DOI: 10.1148/rg.253045094
RadioGraphics 2005;25:687-695
© RSNA, 2005
Contrast-enhanced MR Angiography for Evaluation of Vascular Complications of the Pancreatic Transplant1
Nora Dobos, MD,
David A. Roberts, MD, PhD,
Erik K. Insko, MD, PhD2,
Evan S. Siegelman, MD,
Ali Naji, MD, PhD and
James F. Markmann, MD, PhD
1 From the Department of Radiology, MRI Learning Center, 1 Founders, Hospital of the University of Pennsylvania, Philadelphia (N.D., E.K.I., E.S.S., A.N., J.F.M.); and the Kennedy Health System, Cherry Hill, NJ (D.A.R.). Recipient of a Certificate of Merit award for an education exhibit at the 2003 RSNA Scientific Assembly. Received April 28, 2004; revision requested July 12 and received August 11; accepted August 18. All authors have no financial relationships to disclose.
Address correspondence to N.D., 7239 SW Capitol Hwy, Portland, OR 97219 (e-mail: dobosn{at}att.net).
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Abstract
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Vascular complications are a common cause of postoperative dysfunction in a pancreatic transplant. Coronal three-dimensional (3D) contrast material–enhanced magnetic resonance (MR) angiography performed with high spatial and temporal resolution is a safe and effective method of assessing these vascular complications. A study was performed of selected patients who had undergone MR imaging and MR angiography during the past 6 years for evaluation of graft dysfunction following pancreatic transplantation. Thrombosis within peripheral stump vessels involving either the arterial or venous segments was a commonly observed vascular complication. Isolated distal arterial stump thrombi are incidental findings that may not require treatment, whereas venous stump thrombi may become clinically significant in patients in whom clot propagates proximally to occlude draining pancreatic veins and are typically treated with anticoagulants or thrombectomy. Because it is difficult to predict which patients will experience clot propagation, patients with venous stump thrombi may be followed up with serial imaging regardless of treatment initiated at presentation. Although susceptibility artifacts can mimic anastomotic stenoses at MR imaging, careful attention to the multiple sequences used allows recognition of this potential pitfall. Contrast-enhanced 3D MR angiography is an accurate method of evaluating the vascular anatomy of pancreatic transplants and can help guide clinical management.
© RSNA, 2005
Abbreviations: CIA = common iliac artery, IVC = inferior vena cava, SMA = superior mesenteric artery, SMV = superior mesenteric vein, 3D = three-dimensional
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Introduction
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Vascular complications are a common cause of graft dysfunction following pancreatic transplantation (1,2). Clinical signs and symptoms in the early postoperative period are nonspecific and include graft tenderness, elevated serum glucose and pancreatic enzyme levels, and leukocytosis. Vascular thromboses can be treated empirically with anticoagulants, which may obviate the use of percutaneous biopsy, a more invasive procedure, to identify another cause of graft failure such as rejection. Furthermore, exclusion of vascular thrombosis may allow watchful waiting or empiric treatment for presumed rejection based on other clinical criteria, again obviating the use of an invasive procedure. A thorough understanding of the complex vascular anatomy is critical for accurate diagnosis of postoperative vascular complications (1). Optimally performed contrast material–enhanced magnetic resonance (MR) arteriography and MR venography offer an accurate method for evaluating these vascular complications and can help guide clinical management (3). MR imaging techniques that are tailored to the type of graft and vascular anatomy will ensure optimal visualization of the graft and associated vascular structures. Although computed tomographic (CT) angiography is technically less challenging, the use of gadolinium-enhanced MR angiography is preferred to eliminate potential nephrotoxicity from iodinated contrast material in these patients, who often harbor a renal allograft as well.
In this article, we review the vascular anatomy of pancreatic transplants and the MR imaging technique used to evaluate related complications. We also discuss vascular thrombosis and the effects of graft rejection on the transplant vessels. In addition, we discuss various MR imaging artifacts that can lead to misinterpretation of findings.
