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AJR 2000; 175:1735-1739
© American Roentgen Ray Society


Original Report

Detection of Vascular Complications After Liver Transplantation

Early Experience in Multislice CT Angiography with Volume Rendering

Sanjeev Katyal1, James H. Oliver, III, David G. Buck and Michael P. Federle

1 All authors: Department of Radiology, University of Pittsburgh Medical Center, 200 Lothrop St., Pittsburgh, PA 15213.

Received February 14, 2000; accepted after revision April 17, 2000.

 
Address correspondence to S. Katyal.


Abstract
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
OBJECTIVE. Our objective was to investigate the usefulness of three-dimensional multislice CT angiography for the evaluation of liver transplant recipients presenting with clinical or sonographic findings suggestive of hepatic vascular complications.

CONCLUSION. Our early results indicate that three-dimensional multislice CT angiography with volume rendering can reveal common and potentially lethal vascular complications in patients who have undergone liver transplantation.


Introduction
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
Liver transplantation is an increasingly common curative therapeutic solution for patients with both acute and end-stage liver disease. Graft ischemia after liver transplantation is associated with a high incidence of morbidity and mortality. The most common vascular complication after liver transplantation is hepatic artery thrombosis, occurring in 2-12% of transplants [1]. Hepatic artery stenosis is the second most common vascular complication after liver transplantation, occurring in 5% or less of transplants [2]. If diagnosed early in the postoperative period, surgical repair has good reported success rates [3].

The clinical presentation of hepatic arterial vascular complications is variable, ranging from mild elevation in liver enzymes to fulminant hepatic failure (hepatic artery thrombosis). Because of this variability in clinical presentation, imaging studies are critical for early diagnosis or to eliminate these potentially lethal vascular complications from diagnostic consideration. Angiography remains the gold standard for diagnosing hepatic arterial complications. It is not, however, practical to perform as a screening test in all patients because it is both invasive and expensive, with patients requiring close monitoring after the procedure [4]. Sonography is commonly used as a non-invasive screening technique in patients after liver transplantation but carries a significant incidence of false-negative results. The reported sensitivities of duplex sonography for the detection of hepatic artery stenosis range from 80-85% to 60-80% for the detection of hepatic artery thrombosis [3, 5, 6].

Helical CT angiography with three-dimensional (3D) arterial reconstructions has been shown to accurately depict hepatic arterial anatomy and anatomic variations when compared with conventional catheter angiography [7]. Helical CT angiography has also been shown to have a significant impact on surgical planning for liver transplantation [8]. Traditional helical single-slice CT scanners are still limited in their ability to image large volumes during a single breath-hold and to provide adequate spatial resolution crucial for CT angiography. This limitation prompted the development of faster multislice helical CT scanners that can cover extensive volumes quickly with excellent spatial resolution. With the enhanced spatial resolution provided by the multislice scanner, CT angiography of smaller vessels is now possible, not only for gross anatomic depiction but also for the detection of stenoses. The purpose of this study, therefore, was to investigate the preliminary use of multislice CT angiography with 3D volume-rendering techniques for the evaluation of vascular complications, particularly hepatic artery stenosis and thrombosis, after liver transplantation.


Subjects and Methods
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
Patients
Between July 1999 and January 2000, 18 patients (16 men and 2 women; age range, 35-73 years; mean age, 61 years) who underwent liver transplantation were prospectively examined with multislice contrast-enhanced CT. The mean time interval since liver transplantation was 36 months (range, 4-168 months). The indication for CT was clinical suspicion of hepatic artery stenosis in 12 patients, allograft evaluation in two patients, sonographic evidence of portal vein stenosis in one patient, routine incidental CT findings suggestive of a splenic artery aneurysm in one patient, a hepatic artery pseudoaneurysm in another patient, and follow-up CT for hepatocellular carcinoma in one patient.

Multislice Helical CT
All CT was performed on a LightSpeed QX/I scanner (General Electric Medical Systems, Milwaukee, WI). The LightSpeed multislice CT scanner uses 16 detector cells in the Z direction (direction of patient movement through the gantry). Each of the detector cells is 1.25-mm thick in the Z direction. Four signals are collected per gantry rotation. Each signal can be collected from either an individual detector row or a combination of two, three, or four detector rows.

We performed unenhanced axial CT of the liver using 7-mm thick sections and a 0-mm interscan gap. The proximal descending aorta just above the level of the celiac axis was identified for the test bolus to determine the optimal time of contrast enhancement. Twenty milliliters of ioversol (Optiray 320; Mallinkrodt Medical, St. Louis, MO) was injected via an 18- to 20-gauge IV angiocatheter at 4 mL/sec. After a 10-sec delay, 15 1-sec axial scans, at the chosen level, were obtained with 1-sec interscan delay. The time for peak aortic enhancement was then determined. All patients received 150 mL of Optiray 320 at 4 mL/sec, with a scan delay of time-to-peak aortic enhancement as determined from the test bolus. The scan delays ranged from 16 to 25 sec for the arterial phase data set.

