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AJR 2001; 177:1101-1107
© American Roentgen Ray Society


Vascular and Extravascular Complications of Liver Transplantation

Comprehensive Evaluation with Three-Dimensional Contrast-Enhanced Volumetric MR Imaging and MR Cholangiopancreatography

Pari V. Pandharipande1, Vivian S. Lee1, Glyn R. Morgan2, Lewis W. Teperman2, Glenn A. Krinsky1, Neil M. Rofsky1,3, Marie-Christine Roy1,4 and Jeffrey C. Weinreb1

1 Department of Radiology, Division of Magnetic Resonance Imaging, Basement, Schwartz Bldg., NYU Medical Center, 530 First Ave., New York, NY 10016.
2 Department of Surgery, Division of Transplant Surgery, NYU Medical Center, 403 E. 34th St., New York, NY 10016.
3 Present address: Department of Radiology, Beth Israel Deaconess Medical Center, 330 Brookline Ave., Boston, MA 02215.
4 Present address: Departement de Radiologie, Hopital Maisonneuve-Rosemont, 5415 Blvd. de l'Assomption, Montreal, Quebec H1T 2M4, Canada.

Received November 28, 2000; accepted after revision May 22, 2001.

 
Address correspondence to V. S. Lee.


Abstract
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
OBJECTIVE. Our purpose was to evaluate a comprehensive MR imaging strategy for recipients of liver transplants that relies on dynamic interpolated three-dimensional (3D) MR imaging for simultaneous vascular, parenchymal, and extrahepatic imaging.

MATERIALS AND METHODS. Twenty-three consecutive adult patients underwent 30 MR imaging examinations between 2 days and 99 months (mean, 15 months) after transplantation using a breath-hold 3D gradient-echo sequence (TR range/TE range, 3.7-4.7/1.8-1.9; flip angle, 12-30°) with an intermittent fat-saturation pulse and interpolation in the section-select direction to enable pixel size 3 mm or less in all dimensions. Unenhanced and triphasic contrast-enhanced 3D imaging (average dose, 0.13 mmol/kg of gadopentetate dimeglumine) was performed. A subset of patients (n = 13) also underwent MR cholangiopancreatography using half-Fourier single-shot turbo spin-echo imaging. MR imaging examinations were correlated with digital subtraction angiography (n = 8), contrast-enhanced cholangiography (n = 9), sonography (n = 13), and histopathology (n = 14).

RESULTS. MR imaging revealed abnormal findings in 27 (90%) of 30 examinations, including vascular disease in nine, biliary complications in four, and evidence of intra- or extra-hepatic hepatocellular carcinoma recurrence in six. Digital subtraction angiography confirmed seven MR angiography examinations but suggested disease overestimation in one. Contrast-enhanced cholangiography confirmed findings of MR cholangiopancreatography in seven cases but suggested disease underestimation in two.

CONCLUSION. Dynamic interpolated 3D MR imaging combined with dedicated MR cholangiopancreatography can provide a comprehensive assessment of vascular, biliary, parenchymal, and extrahepatic complications in most recipients of liver transplants.


Introduction
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Advances in the care of recipients of liver transplants combined with refinements in surgical technique have contributed to a current 1-year survival of 87.9% after transplantation [1]. In the acute and subacute phases after surgery, common graft-related complications include rejection, hepatic arterial and portal venous compromise, biliary duct strictures, and bile leaks. In addition to vascular and biliary sequelae, chronic phase complications can include the recurrence of pretransplantation liver disease, such as cirrhosis and hepatocelular carcinoma (HCC) [2,3,4,5].

