AJR 2005; 184:465-473
© American Roentgen Ray Society
Contrast-Enhanced MR Angiography After Pancreas Transplantation: Normal Appearance and Vascular Complications
Klaus D. Hagspiel1,
Kiran Nandalur1,
Brian Burkholder1,
J. Fritz Angle1,
Kenneth L. Brayman2,
David J. Spinosa1,
Alan H. Matsumoto1,
Olivia L. Veldhuis1,
Hilary Sanfey2,
Robert G. Sawyer2,
Timothy L. Pruett2 and
Daniel A. Leung1
1 Department of Radiology, University of Virginia Health System, 1215 Lee St.,
PO Box 800170, Charlottesville, VA 22908.
2 Department of Surgery, University of Virginia Health System, Charlottesville,
VA 22908.
Received March 25, 2004;
accepted after revision July 22, 2004.
Address correspondence to K. D. Hagspiel.
Introduction
Pancreatic transplantation is increasingly used for the treatment of type 1
diabetes mellitus [1]. It
commonly is performed in conjunction with kidney transplantation. The original
procedure is the systemic bladder drainage type, which consists of
intraperitoneal placement of the whole pancreas into the pelvis and
anastomosis of the transplanted splenic and superior mesenteric arteries to
the recipient's iliac arteries via a Y-graft formed from the donor's common,
internal, and external iliac arteries. Pancreatic venous outflow with this
type of graft is into the iliac veins and therefore the systemic circulation
(Figs. 1 and
2A,
2B,
2C). Drainage of the exocrine
secretions is into the urinary bladder using an interposition duodenal
segment. This technique has a number of drawbacks: namely, the development of
peripheral hyperinsulinemia due to venous drainage of the insulin into the
systemic circulation rather than the portal vein. This condition has been
found to accelerate the development of insulin resistance and possibly
atherosclerosis. In addition, urinary tract infections and graft pancreatitis
occur as complications of the drainage of the exocrine secretions into the
urinary bladder, necessitating conversion from bladder to enteric drainage in
a substantial number of patients. These drawbacks led to the development of a
modified form of pancreatic transplantation, commonly referred to as portal
enterically drained pancreas transplant. As in the systemic bladder drainage
technique, the pancreatic allograft is placed intraperitoneally, but higher in
the recipient's abdomen. The allograft is harvested with its two supplying
arteries, the splenic and superior mesenteric arteries, which are anastomosed
to the iliac arteries as well, but, because of the higher position in the
abdomen, via a much longer Y-graft. Pancreatic venous outflow is achieved by
anastomosing the transplanted portal vein with the recipient's superior
mesenteric vein (Figs. 3,
4A,
4B,
4C,
5A,
5B). In this operation, the
exocrine pancreatic secretions are drained into a small-bowel loop. Although
the results with the portal enterically drained allografts are superior to the
standard operation, postoperative pancreatic transplantation dysfunction still
occurs not infrequently [2].
The most common causes of dysfunction are rejection, followed by ischemia due
to graft thrombosis, pancreatitis, and sepsis
[2,
3]. Sonography is typically the
primary technique used to evaluate patients with graft dysfunction. However,
detailed assessment of the complex vasculature of pancreatic allografts can be
difficult and sometimes impossible with sonography. Because MR contrast agents
are only minimally nephrotoxic, the use of 3D contrast-enhanced MR angiography
has been explored in this setting and occasionally preoperatively for the
assessment of the pelvic arteries, and the successful use of this technique
for the evaluation of these patients has been reported in several small series
and case reports
[4–8].
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Fig. 1. —Normal vascular anatomy in systemic bladder drainage
procedure. Allograft can be oriented either head up or down. Splenic (SPLA)
and superior mesenteric (SMA) arteries are anastomosed to external or common
iliac recipient's artery via a Y-graft. Venous drainage of pancreas is via
splenic (SPLV) and superior mesenteric veins (SMV), distal ends of which are
ligated. Donor portal vein (PV) is then anastomosed to common or external
iliac vein of recipient. Drainage of exocrine secretions is into urinary
bladder using interposition duodenal segment. IVC = inferior vena cava, AO =
aorta.