Our prospective scanning parameters for the first scan (arterial phase) acquisition were highspeed mode (pitch of 6:1), table speed of 7.5 mm, and slice thickness of 2.5 mm with 2.5-mm interval. The first scan set was obtained in the caudocranial direction from below the superior mesenteric artery origin to the diaphragm. We reconstructed the 2.5 x 2.5 mm data set to 1.25 x 1.25 mm for 3D reconstructions performed using a freestanding Advantage Windows workstation (General Electric Medical Systems).

The second helical acquisition started approximately 60 sec after beginning the contrast injection. During the second (portal venous) phase, images were obtained in a cranial—caudal direction from the top of the liver to the iliac crest. We used high-speed mode (pitch of 6:1), table speed 15 mm per rotation, and 4 x 2.5 mm detector configuration (minimum slice thickness); 5 x 5 mm slice thickness by interval was used prospectively. In the patient with possible portal vein stenosis, the images were reconstructed to 2.5 x 2.5 mm for the volume-rendered 3D CT angiogram.

Three-Dimensional Reconstructions
All reconstructions were performed by a radiologist experienced in 3D postprocessing techniques, and each procedure required approximately 15 min. Volume rendering was performed in all patients. Volumes of interest were selected manually from the axial source images to include only the aorta; celiac axis; hepatic artery; left gastric, splenic, and superior mesenteric arteries; and the liver. CT angiograms were then reconstructed with the volume-rendering algorithm with lower thresholds of 70-115 H. Display parameters including width, level, opacity, and brightness were chosen subjectively by the individual radiologist performing the volume rendering. The volume-rendered images were obtained in projections selected to best depict the course of the hepatic vasculature. Standard projections performed in all patients included right anterior oblique, inferior, posterior, and lateral projections.

Image Evaluation
The reconstructed axial images along with the 3D volume-rendered reconstructions were prospectively reviewed by two radiologists, and the arterial supply to the liver along with any vascular complications (stenosis, thrombosis, pseudoaneurysm, or aneurysm) was recorded as part of the official CT report. The hepatic arterial anatomy was classified according to the type of hepatic arterial anastomosis present.


Results
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
Eighteen liver transplantation patients underwent multislice helical CT angiography of the transplanted hepatic vasculature because of suspected vascular and biliary complications or for tumor follow-up. Twelve of these patients (67%) had correlative catheter angiography, and the remaining six patients (33%) had clinical follow-up.

Hepatic Artery Stenosis
Two patients had evidence of severe hepatic artery stenosis, and two patients had mild-to-moderate hepatic artery stenosis after liver transplantation on the 3D CT angiograms. One of these patients had a stenosis of a supraceliac aortic graft at the anastomosis of the graft with the donor hepatic artery (Fig. 1A,1B). The remaining three patients had stenoses at the anastomosis between the donor and recipient hepatic artery. After prospective CT interpretations of significant stenoses in these patients, catheter angiography was performed in all patients and confirmed the 3D CT angiographic findings.



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Fig. 1A. 46-year-old man with highgrade hepatic artery stenosis after liver transplantation. Right posterior oblique volume-rendered three-dimensional multislice CT angiogram shows severe stenosis (arrow) of graft at anastomosis of graft with donor hepatic artery.

 


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Fig. 1B. 46-year-old man with highgrade hepatic artery stenosis after liver transplantation. Catheter angiogram of supraceliac aortic graft reveals high-grade stenosis at anastomosis (arrow).

 

Another three patients had redundant donor hepatic arteries after liver transplantation. These arteries were difficult to follow along their entire course on the basis of the axial images alone but were clearly determined to be patent without stenosis on the volume-rendered 3D images. One of these patients had catheter angiography that confirmed both redundancy and no stenosis of the donor hepatic artery (Fig. 2A,2B). A second patient had Doppler sonography performed the same day as CT angiography. The third patient did not have any additional imaging studies.



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Fig. 2A. 50-year-old man with increasing levels of liver enzymes suggestive of possible hepatic artery stenosis after liver transplantation. Selective catheter angiogram of recipient hepatic artery shows redundant hepatic artery. Redundancy at anastomosis (arrow) limits evaluation for possible stenosis.