Certain vascular, biliary, parenchymal, and extrahepatic complications in recipients of liver transplants can be shown well on imaging when the appropriate modality is used. However, because these patients frequently present with nonspecific clinical symptoms, a multimodality approach is often required. Sonography is commonly used to screen for vascular, biliary, and parenchymal abnormalities, although its sensitivity for the detection of hepatic arterial and biliary disease may be low [6,7,8]. Thus, conventional angiography and cholangiography are used to identify definitively vascular and biliary complications, respectively. Additionally, CT and MR imaging are often used to evaluate the liver parenchyma and extrahepatic structures. Although CT in conjunction with CT angiography can provide a noninvasive evaluation of parenchymal and vascular structures [9, 10], supplementary cholangiography is still required for a comprehensive evaluation. MR cholangiopancreatography has proven to be an accurate means of evaluating the biliary system in recipients of transplants [11, 12]. Moreover, hepatic MR angiography can be performed in the same setting as MR cholangiopancreatography and serves as a compelling alternative to invasive angiography [13,14,15]. Until recently, however, hepatic MR angiography has been performed to optimize vascular imaging at the expense of background structures, such as liver parenchyma [13,14,15].

An MR imaging approach using three-dimensional (3D) interpolated gradient-echo MR imaging has recently become available that enables high-resolution, near-isotropic imaging of the entire abdomen in a breath-hold. When performed dynamically after contrast administration, this technique allows simultaneous evaluation of the liver parenchyma and vascular structures [16, 17]. The addition of MR cholangiopancreatography sequences to dynamic 3D MR imaging allows all relevant anatomic systems to be depicted at a single MR imaging examination [11, 12, 18].

In this study, we compared the MR imaging results of a retrospectively identified cohort of recipients of orthotopic liver transplants who underwent 3D MR imaging with or without supplementary MR cholangiopancreatography with those of correlative imaging examinations, including conventional angiography, cholangiography, and sonography, and with relevant histopathology. Our purpose was to evaluate the accuracy and usefulness of a comprehensive MR imaging strategy for recipients of liver transplants.


Materials and Methods
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Using a computerized MR imaging database, we retrospectively identified 35 consecutive abdominal MR imaging examinations from 26 recipients of orthotopic liver transplants performed between March 1998 and January 2000. Patients were unable to meet the breath-holding requirements ({approx}20 sec) of 3D MR imaging in fire cases; these examinations were excluded from the study. The remaining 30 examinations were performed in 23 patients who constituted the study group (18 men, five women; age range, 31-67 years; mean age, 50 years). A subset of these patients was studied on two (n = 1) or three (n = 3) separate occasions.

Original causes of liver failure in the study group included cirrhosis caused by chronic hepatitis C (n = 13), hepatitis B (n = 2), or coinfection with hepatitis B and C (n = 2); fulminant hepatitis B (n = 1) or hepatitis E (n = 1); alcohol-related liver disease (n = 1); primary biliary cirrhosis (n = 1); cryptogenic cirrhosis (n = 1); and autoimmune liver disease (n = 1). Previous graft rejection necessitated retransplantation in two patients before MR imaging. Fourteen (61%) of twenty-three patients had histologic evidence of HCC in their native explanted livers.

Each MR imaging examination was requested by our institution's liver transplantation team with the intention of answering a specific clinical question directly related to patient care. Referral indications included the following: HCC surveillance (n = 7), abnormal finding on sonography suggesting vascular insufficiency (n = 6), elevated results on liver function tests (n = 5), elevated {alpha}-fetoprotein (n = 4), abdominal pain (n = 3), abnormal findings on contrast-enhanced cholangiography suggesting biliary compromise (n = 2), intermittent fever (n = 1), abnormal findings on sonography suggesting fluid collection (n = 1), and follow-up imaging for hepatic artery angioplasty (n = 1). MR imaging was performed from 2 days to 99 months after liver transplantation (mean interval, 15 months). Although most examinations were performed to assess complications arising more than 1 month after transplantation (n = 28), two were performed within 1 month of surgery.

MR Imaging Protocol
After written informed consent for the administration of contrast material, all patients underwent imaging with a 1.5-T MR system and a torso phased array coil. Most examinations (n = 22) were performed on a unit with a 25 mT/m maximal gradient strength and 600-µsec rise time (Vision; Siemens, Erlangen, Germany); the remainder (n = 8) were performed on a unit with a 20 mT/m maximal gradient strength and 400-µsec rise time (Symphony; Siemens). Before the study, a 22-gauge IV catheter was placed in an arm vein and attached to an MR-compatible power injector (Spectris; Medrad, Pittsburgh, PA). Before 3D MR imaging, all patients underwent imaging with fast short inversion time inversion recovery turbo spin-echo and T1-weighted in-phase and out-of-phase gradient-echo sequences, according to our routine protocol.

