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Original Report |
1
Department of Radiology, University of Washington School of Medicine, 1959
N.E. Pacific St., Seattle, WA 98195-7115.
2
Department of Radiology (114), Veterans Affairs Medical Center, 1660 S.
Columbian Way, Seattle, WA 98108-1597.
3
Department of Surgery, University of Washington School of Medicine, Seattle,
WA 98195-7115.
Received November 1, 1999;
accepted after revision January 14, 2000.
Address correspondence to W.B. Eubank.
Abstract
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CONCLUSION. Venous thrombus appeared as serpetine voids within the graft parenchyma or at the venous anastomosis during the venous phase of MR imaging. Nonenhancement or heterogeneous enhancement of graft parenchyma corresponded to glandular necrosis at pancreatectomy in two patients. Initial sonographic evaluation was nondiagnostic of venous thrombosis in two of five patients. Multiphasic breath-hold gadolinium-enhanced three-dimensional MR imaging of pancreatic transplants can provide information to make the specific diagnosis of venous thrombosis or occlusion.
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Several diagnostic imaging techniques have been used in the evaluation of pancreatic graft dysfunction. Scintigraphy, CT, grayscale sonography [4], and MR imaging using standard spin-echo techniques [5] are sensitive but nonspecific for vascular abnormalities. Doppler sonography has shown promise in revealing venous thrombosis [6]; however, the graft may not always be visualized because of overlying bowel gas [7].
Breath-hold gadolinium-enhanced three-dimensional (3D) MR angiography has been evolving as a clinically useful noninvasive method of vascular imaging [8]. To our knowledge, findings from multiphasic breath-hold gadolinium-enhanced 3D MR studies have not been described in patients who have undergone pancreatic transplantation. We describe the findings with this technique of venous thrombosis and occlusion after pancreatic transplantation in five patients.
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All patients underwent color Doppler sonography as the first line of diagnostic imaging in the immediate period after transplantation. The average interval between pancreas transplantation and MR imaging was 22 days (time range, 5-53 days). One patient underwent two MR examinations. All patients were suspected of having venous thrombosis of the graft on the basis of abnormal findings on clinical examination, laboratory test results, or a recent color Doppler sonogram that was suggestive of venous thrombosis.
MR Imaging
All MR imaging was performed with a 1.5-T MR system (Signa Horizon
Echospeed [software version 6.6]; General Electric Medical Systems, Milwaukee,
WI). The peak gradient strength was 23 mT/m and maximum slew rate was 20 T/m
per sec. Patients were imaged in the supine position using a phased array
torso coil.
Imaging of the pelvis was performed using T1-weighted spin-echo (TR/TE, 750/14; field of view, 36-40 x 36-40 cm; matrix size, 256 x 192; and excitations, two) and respiratory-triggered fat-suppressed T2-weighted fast spin-echo sequences (TR range/TEeff range, 5000-18750/84-96; echo train length, eight; field of view, 32-40 x 24-40 cm; matrix size, 256 x 192-224; and excitations, two) with 5-mm slice thickness and an interslice gap of 1 mm.
Unenhanced 3D MR imaging of the pelvis in the coronal plane was performed using a spoiled fat-suppressed gradient-echo sequence (7.6/3.0; flip angle, 20°; field of view, 40 cm, 70% rectangular; bandwidth, 31.2 kHz; matrix size, 256 x 160-192; and excitation, one). The slice thickness was 5 mm for all examinations; 32-36 slices were acquired in a 24- to 36-sec breath-hold. Slice zero fill interpolation, a processing technique (General Electric Medical Systems), was used to improve depiction of small vessels on the 3D reconstructed images. Using these parameters, anatomic coverage of the pancreatic graft and the anastomoses to the iliac vessels was achieved. An Advantage Windows workstation (General Electric Medical Systems) was used to postprocess the images and generate both 3D-rendered (maximum intensity projection and shaded-surface display) and multiplanar reconstructed images. One observer prospectively interpreted and performed the postprocessing of the MR data.