 


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Fig. 2B. 50-year-old man with increasing levels of liver enzymes suggestive of possible hepatic artery stenosis after liver transplantation. Inferior oblique volume-rendered three-dimensional multislice CT angiogram shows tortuous donor hepatic artery-to-recipient hepatic artery anastomosis (arrow) with no evidence of stenosis.

 

Hepatic Artery Thrombosis
Two patients had complete thrombosis of the hepatic artery after liver transplantation. Both patients had occlusion at the origin of the donor hepatic artery. One patient had collateral arterial circulation to the liver via the left gastric artery shown on 3D CT angiograms (Fig. 3A,3B). Doppler sonography in this patient performed 3 days before CT angiography showed low resistive indexes (0.39-0.47) in the right and left hepatic artery, respectively. Both patients underwent catheter angiography confirming hepatic artery thrombosis.



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Fig. 3A. 55-year-old man with clinical evidence of decreased hepatic arterial flow and normal findings on Doppler sonography after liver transplantation. Inferior oblique volume-rendered three-dimensional multislice CT angiogram shows occluded hepatic arterial (HA) stump (arrow) with intrahepatic collateral (collater) vessels from left gastric artery.

 


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Fig. 3B. 55-year-old man with clinical evidence of decreased hepatic arterial flow and normal findings on Doppler sonography after liver transplantation. Catheter angiogram of recipient celiac axis confirms occluded hepatic arterial stump (arrow) with filling of proximal left gastric (arrowheads) and splenic arteries. Intrahepatic collateral vessels from left gastric artery are not visualized on celiac injection.

 

Arterial Aneurysm and Pseudoaneurysm
One patient had a pseudoaneurysm of the intrahepatic right hepatic artery after liver transplantation. The pseudoaneurysm was visualized on axial CT, but the volume-rendered 3D images clearly showed the right hepatic artery supplying the pseudoaneurysm. Follow-up catheter angiography confirmed the 3D CT angiographic findings (Fig. 4A,4B). Of note, hepatic sonography performed 6 days before CT angiography did not reveal the hepatic artery pseudoaneurysm, showing normal hepatic vessels with no evidence of vascular abnormalities.



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Fig. 4A. 46-year-old man with incidental hepatic artery pseudoaneurysm reported on routine helical CT performed for possible abscess after liver transplantation. Inferior oblique volume-rendered three-dimensional multislice CT angiogram shows right hepatic artery pseudoaneurysm (arrow).

 


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Fig. 4B. 46-year-old man with incidental hepatic artery pseudoaneurysm reported on routine helical CT performed for possible abscess after liver transplantation. Selective catheter angiogram of recipient main hepatic artery confirms pseudoaneurysm of right hepatic artery (arrow).

 

A second patient was found to have a splenic artery aneurysm after liver transplantation. The aneurysm was well depicted on axial and 3D CT angiography and confirmed by catheter angiography.

Portal Vein Stenosis
One patient had suspected portal vein stenosis on sonography with a threefold increase in velocity at the portal vein anastomosis. CT angiography revealed the position and degree of stenosis of the extrahepatic portal vein approximately 2 cm from the superior mesenteric vein and splenic vein confluence. Transhepatic portal venography confirmed a moderate anastomotic stenosis, and balloon angioplasty was performed (Fig. 5A,5B).



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Fig. 5A. 50-year-old man who presented with sonographic evidence of portal venous stenosis after liver transplantation. Left posterior oblique volume-rendered three-dimensional multislice CT angiogram of portal vein shows moderate stenosis of lower anastomosis of iliac vein graft (arrow).

 


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Fig. 5B. 50-year-old man who presented with sonographic evidence of portal venous stenosis after liver transplantation. Transhepatic portal venogram confirms moderate stenosis (arrow) of lower anastomosis and widely patent upper portal anastomosis at liver hilum.

 

Normal Hepatic Artery
Six patients had no evidence of vascular complications on 3D CT angiography after liver transplantation. The indications for CT were clinical suspicion of hepatic artery stenosis in three patients (50%), allograft dysfunction in two patients (33%), and follow-up for hepatocellular carcinoma in one patient (17%). Two patients had catheter angiography confirming widely patent hepatic arteries. The remaining four patients had clinical follow-up of 2-5 months with no clinical evidence of hepatic artery stenosis (normal liver enzymes).

Evaluation of Vascular Anatomy
The hepatic arterial anatomy was prospectively reported in the official CT report. We retrospectively correlated our CT angiographic findings with the original surgical transplantation report. In the two patients with hepatic artery stenosis, the distal hepatic artery anastomosis was not visualized because of complete occlusion of the hepatic artery. In the remaining 16 patients, the prospectively reported arterial anatomy completely correlated with the operative transplantation report.