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Fig. 2A. —Normal MR angiography results in 50-year-old man 4 days after
pancreas–kidney transplantation using systemic bladder drainage
technique. Clinically, no indications for pancreatic dysfunction were seen,
and on clinical follow-up pancreatic function remained normal.
Maximum-intensity-projection image shows pancreas and kidney transplants in
right and left hemipelvis, respectively. Note irregular lower pole of kidney
transplant due to infarcts (arrow).
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Fig. 2B. —Normal MR angiography results in 50-year-old man 4 days after
pancreas–kidney transplantation using systemic bladder drainage
technique. Clinically, no indications for pancreatic dysfunction were seen,
and on clinical follow-up pancreatic function remained normal. Subvolume
maximum-intensity-projection image shows allograft with pancreatic head
pointing caudally. Splenic (small arrow) and superior mesenteric
(arrowhead) arteries are anastomosed to external iliac artery via
Y-graft (large arrow).
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Fig. 2C. —Normal MR angiography results in 50-year-old man 4 days after
pancreas–kidney transplantation using systemic bladder drainage
technique. Clinically, no indications for pancreatic dysfunction were seen,
and on clinical follow-up pancreatic function remained normal. Subvolume
thick-slab multiplanar reconstruction shows venous drainage of allograft.
Splenic (long thin arrow) and superior mesenteric (short thin
arrow) veins join to form portal vein (thick arrow), which is
anastomosed to recipient's iliac vein (hidden behind iliac artery). Stenosis
of splenic vein immediately before its confluence with superior mesenteric
vein (arrowhead) is artifactual because of incomplete inclusion of
this vessel in reconstruction subvolume.
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Fig. 3. —Normal vascular anatomy in portal enterically drained
allograft. Allograft is typically oriented with pancreatic head up. Splenic
(SPLA) and superior mesenteric (SMA) arteries are anastomosed to recipient's
external or common iliac artery via a Y-graft, which is usually extended using
a second graft. Venous drainage of allograft is also via splenic (SPLV) and
superior mesenteric (SMV) veins, distal ends of which are ligated. Donor
portal vein (PV) is then anastomosed to recipient's superior mesenteric vein.
Drainage of exocrine pancreatic secretions is into small-bowel loop. SPV =
splenic vein, AO = aorta, CIA = common iliac artery, RA = renal artery, EIA =
external iliac artery, IIA = internal iliac artery.
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Fig. 4A. —47-year-old man undergoing MR angiography 4 days after portal
enterically drained transplant because of hyperglycemia. MR angiography
results were completely normal and allograft completely recovered function.
Hyperglycemia was considered to be caused by steroid medication. Coronal
maximum-intensity-projection image shows allograft is oriented with pancreatic
head up. Splenic (long arrow) and superior mesenteric (short
arrow) arteries are anastomosed to external and internal iliac arteries
of Y-graft. Donor's common iliac donor artery is then anastomosed to
recipient's common iliac artery.
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Fig. 4B. —47-year-old man undergoing MR angiography 4 days after portal
enterically drained transplant because of hyperglycemia. MR angiography
results were completely normal and allograft completely recovered function.
Hyperglycemia was considered to be caused by steroid medication. Subvolume
maximum-intensity-projection image in different oblique coronal orientation
allows display of arterial anatomy in better detail.
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Fig. 4C. —47-year-old man undergoing MR angiography 4 days after portal
enterically drained transplant because of hyperglycemia. MR angiography
results were completely normal and allograft completely recovered function.
Hyperglycemia was considered to be caused by steroid medication. Venous
drainage of allograft is via splenic (large arrow) and superior
mesenteric (arrowhead) veins, which drain into donor's portal vein,
which in turn is anastomosed to recipient's superior mesenteric vein
(small arrow).
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Fig. 5A. —51-year-old man who underwent MR angiography because of
urinary tract infection with increase in serum amylase and lipase 14 years
after receiving portal enterically drained transplant. MR angiography showed
completely normal findings. Hyperamylasemia and hyperlipasemia were considered
to be due to subclinical pancreatitis in setting of infection. Laboratory
abnormalities normalized after antibiotic treatment. Coronal subvolume
maximum-intensity-projection image shows allograft is oriented with pancreatic
head up to left of aorta. Splenic (arrowhead) and superior mesenteric
(arrow) arteries are anastomosed to recipient's infrarenal aorta via
very short Y-graft.