Dimeglumine gadopentetate (Magnevist; Berlex Laboratories, Wayne, NJ) was injected IV by hand at a rate of 2-3 mL/sec for a total volume of 20 mL (dose of 0.1 mmol/kg of body weight) followed by a flush of 10 mL of sterile saline. Image acquisition of the first contrast-enhanced 3D volume set, using the same pulse sequence parameters as the unenhanced imaging, was begun after approximately half the contrast dose was injected. This volume set was considered to coincide with the arterial phase of contrast medium distribution. Two or three additional 3D volume sets, separated by 10-sec breathing periods, were subsequently obtained during the early and late venous phases of the examination.
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In the venous phase of all MR imaging, nonopacification of one or more venous structures, appearing as serpentine voids, was present within the graft parenchyma in the head of the pancreas (superior mesenteric vein) (Fig. 2A,2B), along the superior surface of the pancreatic body and tail (splenic vein) (Fig. 3A,3B,3C,3D), or at the anastomotic site between the donor portal vein and recipient common iliac vein (Fig. 4A). Complete lack of enhancement of the venous anastomosis was present in two patients: one patient had thrombus completely filling the anastomosis, confirmed at conventional venography (Fig. 4B), and the other had an isolated torsion of the portal vein discovered at pancreatectomy (Fig. 5A,5B). In two patients, the anastomosis between donor portal vein and recipient external iliac vein opacified but appeared severely narrowed (Fig. 3C). Opacification of the graft arterial system (Figs. 1B and 4A) was present in all patients.
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Abnormal parenchymal enhancement after administration of IV gadolinium was present in two patients; both had resections of necrotic pancreatic grafts. Complete lack of parenchymal enhancement was found in the patient with torsion of the donor portal vein (Fig. 5A,5B). Heterogeneous gland enhancement was present in the other patient with evolving glandular necrosis caused by venous thrombosis (Fig. 3A,3B,3C,3D). Peripancreatic fluid collections were present on three examinations and best shown on T2-weighted imaging (Fig. 2B).
Four patients were treated with anticoagulation after venous thrombosis was revealed on sonography or MR imaging. Two patients had partial splenic vein thrombosis: one confirmed by intraoperative Doppler sonography and the other by serial color Doppler sonography (Fig. 2A,2B). Both of these patients were treated with IV heparin and oral warfarin sodium (Coumadin; DuPont, Wilmington, DE) and have normally functioning grafts 8 months after institution of anticoagulation therapy. The patient with thrombus filling the venous anastomosis (Fig. 4A,4B) was treated acutely with intra-arterial infusion of tissue plasminogen activator followed by angioplasty of the venous anastomosis and systemic anticoagulation and had a normally functioning graft 6 weeks after therapy. One patient, with a narrowed venous anastomosis (Fig. 3A,3B,3C,3D), developed necrosis of the graft despite systemic anticoagulation.
Initial posttransplantation sonography was nondiagnostic in two (40%) of the five patients because of poor visualization of the graft. In the other three patients, findings on sonography were suggestive of venous thrombosis. In two of these three patients, a tubular structure filled with echoes near the venous anastomosis without demonstrable flow on color Doppler sonography suggested the diagnosis. High-resistance arterial flow in the graft parenchyma (Fig. 3A) and no flow in the splenic vein were the findings in the other patient.
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MR imaging of pancreatic grafts has been used primarily in the past for the detection and grading of potential rejection [5, 9]. Efforts have also been directed at detecting vascular complications of pancreatic grafts with MR angiographic techniques. Use of a time-of-flight MR angiographic technique by one group of investigators [10] showed high accuracy in making the diagnosis of thrombosis of either the arterial or venous anastomosis; however, in one patient (two examinations) with chronic rejection, the MR angiography was falsely positive. Gadolinium-enhanced 3D MR angiography has significant advantages over time-of-flight techniques, including shorter acquisition time, less respiratory related artifacts, less in-plane saturation of flowing blood, less signal loss from dephasing of spins in areas of turbulence, and better visualization of peripheral vessels, all of which allow more accurate depiction of vascular anatomy.