Discussion
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
With the development of multislice CT, we believe that CT angiography of the liver is now a practical noninvasive method of detecting hepatic arterial complications after liver transplantation. The excellent spatial resolution and fast scan times afforded with the multislice scanner allow CT angiography to depict smaller vessels, not only for gross patency but also for stenoses. CT angiography has several advantages over other imaging modalities. Compared with catheter angiography, CT angiography is noninvasive and is less than one-third the cost of conventional angiography. Unlike sonography, CT angiography is not as dependent on the technologist performing the study or on the patient's body habitus. Additionally, CT is more useful in detecting other posttransplantation complications including bile leaks, bile duct necrosis, hematomas, and abscesses. In fact, CT is commonly used in the postoperative period, in addition to routine Doppler sonography, to detect these nonvascular complications.

In this initial prospective study, CT angiography had substantial impact on the postoperative care of several patients. Nine of the 18 patients after liver transplantation had vascular complications diagnosed on CT angiography. All nine of these patients had catheter angiography confirming CT angiographic findings. Doppler sonography misdiagnosed five of the nine patients with vascular complications. Specifically, sonography failed to reveal the three patients with hepatic artery stenosis, one patient with hepatic artery thrombosis (left gastric intrahepatic collaterals), and the patient with the right hepatic artery pseudoaneurysm. Without CT angiography in the patients with hepatic artery stenosis, the diagnosis of hepatic artery stenosis would certainly have been delayed and possibly not made until these stenoses progressed to hepatic artery thrombosis, in light of the sonographic findings. Although sonography is commonly used as a screening modality in patients after liver transplantation, our preliminary study suggests that multislice CT angiography is more accurate than Doppler sonography in the detection of vascular complications.

Our study had several limitations. First, our sample size was small and not all patients in our study population had correlative catheter angiography. Two thirds of our patients did, however, have catheter angiography, and the six patients with no angiographic correlation had normal hepatic arteries on CT angiography and no clinical evidence of decreased hepatic arterial flow (normal liver function tests, no biliary dilatation or bile duct necrosis) 2-5 months after CT. Our study was an initial prospective study intended to identify a possible role of CT angiography in the evaluation of posttransplantation hepatic arterial complications. A prospective study in a large population of liver transplant recipients with correlation to sonography and conventional catheter angiography would be useful in determining the true accuracy of CT angiography. Our preliminary results indicate that multislice CT angiography with 3D volume rendering has the ability to accurately show a variety of common and potentially lethal vascular complications after liver transplantation. Combined with the current role of CT for the detection of nonvascular transplant complications, multislice CT angiography with 3D volume rendering is an exciting modality that may be the only imaging test required in the evaluation of patients after liver transplantation.


References
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 

  1. Tzakis AG, Gordon RD, Shaw BW Jr, Iwatsuki S, Starzl TE. Clinical presentation of hepatic artery thrombosis after liver transplantation in the cyclosporine era. Transplantation 1985;40:667 -671[Medline]
  2. Dodd GD III, Memel DS, Zajko AB, Baron RL, Santaguida LA. Hepatic artery stenosis and thrombosis in transplant recipients: Doppler diagnosis with resistive index and systolic acceleration time. Radiology 1994;192:657 -661[Abstract/Free Full Text]
  3. Abbasoglu O, Levy MF, Vodapally MS, et al. Hepatic artery stenosis after liver transplantation: incidence, presentation, treatment, and long-term outcome. Transplantation 1997;63:250 -255[Medline]
  4. Abad J, Hidalgo EG, Cantarero JM, et al. Hepatic artery anastomotic stenosis after transplantation: treatment with percutaneous transluminal angioplasty. Radiology 1989;171:661 -662[Abstract/Free Full Text]
  5. Platt JF, Yutzy GG, Bude RO, Ellis JH, Rubin JM. Use of Doppler sonography for revealing hepatic artery stenosis in liver transplant recipients. AJR 1997;168:473 -476[Abstract/Free Full Text]
  6. Nolten A, Sproat IA. Hepatic artery thrombosis after liver transplantation: temporal accuracy of diagnosis with duplex US and the syndrome of impending thrombosis. Radiology 1996;198:553 -560[Abstract/Free Full Text]
  7. Winter TC, Freeny PC, Nghiem HV, et al. Hepatic arterial anatomy in transplantation candidates: evaluation with three-dimensional CT arteriography. Radiology 1995;195:363 -370[Abstract/Free Full Text]
  8. Nghiem HV, Dimas CT, McVicar JD, et al. Impact of double helical CT and three-dimensional CT arteriography on surgical planning for hepatic transplantation. Abdom Imaging 1999;24:278 -284[Medline]

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