Three-Dimensional Volumetric Imaging
We used an interpolated 3D spoiled gradient-echo sequence similar to that described in the literature [16, 17]. Imaging parameters included the following: TR range/TE range, 3.7-4.7/1.8-1.9; flip angle, 12° (n = 25) or 18-30° (n = 5); mean acquisition time, 20 sec (range, 15-27 sec). Sequence details are summarized briefly as follows: symmetric echo (160 points) in the read direction (ky, left-to-right); symmetric echo in the phase-encoding direction (ky, anteroposterior) in the original sequence design (n = 16), and 80% partial Fourier sampling (128/160 points) in a revised sequence (n = 14) in which each 160 partition was interpolated to a 256 matrix; asymmetric echo sampling in the section-select direction (kz, superior-to-inferior) to obtain 32-64 data points that were then interpolated using zero-filling (sinc interpolation) to produce 64-128 partitions.

Use of a rectangular field of view resulted in an inplane spatial resolution of 2.8 mm or less for the 160 matrix; pixel size of 1.8 mm or less was obtained using the full 256 matrix. Section thickness ranged from 160 to 232 mm to ensure full coverage of the liver and yielded a partition thickness of 1.6-3.0 mm. The 3D sequence incorporated a frequency-selective fat-saturation pulse before each partition (section) loop. Each partition loop was centric-reordered to maximize fat saturation.

In all cases, unenhanced interpolated 3D MR imaging was performed first, followed by a timing examination, and then repeated three times at 45-sec intervals after administration of 19 mL of gadopentetate dimeglumine (average, 0.13 mmol/kg; Magnevist; Berlex Imaging, Wayne, NJ). The timing examination was performed as described by Earls et al. [19], who used a 1-mL test dose of contrast material; delay time was calculated as described by Prince et al. [20]. All 3D examinations were performed during breath-holding at the end of expiration.

MR Cholangiopancreatography
MR cholangiopancreatography was performed in 14 examinations in 13 patients with coronal or axial half-Fourier acquisition single-shot turbo spin-echo imaging, or both. Half-Fourier acquisition single-shot turbo spin-echo sequence parameters for both coronal and axial imaging varied as follows: TR/effective TE, infinite/43 or 62 msec; refocusing pulse, 120-180°; field of view, 300-400 mm; matrix, 128-208 x 256; section thickness, 4.0-8.0 mm; mean acquisition time, 29 sec. MR cholangiopancreatography was performed before gadolinium contrast administration in all patients.

Image Processing and Interpretation
Before 3D MR imaging, all patients underwent imaging with short tau inversion recovery and T1-weighted in-phase and out-of-phase gradient-echo sequences, according to our routine protocol. Volumetric 3D imaging source data were routinely evaluated interactively on a commercially available MR workstation (Numaris, Siemens), and pertinent multiplanar reconstructions were performed. For each study, the time required to create multiplanar reconstructions was approximately 8-10 min.

Abnormal findings on vascular evaluations were prospectively reported to show thrombotic disease, focal stenotic disease, or "vessel attenuation," a term used to describe diffuse narrowing without dominant focal stenoses. The hepatic parenchyma was evaluated for focal disease, including tumor and fluid collection, and the presence of diffuse hepatic processes, such as periportal edema and perihepatic fluid. The biliary system was primarily evaluated for stricture and bile leak. All abnormal extrahepatic findings, including findings suggestive of recurrent metastatic HCC in particular, were also reported prospectively. MR imaging reports dictated at the time of imaging served as the primary source of data in this study. In cases of discrepancy between MR imaging findings and correlative imaging results, MR imaging studies were retrospectively reviewed to evaluate possible sources of error.