Venous thrombosis after pancreas transplantation typically occurs during the immediate posttransplantation period [6]. Predisposing factors include low venous flow rate in pancreatic grafts, technical problems such as tension or torsion of surgically created vascular pedicle, or vascular injury of the graft caused by preservation injury or pancreatitis. Venous thrombosis leading to infarction and parenchymal necrosis requires pancreatectomy [2]. Either partial or complete lack of enhancement of the graft parenchyma after the administration of IV gadolinium was present in both patients in our study who had proven parenchymal necrosis at pancreatectomy. The grafts in three patients that enhanced homogeneously have survived with ongoing anticoagulation therapy. This outcome suggests that venous thrombosis, if partial or limited by anticoagulation, is not always devastating for the pancreatic graft. This technique shows promise for both direct visualization of venous thrombosis and the assessment of graft parenchymal viability.
Multiphasic breath-hold gadolinium-enhanced 3D MR imaging has advantages over other imaging techniques used to detect vascular complications. Scintigraphy is sensitive to the detection of a vascular abnormality but lacks specificity [4]. CT and unenhanced MR imaging reveal morphologic changes of the graft and perigraft fluid collections that may occur as a result of a vascular complication but that are also nonspecific. Color and spectral Doppler sonography provide information about vascular patency and potential stenosis; however, visualization of the pancreatic graft is often obscured by overlying bowel gas. The grafts in two of the five patients in this study were not adequately visualized initially on sonography. However, sonography continues to be used as a screening method for patients suspected of having vascular complications after pancreas transplantation at our institution. Sonography is a relatively inexpensive and often more convenient method of examining patients in the immediate posttransplantation period. A multiphasic breath-hold gadolinium-enhanced 3D MR examination is reserved for patients whose grafts are nonvisualized on sonography or suspected of having venous thrombosis on the basis of the sonographic findings.
A major limitation of this study is the small number of subjects with venous thrombosis. Prospective evaluation of a larger series of patients with early graft dysfunction with multiphasic breath-hold gadolinium-enhanced 3D MR imaging and conventional angiographic correlation is necessary to determine the accuracy of this technique in making the diagnosis of venous thrombosis. Another limitation of this study was the method of patient selection for MR imaging. Several patients had findings suggestive of venous thrombosis on sonography; this selection process introduces a potential bias in our results. The high prevalence of positive findings on MR imaging in our study was caused in part by this selection bias.
No significant arterial complications were identified in the patients included in this study. In general, patients suspected of having a serious arterial complication such as an occluding thrombus, significant stenosis, or pseudoaneurysm are referred for conventional angiography because intraluminal therapeutic procedures potentially can be performed after making a diagnosis. The efficacy of breath-hold gadolinium-enhanced 3D MR imaging in the evaluation of arterial complications needs further investigation. Diagnostic MR imaging revealing a vascular complication amenable to intraluminal therapy would obviate the need for diagnostic conventional angiography, thereby decreasing the risk of nephrotoxicity associated with the administration of iodinated contrast material.
Several improvements could be made on our MR imaging technique. A timing-bolus examination performed before the contrast-enhanced data acquisition could optimize the individual examination [11]. In addition, the use of thinner slices (2 mm instead of 5 mm) would result in near-isotropic data acquisition, provided anatomic coverage of the transplanted pancreas is obtained in a reasonable breath-hold period. This procedure would allow postprocessing of data for 3D reconstruction or reformation with spatial resolution in any prescribed plane nearly equal to the plane in which the data were acquired (coronal, in our patients). The flexibility in visualizing the data in virtually any plane at the workstation offers potential advantages in making a diagnosis of vascular complications in these patients.
In conclusion, multiphasic breath-hold gadolinium-enhanced 3D MR imaging can provide information to make the specific diagnosis of venous thrombosis and to assess parenchymal viability after pancreas transplantation. This technique shows promise in the evaluation of early graft dysfunction when vascular complication is suspected and clinical examination and sonography are inconclusive.
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