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Fig. 5B. —51-year-old man who underwent MR angiography because of
urinary tract infection with increase in serum amylase and lipase 14 years
after receiving portal enterically drained transplant. MR angiography showed
completely normal findings. Hyperamylasemia and hyperlipasemia were considered
to be due to subclinical pancreatitis in setting of infection. Laboratory
abnormalities normalized after antibiotic treatment. Venous drainage of
allograft is via splenic (thin arrow) and superior mesenteric
(arrowhead) veins, which drain into donor's portal vein (long
thick arrow). Portal vein is anastomosed to recipient's splenic vein
(short thick arrow).
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To our knowledge, this pictorial essay is the first comprehensive review of
its kind detailing the normal appearance of the two types of pancreatic
transplant and the appearance of the major vascular complications that can be
encountered in this patient population using state-of-the-art high-resolution
3D contrast-enhanced MR angiography.
MR Technique
All pancreatic MR examinations at our institution are performed on a
high-performance 1.5-T system with a 40 mT/m gradient system (Sonata, Siemens
Medical Solutions) and a minimum rise time of 200 µsec. A
4-element phased-array body coil is routinely used. MRI includes axial
T1-weighted fast low-angle shot sequences, axial T2-weighted turbo spin-echo
sequences with fat suppression, and axial T1-weighted 3D volumetric
interpolated breath-hold examination using unenhanced and gadolinium-enhanced
sequences with fat suppression. Three-dimensional contrast-enhanced MR
angiography is performed in the coronal orientation using a 3D fast low-angle
shot sequence with the following parameters: TR/TE, 3.3/1.2; flip angle,
25°; bandwidth, 390 Hz/pixel; matrix, 211 x 512; and a 6/8
rectangular field of view with a maximum dimension of 400 mm. The resulting
voxel size is 0.8 x 1.3 x 1.3–1.8 mm with 55% phase
resolution. Scanning duration is 24 sec. Forty milliliters of gadodiamide
(Omniscan, Amersham Health) is injected at a rate of 2.0 mL/sec with a power
injector (Spectris, Medrad). A timing bolus technique is used to determine
optimal scanning delay, and at least two acquisitions are performed with an
interscan delay of 10 sec to depict both arterial and venous enhancement
phases. All examinations are acquired in breath-hold and with subtraction
technique: for example, an unenhanced mask MR angiography acquisition is
subtracted from the arterial or venous phase. Three-dimensional
reconstructions are performed on dedicated 3D workstations.
Normal Pancreatic Transplants
Systemic Bladder Drainage Allografts
The normal appearance of a systemic bladder drainage allograft is shown in
Figures 1 and
2A,
2B,
2C. The allograft shows
homogeneous enhancement throughout the whole gland on both the MR angiography
source images and on delayed contrast-enhanced T1-weighted images
[3].
Portal Enterically Drained Allografts
The normal appearance of a portal enterically drained allograft is shown in
Figures 3,
4A,
4B,
4C,
5A,
5B.
Vascular Complications
Vascular Thrombosis
Vascular thrombosis is the second most common cause of pancreatic
transplant dysfunction after graft rejection, with a reported incidence of
2–19% [4]. Both arterial
and venous thrombosis can occur and, if not detected early, typically lead to
transplant pancreatectomy because of pancreatic infarction or pancreatitis
[4]. The typical appearance of
acute thrombosis on contrast-enhanced MR angiography is that of a very dark
hypointense filling defect occluding the arterial lumen, with or without a
trailing edge [5]. Venous
thrombosis is frequently the cause of early postoperative graft failure,
presumably as a result of the decreased flow in the allograft.
Figure 6 shows a patient with
acute and complete occlusion of the transplant artery Y-graft due to
thrombosis of the common iliac artery resulting in infarction of the pancreas
and necessitating removal of the gland. Figure
7A,
7B,
7C,
7D,
7E,
7F illustrates an example with
occlusion of the allograft superior mesenteric artery and preserved patency of
the splenic artery. Patency of only one allograft artery is sufficient to
supply adequate perfusion to the entire gland
[6]. This patient also had
complete thrombosis of the allograft portal vein and the allograft superior
mesenteric and splenic veins.