Data Analysis
Each patient's imaging records were reviewed to identify digital subtraction angiography, contrast-enhanced cholangiography (T-tube cholangiography, percutaneous transhepatic cholangiography, and endoscopic retrograde cholangiopancreatography), and sonographic evaluations that were performed close to the time of MR imaging. Our search yielded correlative imaging studies for 20 (67%) of 30 3D MR imaging examinations and 17 (74%) of the 23 patients included in this study. Correlative vascular imaging studies (digital subtraction angiography, sonography, or both) were available for 17 (57%) of 30 3D MR imaging examinations and 14 (61%) of the 23 patients included in the study. Correlative imaging studies included eight digital subtraction angiography examinations performed within 45 days (mean interval, 12 days) after eight MR imaging studies from seven patients; 13 sonographic examinations performed within 7 days (mean interval, 3 days) before 13 MR imaging studies from 11 patients; and nine contrast-enhanced cholangiograms obtained within 5 days (mean interval, 2 days) of nine MR imaging studies from seven patients. Dedicated MR cholangiopancreatograms were used in six of the nine MR imaging examinations from six of the seven patients with correlative contrast-enhanced cholangiography.

Correlative histopathology was available for 14 (47%) of 30 MR imaging examinations from 10 (43%) of 23 patients, five of whom underwent liver biopsy to evaluate for diffuse parenchymal disease, such as graft rejection, and five of whom underwent biopsy of an extrahepatic mass to determine HCC recurrence. Of the 20 MR imaging examinations for which correlative imaging was available, nine also had correlative histopathology. Thus, correlative digital subtraction angiography, sonography, contrast-enhanced cholangiography, histopathology, or a combination of these was available for 25 (83%) of 30 MR imaging examinations and 18 (78%) of 23 patients in the study.

Patient medical records were reviewed in all cases to determine the clinical context of each imaging study and to ensure that patients' clinical courses did not change between MR imaging and correlative imaging evaluation. In addition, the liver transplantation team clarified the clinical course and follow-up of patients with complicated histories.


Results
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Thirty 3D MR imaging examinations were successfully completed without complications for the study cohort of 23 patients. Abnormal findings were shown in 27 (90%) of 30 examinations from 21 (91%) of 23 patients. Dedicated MR cholangiopancreatography revealed abnormal findings in three (21%) of 14 examinations from three (23%) of 13 patients. Of the five MR imaging examinations for which no correlative imaging or histopathology was available, three revealed no abnormal findings. Thus, correlative digital subtraction angiography, sonography, contrast-enhanced cholangiography, histopathology, or a combination of these was available for all except two of the 27 MR imaging examinations with abnormal findings. Of these two, one MR imaging examination depicted an incisional hernia, but no other abnormalities; this finding was determined by physical examination before MR examination. The other MR imaging examination showed a single 1-cm intrahepatic lesion that had signal characteristics consistent with a fast-filling hemangioma, unchanged from a prior CT.

Vascular Complications
Vascular complications at MR imaging were detected in nine examinations from eight patients and included the following findings: celiac artery stenosis (n = 2) (Fig. 1A,1B), hepatic artery thrombosis (n = 2) (Fig. 2A,2B), hepatic artery attenuation (n = 2), mild to moderate hepatic artery stenosis (n = 2), attenuation of intrahepatic arterial branches (n = 4), and portal vein stenosis (n = 1).



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Fig. 1A. 54-year-old man referred for MR imaging with absent hepatic arterial tracing on Doppler sonography (not shown). Lateral image of volume-rendered arterial phase contrast-enhanced three-dimensional MR angiogram (TR/TE, 3.8/1.8; flip angle, 25°) shows celiac artery stenosis (arrow).

 


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Fig. 1B. 54-year-old man referred for MR imaging with absent hepatic arterial tracing on Doppler sonography (not shown). Correlative digital subtraction angiogram confirms findings in A of celiac artery stenosis (arrow).

 


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Fig. 2A. 33-year-old man referred for MR imaging 4 months after liver transplantation for suspected hepatic arterial compromise in context of known biliary compromise. Oblique frontal image of volume-rendered arterial phase contrast-enhanced three-dimensional MR angiogram (TR/TE, 4.2/1.8; flip angle, 12°) shows hepatic artery thrombosis (arrow).