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Vascular Anatomy of Pancreatic Transplants
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During the harvest of transplant organs, the common hepatic artery is taken with the transplant liver; consequently, the superior pancreaticoduodenal supply to the pancreatic head via the gastroduodenal artery is sacrificed. As a result, the arterial supply to the pancreatic transplant is divided into (a) supply to the body and tail via the splenic artery and (b) supply to the head via the inferior pancreaticoduodenal artery from the superior mesenteric artery (SMA) (Fig 1). The lack of availability of the celiac trunk and common hepatic artery necessitates the additional harvest of an arterial Y graft of the donor common iliac artery (CIA) through its bifurcation. The transplant arterial anastomoses occur at the junction of the donor external iliac and donor splenic arteries, the junction of the donor internal iliac artery and donor SMA, and, finally, from the donor common iliac limb of the Y graft to the right common or external iliac artery of the recipient (Fig 2). The venous anastomoses connect the donor portal vein to the recipient inferior vena cava (IVC) or right common iliac vein (Fig 3) or to the SMV (Fig 4). The duodenal stump is preferably anastomosed to a segment of jejunum in the right side of the abdomen for enteric exocrine drainage (1,4), rather than to the bladder, which was the standard in past years.
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Figure 1. Drawing illustrates a pancreatic transplant after harvesting. a = portal vein stump, b = splenic vein stump, c = superior mesenteric vein (SMV) stump, d = splenic artery origin, e = splenic artery stump, f = SMA origin, g = SMA stump, h = inferior pancreaticoduodenal artery, i = inferior pancreaticoduodenal vein, j = dorsal pancreatic artery, k = dorsal pancreatic veins, l = duodenum.
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Figure 2. Drawing illustrates typical arterial anastomoses of a pancreatic transplant. a = Y graft donor CIA, b = Y graft donor external iliac artery, c = Y graft donor internal iliac artery, d = recipient CIA or external iliac artery.
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Study Population
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Using a DecRAD (radiology information system) search, we identified all patients who had undergone MR imaging and MR angiography during the past 6 years for evaluation of graft dysfunction following pancreatic transplantation and selected those in whom the vascular anatomy was clearly depicted.
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MR Imaging Technique
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All images in this article were obtained on 1.5-T systems using a full complement of abdominal MR imaging sequences in addition to a dedicated contrast material–enhanced MR angiographic sequence for a full anatomic parenchymal and vascular evaluation. This work was performed with the approval of the Institutional Review Board at the University of Pennsylvania. Initial coronal and sagittal single-shot fast spin-echo T2-weighted images are obtained to confirm appropriate coil placement in relation to the pancreatic transplant and to evaluate for peripancreatic fluid collections. Once satisfactory coil placement is confirmed, axial gradient-echo T1-weighted imaging with echo times of approximately 2.3 and 4.6 msec is performed to obtain both in-phase and opposed-phase images. T1-weighted images are useful in evaluating for normal pancreatic signal intensity (5) and for peripancreatic hematoma or hemorrhagic necrosis. Respiratory-gated T2-weighted imaging is performed to obtain anatomic images of the transplant and is also useful in evaluating for peripancreatic edema or lymph-adenopathy; the latter may be depicted in post-transplantation lymphoproliferative disease (6). Precontrast 3D imaging is performed to help confirm placement of the 3D volume. Next, gadolinium-based contrast material is administered, and coronal three-dimensional (3D) fat-suppressed breath-hold gradient-echo T1-weighted imaging is performed before and during dynamic phases of enhancement. The use of fat suppression aids in evaluating the signal intensity of the pancreas, which is normally hyperintense relative to the liver. Hyperintense intravascular thrombus secondary to methemoglobin (if present) will also be accentuated with this sequence. Furthermore, using identical parameters for precontrast and postcontrast sequences allows postprocessing, which can be used to subtract out hyperintense structures such as hematoma or bowel content on the precontrast images (7,8). Imaging is performed during both the arterial and venous phases of enhancement to evaluate the arterial and venous components of the transplant, respectively, followed by delayed axial fat-suppressed T1-weighted imaging. The dynamic sequence requires a relatively small field of view (<30 cm) with as high a matrix as possible given anatomic and patient limitations (320–384 in the frequency encoding direction and 160–192 in the phase encoding direction) to achieve high spatial resolution. The minimum achievable 3D slab thickness that encompasses the graft and relevant vascular anatomy is used to allow maximal spatial resolution (4-mm section thickness interpolated to 2 mm). At our institution, the physician monitoring the study is present at the console, assisting in prescribing the 3D volume and modifying the imaging parameters to achieve an optimal study within the clinical constraints. Patients are provided with careful breathing instructions, since respiratory motion will degrade image quality. Fortunately, these patients are usually ambulatory, fairly young, and highly motivated and can sustain long breath holds on the order of 30–40 seconds if necessary.