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Fig. 6. —Acute occlusion of recipient's common iliac artery due to
surgical clamp injury in 39-year-old woman with preexisting atherosclerotic
disease, which led to complete thrombosis and infarction of allograft 2 days
after systemic bladder drainage type of transplantation.
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Fig. 7A. —MR angiography 28 days after transplantation in 34-year-old
male recipient with arterial thrombosis resulting in complete occlusion of
limb of Y-graft supplying superior mesenteric artery and transplant superior
mesenteric artery with preserved patency of splenic artery. Note concurrent
complete venous thrombosis of allograft portal vein and allograft superior
mesenteric (SMV) and splenic veins. Note also inhomogeneous enhancement of
pancreatic tissue. Oblique maximum-intensity-projection image shows pancreatic
Y-graft (arrow) and allograft renal arteries
(arrowhead).
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Fig. 7B. —MR angiography 28 days after transplantation in 34-year-old
male recipient with arterial thrombosis resulting in complete occlusion of
limb of Y-graft supplying superior mesenteric artery and transplant superior
mesenteric artery with preserved patency of splenic artery. Note concurrent
complete venous thrombosis of allograft portal vein and allograft superior
mesenteric (SMV) and splenic veins. Note also inhomogeneous enhancement of
pancreatic tissue. Subvolume maximum-intensity-projection image (B) and
confirmatory selective pancreatic arteriogram (C) show that only one
limb of Y-graft is patent (arrow, B).
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Fig. 7C. —MR angiography 28 days after transplantation in 34-year-old
male recipient with arterial thrombosis resulting in complete occlusion of
limb of Y-graft supplying superior mesenteric artery and transplant superior
mesenteric artery with preserved patency of splenic artery. Note concurrent
complete venous thrombosis of allograft portal vein and allograft superior
mesenteric (SMV) and splenic veins. Note also inhomogeneous enhancement of
pancreatic tissue. Subvolume maximum-intensity-projection image (B) and
confirmatory selective pancreatic arteriogram (C) show that only one
limb of Y-graft is patent (arrow, B).
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Fig. 7D. —MR angiography 28 days after transplantation in 34-year-old
male recipient with arterial thrombosis. Source image from venous phase shows
hypointense filling defects consistent with venous thrombus of allograft
splenic (arrow) and portal (arrowhead) veins.
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Fig. 7E. —MR angiography 28 days after transplantation in 34-year-old
male recipient with arterial thrombosis. Subvolume
maximum-intensity-projection image of venous phase shows absent allograft
veins. Small portion of allograft SMV (arrowhead) is contrast-filled.
Recipient's SMV (arrow) is patent.
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Fig. 7F. —MR angiography 28 days after transplantation in 34-year-old
male recipient with arterial thrombosis. Confirmatory delayed venous phase of
pancreatic arteriogram also shows absent allograft veins and small segment of
SMV that was seen on MR venography (arrowhead). Abundant small venous
collaterals are seen surrounding allograft, which filled recipient's SMV. That
vein was faintly visualized on a later frame (not shown).
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Vascular Stenoses and Kinks
All anastomoses can develop stenoses, which are readily detected by
contrast-enhanced MR angiography
[8]. In addition, portal
enterically drained grafts are prone to kinking of the Y-graft due to the
length of this vessel (Fig.
8A,
8B,
8C,
8D,
8E,
8F,
8G). Invasive pressure
measurements can be needed to determine the hemodynamic relevance of these
kinks and stenoses, and they can be treated endovascularly with percutaneous
transluminal angioplasty or stent placement
[7].
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Fig. 8A. —30-year-old woman with portal enterically drained type of
allograft presenting with hyperglycemia. Sonography on sixth postoperative day
failed to visualize pancreas because of bowel gas. MR angiography performed on
seventh postoperative day shows 90% stenosis caused by kink in Y-graft, and
partial obstruction of distal superior mesenteric artery (SMA) due to
thrombus. Follow-up MR angiography on 31st postoperative day shows
patency of Y-graft after successful angioplasty and spontaneous recanalization
of SMA. Coronal maximum-intensity-projection image shows abdominal aorta and
portal enterically drained allograft.