 


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Fig. 2B. 33-year-old man referred for MR imaging 4 months after liver transplantation for suspected hepatic arterial compromise in context of known biliary compromise. Correlative digital subtraction angiogram confirms findings in A of hepatic artery thrombosis (arrow).

 

Of the eight MR angiographic studies with correlative digital subtraction angiography, MR angiography that showed no abnormal findings was confirmed in four cases, and abnormal findings on MR angiography were confirmed in three. Disease was overestimated in one patient who underwent MR angiography and digital subtraction angiography within 3 days after transplantation and in whom severe attenuation of the hepatic artery and of the hepatic artery branches seen on MR angiography was not depicted on digital subtraction angiography; digital subtraction angiography instead revealed only mild stenosis at the origin of the left hepatic artery (Fig. 3A,3B). However, slow flow suggestive of high hepatic arterial resistance was noted at digital subtraction angiography. A retrospective review of MR images from all phases of dynamic imaging with knowledge of digital subtraction angiography findings did not change the initial MR imaging interpretation in this case.



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Fig. 3A. 54-year-old man referred for MR imaging with abnormal hepatic arterial waveforms on Doppler sonography (not shown) 2 days after liver transplantation. Frontal image of volume-rendered arterial phase contrast-enhanced three-dimensional MR angiogram (TR/TE, 4.2/1.8; flip angle, 25°) shows hepatic artery attenuation originating at bifurcation (arrow) of right and left hepatic arterial branches.

 


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Fig. 3B. 54-year-old man referred for MR imaging with abnormal hepatic arterial waveforms on Doppler sonography (not shown) 2 days after liver transplantation. Correlative digital subtraction angiogram shows nearly normal hepatic arterial tree (arrow). On other projections, mild stenosis was seen at origin of left hepatic artery (not shown). Digital subtraction angiographic findings suggest overestimation of arterial disease on MR angiography. Slow hepatic arterial flow noted during digital subtraction angiography may have resulted in attenuated appearance of hepatic artery and its branches on MR angiography.

 

An equivocal finding was present in the MR angiography examination of one patient; a region of signal loss in the hepatic artery was thought to be a result of either surgical clips or stenotic disease. A direct comparison of findings on MR angiography and digital subtraction angiography confirmed the presence of surgical clips in the region of question. This patient also had disease at the origin of the celiac axis detected on both MR angiography and digital subtraction angiography.

Thirteen MR imaging examinations from 11 patients were compared with 13 sonographic studies performed within 7 days before MR imaging. In four cases, both sonography and MR angiography revealed normal celiac and hepatic arterial systems; in five cases, both modalities depicted abnormal findings. In two of the five cases, arterial abnormalities were confirmed at digital subtraction angiography: in one, the absence of a hepatic arterial tracing at sonography led to subsequent evaluation with MR angiography and digital subtraction angiography, both of which revealed celiac artery stenosis consistent with median arcuate ligament compression; in the other, hepatic arterial stenosis found at sonography also led to subsequent evaluation with MR angiography and digital subtraction angiography, both of which revealed diffuse attenuation of the hepatic artery and intrahepatic arterial branches. In one of the five cases, discussed previously in the context of the patient in whom hepatic arterial disease was overestimated at MR angiography, sonographic findings also overestimated arterial disease when compared with those of digital subtraction angiography.

MR angiography and sonography yielded discrepant results in four examinations from three patients. In one patient, sonography showed likely hepatic arterial stenosis; however, findings on follow-up MR angiography were normal. Sonography revealed no hepatic artery disease in two patients in whom MR angiography revealed disease. In one patient, mild to moderate hepatic artery stenosis shown on MR angiography was not observed on sonography; in the other patient, sonography failed to reveal hepatic artery thrombosis noted on both MR angiography and digital subtraction angiography during the patient's first imaging workup. Sonography was equivocal at a later imaging workup of this patient, during which MR angiography showed recurrent thrombosis. Collateral arterial vessels were revealed on MR angiography on both occasions.

Sonography of the portal vein that showed no abnormal findings was consistent with MR angiographic findings in 12 cases. However, findings on MR angiography and sonography were discrepant in one patient in whom portal vein stenosis shown on MR angiography was not observed on sonography. The portal venous system was not further evaluated in this patient and was not a suspected cause of further complications in this patient at clinical follow-up.