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Normal Vascular Anatomy of the Graft
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The placement of the pancreatic graft in the recipient is largely determined by the type of venous anastomosis (1). With systemic venous drainage, the donor portal vein and, therefore, the pancreatic head is placed in the pelvis or right lower quadrant due to the short length of portal vein available to create a venous anastomosis to a systemic vein such as the IVC, common iliac vein, or external iliac vein (Fig 5). No accessory venous grafts are used. With portal venous drainage, the venous anastomosis occurs at the level of the SMV just proximal to the native portosplenic confluence, necessitating placement of the pancreatic head within the right upper abdomen to the right of the native SMV (Fig 6) (1,4).
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Figure 5. Coronal contrast-enhanced 3D venous phase MR angiogram shows normal arterial supply and systemic venous drainage, with the venous anastomosis to the IVC and the pancreas situated in the right lower quadrant and pelvis. The donor SMV (arrowhead), splenic vein (small arrow), and splenic artery (large arrow) are all well demonstrated.
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Figure 6. Contrast-enhanced 3D venous phase MR angiogram shows normal portal venous drainage, with the venous anastomosis (arrow) to the recipient SMV just inferior to the portosplenic confluence.
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Arterial anastomoses do not affect graft placement, since the length of the arterial anastomosis is inherently flexible due to the incorporation of a variable-length Y graft, theoretically allowing the graft to be placed anywhere in the body (Fig 7).
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Figure 7. Coronal contrast-enhanced 3D arterial phase MR angiogram shows normal arterial anastomoses, with the arterial anastomosis of the Y graft to the recipient right CIA (arrow). The donor splenic artery (arrowhead) is well shown along the tail of the pancreatic transplant, thereby demonstrating the orientation of the pancreas.
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Vascular Thrombosis
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Vascular stumps are created on both the venous and arterial components of the transplant. There is typically a redundant tortuous splenic artery stump that is ligated distal to the blood supply to the pancreatic tail via the dorsal pancreatic artery and splenic artery perforators. A similar situation exists with the donor SMA stump, which is ligated a variable distance distal to the origin of the inferior pancreaticoduodenal artery, which supplies the pancreatic head (Fig 1).
On the venous side, the peripheral segment of the donor splenic vein does not receive significant venous drainage from the pancreatic body and tail. Similarly, the ligated stump of the SMV occurs a variable distance from the inferior pancreaticoduodenal vein, which drains blood from the pancreatic head into the SMV (Fig 1).
Stagnant blood often clots in these low-circulation stump areas. It is not uncommon to identify stump thrombi within either the arterial or venous segments, especially in the longer stumps.