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Fig. 8B. —30-year-old woman with portal enterically drained type of
allograft presenting with hyperglycemia. Sonography on sixth postoperative day
failed to visualize pancreas because of bowel gas. MR angiography performed on
seventh postoperative day shows 90% stenosis caused by kink in Y-graft, and
partial obstruction of distal superior mesenteric artery (SMA) due to
thrombus. Follow-up MR angiography on 31st postoperative day shows
patency of Y-graft after successful angioplasty and spontaneous recanalization
of SMA. Subvolume maximum-intensity-projection image shows high-grade stenosis
caused by kink in Y-graft and abrupt occlusion of SMA
(arrowhead).
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Fig. 8C. —30-year-old woman with portal enterically drained type of
allograft presenting with hyperglycemia. Sonography on sixth postoperative day
failed to visualize pancreas because of bowel gas. MR angiography performed on
seventh postoperative day shows 90% stenosis caused by kink in Y-graft, and
partial obstruction of distal superior mesenteric artery (SMA) due to
thrombus. Follow-up MR angiography on 31st postoperative day shows
patency of Y-graft after successful angioplasty and spontaneous recanalization
of SMA. Catheter angiogram confirms MR angiography findings. Patient
subsequently underwent successful percutaneous transluminal angioplasty.
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Fig. 8D. —30-year-old woman with portal enterically drained type of
allograft presenting with hyperglycemia. Sonography on sixth postoperative day
failed to visualize pancreas because of bowel gas. MR angiography performed on
seventh postoperative day shows 90% stenosis caused by kink in Y-graft, and
partial obstruction of distal superior mesenteric artery (SMA) due to
thrombus. Follow-up MR angiography on 31st postoperative day shows
patency of Y-graft after successful angioplasty and spontaneous recanalization
of SMA. Venous phase maximum-intensity-projection image shows patent venous
anatomy with splenic (short arrow) and superior mesenteric
(arrowhead) veins of allograft forming portal vein (medium
arrow), which is anastomosed to recipient's superior mesenteric vein
(long arrow).
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Fig. 8E. —30-year-old woman with portal enterically drained type of
allograft presenting with hyperglycemia. Sonography on sixth postoperative day
failed to visualize pancreas because of bowel gas. MR angiography performed on
seventh postoperative day shows 90% stenosis caused by kink in Y-graft, and
partial obstruction of distal superior mesenteric artery (SMA) due to
thrombus. Follow-up MR angiography on 31st postoperative day shows
patency of Y-graft after successful angioplasty and spontaneous recanalization
of SMA. Venous phase of selective pancreatic arteriogram confirms patency of
allograft veins and recipient's superior mesenteric vein.
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Fig. 8F. —30-year-old woman with portal enterically drained type of
allograft presenting with hyperglycemia. Coronal maximum-intensity-projection
image from follow-up MR angiography performed on 31st postoperative day shows
patent allograph vessel.
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Fig. 8G. —30-year-old woman with portal enterically drained type of
allograft presenting with hyperglycemia. Subvolume
maximum-intensity-projection image from same study as in F shows
patency of Y-graft without significant residual stenosis after angioplasty and
spontaneous recanalization of previously distally occluded SMA
(arrowhead). Note visualization of first- and second-order allograft
arterial branches (arrow), which shows the excellent spatial
resolution of this technique.
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Other Vascular Complications and Transplant Rejection
Other vascular complications include inflow vessel occlusion due to
surgical clamp injuries or preexisting atherosclerotic disease
[7]
(Fig. 6).
Pseudoaneurysms and arterial venous fistulas occur occasionally. They can
be related to the procurement technique of the allograft, namely, the blind
ligation of mesenteric vessels along the inferior border of the pancreas
[6]. More frequently they are
mycotic pseudoaneurysms in the setting of graft infection (Fig.
9A,
9B,
9C). Both surgical and
endovascular treatments have been successfully performed for a number of these
complications [6].