Biliary Complications
Biliary abnormalities were shown on MR imaging in four examinations from three patients and included presumed bile leak (n = 3) and a choledochocholedochostomy anastomotic stricture (n = 1) (Fig. 4A,4B) visualized on the basis of supplementary MR cholangiopancreatography sequences in three of the four examinations. In the case of the anastomotic stricture, MR imaging was performed before correlative contrast-enhanced cholangiography. Periportal fluid collections visualized at MR imaging were assumed to represent bile leaks on the basis of the knowledge of the results of prior contrast-enhanced cholangiography.



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Fig. 4A. 38-year-old man who was referred for MR imaging with elevated liver function tests. Coronal half-Fourier acquisition single-shot turbo spin-echo image (TR/TE, infinite, 62; refocusing pulse, 120°) shows abrupt change in caliber of distal common bile duct suggestive of anastomotic stricture (white arrow). Central signal loss in common bile duct is due to presence of biliary catheter (black arrow).

 


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Fig. 4B. 38-year-old man who was referred for MR imaging with elevated liver function tests. T-tube cholangiography confirms presence of stricture (arrow).

 

Of the nine MR imaging studies with correlative contrast-enhanced cholangiography, normal MR imaging findings were confirmed in three cases, and abnormal MR imaging findings were confirmed in four cases. False-negative interpretations of biliary disease occurred in two MR examinations from two patients, both of whom underwent dedicated MR cholangiopancreatography. A choledochocho-ledochostomy anastomotic stricture detected on contrast-enhanced cholangiography was missed on MR imaging in one patient. The stricture was detected in a retrospective review of this MR imaging study but was a subtle finding because of the absence of common bile duct dilatation proximal to the stricture. A plastic common bile duct stent in another patient resulted in regional signal loss, prohibiting an adequate analysis of the stent lumen at MR cholangiopancreatography. When the stent was subsequently removed at endoscopic retrograde cholangiopancreatography, it was found to be partially occluded.

Intrahepatic and Extrahepatic Tumor
Evidence of recurrent HCC was detected on MR imaging in six patients (Figs. 5 and 6), all of whom had histologic evidence of multifocal HCC in their native explanted liver specimens. In these six patients, evidence of recurrent extrahepatic HCC was detected on MR imaging in the following distribution: lung bases (n = 4), adrenal glands (n = 3), subcutaneous fat (n = 2), lymph nodes (n = 2, paraaortic and portacaval), vertebral body (n = 1), and peritoneum (n = 1). Of these patients, three also had simultaneous evidence of intrahepatic HCC. Five of the six patients underwent biopsy of an extrahepatic mass; histopathologic results confirmed HCC recurrence in all cases. The remaining patient underwent digital subtraction angiography before MR angiography, revealing multiple hypervascular hepatic masses consistent with recurrent HCC; subsequent chemoembolization was performed. One patient had a single 1-cm intrahepatic lesion that had signal characteristics consistent with a fast-filling hemangioma, unchanged from a prior CT. This patient was doing well 1 year after MR imaging with no clinical data to suggest recurrent HCC.



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Fig. 5. 59-year-old man with recurrent hepatocellular carcinoma 8 months after liver transplantation. Axial image from arterial phase contrastenhanced three-dimensional MR imaging (TR/TE, 4.5/1.9; flip angle, 12°) shows multiple intrahepatic masses (short arrows identify subset of visible lesions) and subcutaneous nodule (long arrow) with dynamic imaging features consistent with hepatocellular carcinoma. Subsequent biopsy of subcutaneous nodule confirmed recurrent hepatocellular carcinoma.

 


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Fig. 6. 57-year-old man with recurrent hepatocellular carcinoma 27 months after liver transplantation. Axial image from arterial phase contrast-enhanced three-dimensional MR imaging (TR/TE, 4.2/1.9; flip angle, 12°) shows large portacaval lymph node (arrow) subsequently biopsied and found to be consistent with recurrent hepatocellular carcinoma.