Short-segment stump thrombi occurring within peripheral segments of vessels that do not contribute arterial supply or venous drainage to the pancreatic graft are often incidental findings and do not interfere with the normal vascular function of the graft, especially on the arterial end within the typically long-segment tortuous splenic artery stump. Most isolated arterial stump thrombi are not treated (Figs 8, 9). Some venous stump thrombi may propagate proximally and obstruct smaller vessels that drain portions of the pancreatic parenchyma, such as the inferior pancreaticoduodenal vein, which drains the pancreatic head (Figs 10 –12). In these instances, due in part to the lack of adequate collateral venous drainage, patients may present with pain over the graft because of venous congestion or with hyperglycemia due to graft dysfunction. These patients are treated with anticoagulants. Unfortunately, we have no good imaging or clinical predictors to help identify those patients in whom small venous stump thrombi will propagate; therefore, once a venous stump thrombus is identified, the patient is often required to undergo short-interval serial imaging and close clinical follow-up.
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Figure 8a. Arterial stump thrombosis. (a) Contrast-enhanced MR angiogram shows normal pancreatic graft enhancement. The venous anastomosis is to the right common iliac vein (not shown), and the pancreatic head is located inferiorly. (b) Contrast-enhanced MR angiogram shows a thrombus in the SMA stump (arrow). The thrombus is distal to any perforating arteries feeding the pancreatic transplant and did not require therapy.
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Figure 8b. Arterial stump thrombosis. (a) Contrast-enhanced MR angiogram shows normal pancreatic graft enhancement. The venous anastomosis is to the right common iliac vein (not shown), and the pancreatic head is located inferiorly. (b) Contrast-enhanced MR angiogram shows a thrombus in the SMA stump (arrow). The thrombus is distal to any perforating arteries feeding the pancreatic transplant and did not require therapy.
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Figure 9a. Arterial stump thrombus in a graft with SMV venous drainage. (a) Precontrast T1-weighted MR angiogram clearly depicts the arterial branches, with the SMA branch (arrowhead) supplying the superiorly positioned pancreatic head and the splenic artery branch (arrow) feeding the inferiorly positioned pancreatic tail. (b) Precontrast T1-weighted MR angiogram shows a high-signal-intensity thrombus (arrow) within the distal SMA stump in the right upper quadrant just inferior to the edge of the liver (arrowhead). High-signal-intensity clot secondary to methemoglobin can potentially mimic normal flow at contrast-enhanced MR angiography. Thus, both imaging technique and the interpretation of findings at precontrast MR angiography are important to avoid this potential pitfall of false-positive vessel patency (8).
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Figure 9b. Arterial stump thrombus in a graft with SMV venous drainage. (a) Precontrast T1-weighted MR angiogram clearly depicts the arterial branches, with the SMA branch (arrowhead) supplying the superiorly positioned pancreatic head and the splenic artery branch (arrow) feeding the inferiorly positioned pancreatic tail. (b) Precontrast T1-weighted MR angiogram shows a high-signal-intensity thrombus (arrow) within the distal SMA stump in the right upper quadrant just inferior to the edge of the liver (arrowhead). High-signal-intensity clot secondary to methemoglobin can potentially mimic normal flow at contrast-enhanced MR angiography. Thus, both imaging technique and the interpretation of findings at precontrast MR angiography are important to avoid this potential pitfall of false-positive vessel patency (8).
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Figure 10a. Splenic vein thrombosis. (a) Coronal 3D arterial phase MR angiogram shows the arterial anastomosis of the Y graft to the recipient right CIA. The donor SMA anastomosis is present superiorly in the pancreatic transplant, which is oriented with the head located superiorly and the tail inferiorly as the venous anastomosis is to the SMV. (b) Coronal 3D MR angiogram shows thrombosis of the donor splenic vein branch draining the tail of the pancreas (arrow). The tail was hypoperfused as a result of the splenic vein thrombosis. (c) Coronal oblique MR angiogram better delineates the long segment of thrombosis within the donor splenic vein (arrow).