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Fig. 9A. —Pseudoaneurysm and arteriovenous fistula in 47-year-old man
with systemic bladder drainage type of transplant 67 days after surgery.
Diagnosis was made on day 66 on CT. Attempt was made to embolize fistula and
aneurysm but was ultimately unsuccessful despite use of multiple coils and
detachable balloons. Surgical pancreatectomy was performed. Pathologic
evaluation of explanted pancreas showed these to be pseudoaneurysms caused by
vancomycin-resistant enterococci. Subvolume coronal
maximum-intensity-projection image shows right systemic bladder drainage
allograft with large pseudoaneurysms. Proximal Y-graft (arrowhead)
can be seen originating from external iliac artery (thick arrow).
Arteriovenous fistula (small thin arrow) off Y-graft can also be
seen. Note enlarged external iliac vein (long thin arrow) that
occludes at level of aneurysms.
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Fig. 9B. —Pseudoaneurysm and arteriovenous fistula in 47-year-old man
with systemic bladder drainage type of transplant 67 days after surgery.
Diagnosis was made on day 66 on CT. Attempt was made to embolize fistula and
aneurysm but was ultimately unsuccessful despite use of multiple coils and
detachable balloons. Surgical pancreatectomy was performed. Pathologic
evaluation of explanted pancreas showed these to be pseudoaneurysms caused by
vancomycin-resistant enterococci. Catheter angiogram of right hemipelvis shows
Y-graft (arrowhead) and defect in graft causing arteriovenous fistula
(arrow) that supplies pseudoaneurysms.
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Fig. 9C. —Pseudoaneurysm and arteriovenous fistula in 47-year-old man
with systemic bladder drainage type of transplant 67 days after surgery.
Diagnosis was made on day 66 on CT. Attempt was made to embolize fistula and
aneurysm but was ultimately unsuccessful despite use of multiple coils and
detachable balloons. Surgical pancreatectomy was performed. Pathologic
evaluation of explanted pancreas showed these to be pseudoaneurysms caused by
vancomycin-resistant enterococci. Multiplanar reconstruction perpendicular
through Y-graft (lower arrow) shows fistula connecting it to
pseudoaneurysm (upper arrow).
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The most frequent complication is acute graft rejection. MR angiography
shows normal vessels but an inhomogeneously enhancing gland with patent
vessels. The degree of parenchymal enhancement compared with normal glands is
decreased [3] (Fig.
10A,
10B).
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Fig. 10A. —50-year-old man 40 days after transplantation presenting with
hyperglycemia (same patient as in Fig.
2A,
2B,
2C). MR angiography findings
were normal, but evaluation of parenchyma showed allograft to be enlarged with
inhomogeneous and decreased enhancement. This is typical finding in acute
rejection. Immunosuppressive treatment was instituted, and pancreas function
became completely normal. Three-dimensional volumetric interpolated
breath-hold examination image obtained after MR angiography examination shows
enlarged and inhomogeneously enhancing pancreas (arrow).
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Fig. 10B. —50-year-old man 40 days after transplantation presenting with
hyperglycemia (same patient as in Fig.
2A,
2B,
2C). MR angiography findings
were normal, but evaluation of parenchyma showed allograft to be enlarged with
inhomogeneous and decreased enhancement. This is typical finding in acute
rejection. Immunosuppressive treatment was instituted, and pancreas function
became completely normal. Two-dimensional fast low-angle shot image with fat
suppression obtained after MR angiography 36 days earlier shows normal-sized
and homogeneously enhancing allograft.
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Occasionally, patients require removal of the allograft for various
reasons. A small stump of the ligated Y-graft can occasionally be seen
(Fig. 11).
Summary
In patients with suspected vascular compromise to the transplanted
pancreas, state-of-the-art high-resolution 3D contrast-enhanced MR angiography
is an extraordinarily accurate diagnostic technique that should be routinely
used if sonography, which is less expensive and more readily available, fails
to provide the needed diagnostic information. Three-dimensional
contrast-enhanced MR angiography allows the delineation of the normal venous
and arterial anatomy of pancreatic allografts and shows the appearance of the
major vascular complications.
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Introduction
Normal Pancreatic Transplants