 

Diffuse Parenchymal Disease
Five patients underwent liver biopsy within 23 days of MR imaging. Biopsy results included rejection (chronic [n = 2], acute [n = 1], acute vs drug toxicity [n = 1]), and infectious hepatitis [n = 1]). Two patients showed potentially associated, but nonspecific, findings on MR imaging. Perihepatic fluid was noted in the patient with hepatitis, and periportal edema was noted in the patient with acute rejection versus drug toxicity by biopsy. Of the remaining three patients, one had a high resistance pattern of the hepatic artery on sonography, and subsequent MR angiography showed diffuse attenuation of the intrahepatic arterial branches. One had a known biliary anastomotic stricture, and one had no evidence of vascular or biliary compromise during her workup.

Miscellaneous Extrahepatic Findings
Extrahepatic findings on MR imaging included postoperative seroma (n = 3), DeBakey type III aortic dissection (n = 1), subcapsular fluid collection causing compression of the liver (n = 1), splenic infarct (n = 1), and incisional hernia (n = 1). Although the aortic dissection and incisional hernia were previously known, other findings were first depicted on MR imaging.


Discussion
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
The distinctive feature of the interpolated 3D MR imaging technique used in this study is its ability to provide dynamic contrast-enhanced imaging sufficient for simultaneous evaluation of the liver parenchyma and the hepatic arterial and venous systems of recipients of liver transplants. Vascular complications have been reported to occur in 3-12% of recipients of liver transplants [21,22,23,24] and may result from anastomotic strictures or secondary compromise such as celiac artery compression, as found in two patients in our series (Fig. 1A,1B). In our study of patients referred with a wide spectrum of indications, including suspected vascular compromise, vascular complications were detected in eight (35%) of 23 patients.

Our combined vascular and parenchymal 3D MR imaging approach yielded results comparable with those reported using dedicated MR angiography sequences [13,14,15]. Two other groups of researchers have investigated the accuracy of dynamic 3D MR angiography in evaluating recipients of liver transplants using digital subtraction angiography, surgical findings, or both for comparison [14, 15]. Both studies used dedicated 3D MR angiography with a higher flip angle (35° [15] and 45° [14] vs 12° typically used in our study) to achieve greater background suppression and higher doses of gadolinium contrast material (40-60 mL vs 20 mL in our study). For their 19 patients with correlative digital subtraction angiography, surgical findings, or both, Glockner et al. [15] reported one false-negative and three false-positive MR angiographic interpretations of hepatic arterial stenosis and one false-positive interpretation of portal venous stenosis. Stafford-Johnson et al. [14] reported minor discrepancies of hepatic artery and inferior vena cava disease on MR imaging in four patients of the 13 they studied. In our study, MR angiographic findings were confirmed at digital subtraction angiography in seven of eight examinations; hepatic arterial disease was markedly overestimated on MR imaging in only one patient.

Although factors such as spatial resolution and signal loss in regions of disturbed flow are known causes of error in disease estimation on MR angiography, two other factors may arise in the context of recipients of liver transplants. First, surgical clips and stents create regional signal loss on MR imaging, although investigative efforts to identify MR imaging strategies that minimize such artifacts are underway [25, 26]. Second, low-flow states, commonly present in newly transplanted edematous, ischemic, or necrotic livers and during systemic hypotension and graft rejection, have been shown to contribute to false-positive interpretations of vascular disease [6, 27]. In the patient in our study in whom arterial disease was overestimated at MR angiography, slow hepatic arterial flow (as shown at digital subtraction angiography) likely resulted from edematous hepatic parenchyma associated with recent transplantation. Similarly, Glockner et al. [15] reported arterial disease overestimation on MR angiography in two patients with graft rejection. Thus, MR angiographic interpretation should be conducted with an understanding of clinical factors that may contribute to low-flow states.

In our series, hepatic arterial thrombosis detected on MR angiography and on digital subtraction angiography was missed on sonography in one patient. In this patient, the presence of collateral arterial vessels shown on MR angiography likely accounted for disease underestimation on sonography, a reported limitation of sonography in the context of recipients of liver transplants [6, 7]. The use of high-resolution contrast-enhanced imaging as opposed to flow-dependent imaging likely reduces false-negative interpretations of hepatic arterial disease in the presence of collateral vessels.