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Figure 10b. Splenic vein thrombosis. (a) Coronal 3D arterial phase MR angiogram shows the arterial anastomosis of the Y graft to the recipient right CIA. The donor SMA anastomosis is present superiorly in the pancreatic transplant, which is oriented with the head located superiorly and the tail inferiorly as the venous anastomosis is to the SMV. (b) Coronal 3D MR angiogram shows thrombosis of the donor splenic vein branch draining the tail of the pancreas (arrow). The tail was hypoperfused as a result of the splenic vein thrombosis. (c) Coronal oblique MR angiogram better delineates the long segment of thrombosis within the donor splenic vein (arrow).
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Figure 10c. Splenic vein thrombosis. (a) Coronal 3D arterial phase MR angiogram shows the arterial anastomosis of the Y graft to the recipient right CIA. The donor SMA anastomosis is present superiorly in the pancreatic transplant, which is oriented with the head located superiorly and the tail inferiorly as the venous anastomosis is to the SMV. (b) Coronal 3D MR angiogram shows thrombosis of the donor splenic vein branch draining the tail of the pancreas (arrow). The tail was hypoperfused as a result of the splenic vein thrombosis. (c) Coronal oblique MR angiogram better delineates the long segment of thrombosis within the donor splenic vein (arrow).
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Figure 11a. Propagation of venous stump thrombus. (a) Coronal 3D venous phase MR angiogram shows a pancreatic graft with a venous anastomosis to the SMV (not shown). The SMV is thrombosed to the portosplenic confluence of the graft (arrow). (b) Routine axial two-dimensional postcontrast T1-weighted MR image shows a portion of a thrombosed arterial stump (arrow). Low-signal-intensity thrombus on T1-weighted images is often difficult to visualize on maximum-intensity-projection reformatted images.
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Figure 11b. Propagation of venous stump thrombus. (a) Coronal 3D venous phase MR angiogram shows a pancreatic graft with a venous anastomosis to the SMV (not shown). The SMV is thrombosed to the portosplenic confluence of the graft (arrow). (b) Routine axial two-dimensional postcontrast T1-weighted MR image shows a portion of a thrombosed arterial stump (arrow). Low-signal-intensity thrombus on T1-weighted images is often difficult to visualize on maximum-intensity-projection reformatted images.
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Figure 12. Consequences of complete venous thrombosis. Three-dimensional arterial phase MR angiogram shows lack of perfusion of a pancreatic transplant due to complete venous thrombosis extending to the anastomosis with the right common iliac vein (not shown). Secondary graft infarction required surgical removal (outlined). Note the duplicated left-sided IVC (arrow) and the left pelvic kidney transplant (arrowhead).
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Effects of Graft Rejection on the Transplant Vessels
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Acute graft rejection occurs in approximately 5% of pancreatic transplants (9). At pathologic analysis, rejection is described as an alloimmune arteritis that results in small vessel occlusion, which can in turn progress to proximal vessel occlusion. Inflammatory cell infiltration of the islet cells resulting in hyperglycemia is a late occurrence. No reliable biochemical markers have been identified that can help diagnose acute rejection. Graft edema and pancreatitis can be manifestations of both postoperative pancreatitis and rejection. The serum creatinine in simultaneous pancreas-kidney transplants is sometimes used as a surrogate marker for rejection. However, approximately 25% of patients with pancreatic graft rejection do not have rejection of the renal graft. Dynamic contrast-enhanced MR imaging has been used to correlate the degree of graft enhancement with the presence of rejection; however, although MR imaging enhancement below a 100% cutoff point at 1 minute was highly sensitive for acute rejection, it was only moderately specific (10). At our institution, patients are initially placed on a maximal immunosuppression regimen of four drugs, and if no treatable vascular thrombosis is identified at the time of MR imaging, they are usually followed up expectantly without biopsy. As a result, only minimal radiologic-pathologic correlation in this setting exists at our institution; therefore, imaging-based diagnosis of suspected acute rejection can only be surmised in the setting of serial follow-up examinations (Fig 13).
