriography in four patients. AJR Am J Roentgenol 160:291-294, 1993 11. Crossin JD, Muradali D, Wilson SR: US of liver transplants: normal and abnormal. Radiographics 23:1093-1114, 2003 12. Nolten A, Sproat IA: Hepatic artery thrombosis after liver transplantation: Temporal accuracy of diagnosis with duplex US and the syndrome of impending thrombosis. Radiology 198:553-559, 1996 13. Garcia-Criado A, Gilabert R, Salmeron JM, et al: Significance of and contributing factors for a high resistive index on Doppler sonography of the hepatic artery immediately after surgery: prognostic implications for liver transplant recipients. AJR Am J Roentgenol 181:831-838, 2003 14. Quiroga S, Sebastia MC, Margarit C, et al: Complications of orthotopic liver transplantation: spectrum of findings with helical CT. Radiographics 21:1085-1102, 2001 15. Boraschi P, Donati F, Cossu MC, et al: Multi-detector computed tomog-
16.
17.
18.
19.
20.
21. 22.
23.
24.
25.
26.
27.
28.
29.
raphy angiography of the hepatic artery in liver transplant recipient. Acta Radiol 46:455-461, 2005 Vignali C, Bargellini R, Cioni P, et al: Diagnosis and treatment of hepatic artery stenosis after orthotopic liver transplantation. Transpl Proc 36: 2771-2773, 2004 Piolanti M, Fabbro E, Pascali E, et al: CT angiography for the evaluation of adult orthotopic liver transplantation arterial complications. Radiol Med (Torino) 102:348-356, 2001 Brancatelli G, Katyal S, Federle MP, et al: Three-dimensional multi-slice helical computed tomography with volume rendering technique in the detection of vascular complications after liver transplantation. Transplantation 73:237-242, 2002 Saad WEA, Davies MG, Ryan CK, et al: Incidence of arterial injuries detected by angiography following percutaneous right-lobe ultrasound-guided core liver biopsies in human subjects. Am J Gastroenterol 101:2641-2645, 2006 Saad WEA, Davies MG, Rubens DJ, et al: Endoluminal management of arterio-portal fistulae in liver transplant recipients: a single center experience. Vasc Endovasc Surg 40:451-459, 2006 Hellekant C: Vascular complications following needle puncture of the liver. Acta Radiol Diagn 17:209-222, 1976 Hellekant C, Olint T: Vascular complications following needle puncture of the liver. An angiographic investigation in the rabbit. Acta Radiol Diagn 14:577-582, 1973 Chavan A, Harms J, Picjlmayr R, Galanski M: Transcatheter coil occlusion of an intrahepatic arterioportal fistula in a transplanted liver. Bildgebung 60:215-218, 1993 Strodel E, Eckhauser FE, Lemmer JH, Whitehouse M Jr, Williams DM: Presentation and perioperative management of arterioportal fistulas. Arch Surg 122:563-571, 1987 Glockner JF, Forauer AR: Vascular or ischemic complications after liver transplantation: pictorial essay. AJR Am J Roentgenol 173:1055-1059, 1999 Uzochukwu LN, Bluth EI, Smetherman DH, et al: Early postoperative hepatic sonography as a predictor of vascular and biliary complications in adult orthotopic liver transplant patients. AJR Am J Roentgenol 185: 1558-1570, 2005 Chong WK, Beland JC, Weeks SM: Sonographic evaluation of venous obstruction in liver transplants. AJR Am J Roentgenol 188:515-521, 2007 Egawa H, Tanaka K, Uemoto S, et al: Relief of hepatic vein stenosis by balloon angioplasty after living-related donor liver transplantation. Clin Transpl 7(4):306-311, 1993 Fujimoto M, Moriyasu F, Someda H, et al: Recovery of graft circulation following percutaneous transluminal angioplasty for stenotic venous complications in pediatric liver transplantation: assessment with Doppler ultrasound. Transpl Int 8(2):119-125, 1995