HCC recurrence has been reported in 7-40% of recipients of liver transplants with a pretransplantation history of HCC [2,3,4,5]. Our MR imaging approach enabled detection of intra- and extrahepatic masses suspicious for recurrent HCC in six (26%) of 23 patients, all of whom had biopsy or other imaging data consistent with HCC recurrence. Three features of the 3D MR imaging technique described in this study serve to optimize tumor surveillance. First, interpolation methods allow imaging with thinner sections than those typically obtained in routine abdominal MR imaging, thereby improving the likelihood of small-lesion detection and characterization. Second, a timing examination ensures reliable arterial phase imaging for improved HCC detection. As many as 9-11% of patients with HCC have been reported to have tumors visible only during arterial phase imaging [28,29,30]. Third, our technique enables complete evaluation of the upper abdomen, including the lung bases and adrenal glands, common sites for HCC metastases [5]. Our technique is not sufficient for evaluation of suspected recurrent HCC in the chest, for which CT should be performed. A liberal extrahepatic examination does, however, provide valuable insight into nonspecific clinical symptoms, such as abdominal pain, by allowing detection of unsuspected abnormalities such as splenic disease or postoperative fluid collections, as observed in our series.

A limitation of the parenchymal evaluation provided by MR imaging is its inability to depict findings specific for rejection of a liver transplant [31]. Because other imaging modalities are also limited in identifying graft rejection [32, 33], patients with suspected rejection continue to require biopsy for a definitive diagnosis. The interpolated 3D MR imaging approach is also limited at present to patients who can breath-hold for 20 sec. Recipients of a transplant who are severely debilitated or intubated, therefore, cannot benefit from 3D MR imaging. However, continued improvements in MR technology already have shortened minimum TRs and TEs and will continue to do so, thereby reducing breath-hold requirements. Other limitations of the proposed approach are the inability to visualize accurately small hepatic vessels and the overestimation of vascular disease in low-flow states. Using higher doses of IV contrast material may improve both small artery visualization and vascular disease characterization in low-flow states and deserves further investigation.

Although no false-positive interpretations were made on MR cholangiopancreatography in our study, two complications detected at contrast-enhanced cholangiography were prospectively missed and illustrate important limitations of MR cholangiopancreatography in recipients of transplants. First, one anastomotic stricture was missed, in part because of the lack of biliary dilatation proximal to the stenosis. The absence of such dilatation has been reported to have poor negative predictive value for biliary duct obstruction on contrast-enhanced cholangiography in recipients of liver transplants [34]. Second, partial occlusion of a common bile duct stent was missed on MR cholangiopancreatography because of signal loss associated with the stent. In this setting, functional MR cholangiopancreatography has the potential to improve evaluation of the biliary system and deserves further investigation (Kim J-H et al., presented at the International Society for Magnetic Resonance in Medicine meeting, April 2000).

In our study, periportal fluid collections depicted on MR cholangiopancreatography were presumed to represent biliary leaks on the basis of known contrast-enhanced cholangiographic results. Currently, it is difficult to distinguish a periportal biliary leak from a postoperative seroma on MR cholangiopancreatography alone, without contrast-enhanced cholangiography. A new approach using MR imaging that may enable this distinction has been reported by Vitellas et al. [35], who have recently shown that mangafodipir trisodium, an approved MR imaging biliary contrast agent excreted by the biliary system, can be useful for detecting biliary leaks on MR cholangiopancreatography. In the future, this approach may obviate contrast-enhanced cholangiography for the diagnosis of biliary leaks in patients with periportal fluid collections.

In conclusion, the results of our study suggest that dynamic interpolated 3D MR imaging combined with dedicated MR cholangiopancreatography can provide a comprehensive assessment of vascular, biliary, parenchymal, and extrahepatic complications in most recipients of liver transplants. This study reflects our preliminary experience and is limited by its retrospective nature and number of patients; however, our results support further prospective investigation in this growing field of MR imaging.


References
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 

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