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Figure 13a. Suspected acute rejection in a patient who presented 6 days following transplantation with pain over the graft. (a) Initial coronal 3D MR angiogram shows a widely patent splenic artery branch of the donor pancreas. The venous anastomosis is to the right common iliac vein (not shown), and the pancreatic head is located inferiorly with the tail oriented more superiorly. Arrow indicates the arterial anastomosis of the Y graft to the donor splenic artery. The patient was treated expectantly, only to return 5 days later with persistent pain and an elevated serum glucose level. (b) Repeat coronal 3D MR angiogram demonstrates patency of all the vessels (donor splenic artery segment shown) but a dramatic decrease in the caliber of the arteries distal to the anastomosis, a finding that was thought to be due to acute rejection. No biopsy was performed. The patient was treated expectantly, with subsequent normalization of the serum glucose level and resolution of symptoms.
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Figure 13b. Suspected acute rejection in a patient who presented 6 days following transplantation with pain over the graft. (a) Initial coronal 3D MR angiogram shows a widely patent splenic artery branch of the donor pancreas. The venous anastomosis is to the right common iliac vein (not shown), and the pancreatic head is located inferiorly with the tail oriented more superiorly. Arrow indicates the arterial anastomosis of the Y graft to the donor splenic artery. The patient was treated expectantly, only to return 5 days later with persistent pain and an elevated serum glucose level. (b) Repeat coronal 3D MR angiogram demonstrates patency of all the vessels (donor splenic artery segment shown) but a dramatic decrease in the caliber of the arteries distal to the anastomosis, a finding that was thought to be due to acute rejection. No biopsy was performed. The patient was treated expectantly, with subsequent normalization of the serum glucose level and resolution of symptoms.
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Chronic rejection is believed to be the result of multiple undiagnosed or incompletely treated episodes of acute rejection, culminating in a small atrophic graft with decreased T1- and T2-weighted signal intensity secondary to fibrosis and diminutive feeding vessels, but normal enhancement.
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MR Imaging Artifacts
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MR imaging artifacts can lead to misinterpretation of imaging findings. False-positive interpretations of arterial and venous anastomotic narrowing can occur due to the presence of susceptibility artifact from anastomotic surgical clips (Fig 14). Susceptibility artifacts are accentuated with gradient-echo sequences that lack 180° refocusing pulses. The longer the echo time of the gradient-echo sequence, the greater the degree of loss of T2* signal. Fortunately, 3D MR angiography has a shorter echo time (range, 0.4–1.4 msec) compared with the routine two-dimensional sequences, thus minimizing potential signal loss from clips and allowing differentiation between true stenoses and signal loss due to susceptibility artifact.
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Figure 14. Susceptibility artifact mimicking stenosis. Coronal 3D MR angiogram shows loss of signal near the bifurcation of the arterial Y graft. This signal loss is due to susceptibility artifact from an adjacent surgical clip and not to any pathologic condition at the anastomosis.
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Conclusions
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Coronal 3D contrast-enhanced MR angiography is a safe and effective method of assessing the arterial and venous anatomy of pancreatic transplants. Understanding the complex vascular anatomy is essential to properly performing and interpreting the study. For example, knowledge of the pancreatic venous drainage (via the SMV, IVC or iliac vein) aids in the positioning of the 3D volume to include only the relevant anatomy and optimize the temporal and spatial resolution. Our experience with imaging-based diagnosis of acute rejection is limited by practice patterns at our institution. However, stump thromboses, either arterial or venous, are a commonly observed vascular complication in our practice. Arterial stump thromboses usually occur distal to arterioles that supply the pancreatic parenchyma and thus are thought to be clinically insignificant. Peripheral venous stump thrombi do not compromise graft function unless they propagate centrally to involve proximal segments of the pancreatic transplant veins (SMV, splenic vein, portal vein) and compromise parenchymal venous drainage. Because of the inability to predict the outcome of small venous stump thrombi, the clinical decision is often made to perform serial imaging, regardless of whether anticoagulation therapy is initiated.
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Footnotes
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2 Current address: Mecklenburg Radiology Associates, Charlotte, NC. 
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References
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Abstract
Introduction
