Downloaded from www.ajronline.org by 117.253.182.228 on 10/27/15 from IP address 117.253.182.228. Copyright ARRS. For personal use only; all rights reserved
13
Progress
Pancreas Robert
A. Low,1
Transplant Christopher
Imaging:
diabetics
than 50% of type I diabetics have or neuropathy within 20 years of [1 ]. Pancreatic transplantation is
undertaken in selected patients in an attempt to prevent, arrest, or reverse progression of these complications [1 , 2]. The first human pancreas transplantation was performed in 1966. Through June 1989, 2004 pancreas transplantations have been reported at 128 institutions [3]. Improved surgical techniques combined with increasingly efficacious immunosuppression have led to continuous improvement in function of pancreatic grafts and survival rates of patients. For the 3year period 1 986 through 1 988, 1 -year graft function and recipent survival rates were 54% and 87%, respectively [4, 5]. Surgical techniques in pancreatic allografting have evolved considerably [1 , 2, 6]. All live donor grafts are necessarily segmental (Fig. 1). A whole or segmental graft may be obtamed from a cadaver (Figs. 1-3). Whole pancreas transplantation is preferred over segmental transplantation because of the theoretically lower risk of thrombosis in whole grafts, which have a higher blood flow, and because of the larger beta-cell mass available [1]. Revascularization of the pancreatic graft usually is accomplished through anastomoses with the iliac vessels (Figs. 13). However, revascularization of the graft is occasionally done with anastomoses made to the recipient splenic or inferior mesenteric vessels, permitting the venous effluent to drain
into the portal venous with these
has been shown
system; no metabolic variations [1].
advantage
Received November 17, 1989; accepted after revision February ‘All authors: Department of Radiology, University of Minnesota reprintrequests to J. G. Letoumeau. AJR 155:13-21,
An Overview
C. Kuni, and Janis Gissel Letourneau
There are more than one million insulin-dependent in the United States. More retinopathy, nephropathy, the onset of the disease
in Radiology
July 1990 036i-803X/90/i551-00i3
© American
Numerous techniques have been used to manage exocrine secretions in pancreas transplants, including duct ligation and free intraperitoneal drainage. These methods generally have been abandoned, as have synthetic polymer ductal injection and exocrine drainage to recipient ureter and stomach. Both segmental and whole pancreas grafts typically are drained to either small bowel (Fig. 1) or bladder (Figs. 2 and 3); bladder drainage is now the preferred technique [1 , 4, 5]. Bladder
exocrine drainage appears to minimize leaks and facilitates urinary monitoring of pancreatic exocrine function. Complications of pancreatic transplantation are common and are associated with a substantial risk of patient morbidity or mortality [2]; the clinical setting is often nonspecific and it is not uncommon
i4, i990. Hospital and Clinic, Roentgen
for there
to be coexisting
complications.
Rejection is the most common cause of endocrine failure, occurring in up to 35% of pancreas transplants [1 , 2]. Pancreatic or peripancreatic abscess is a life-threatening problem, often requiring transplant pancreatectomy, and is seen in 822% of recipients [2, 4]. Thrombosis leads to graft failure in 12% of pancreas grafts [4]. Other complications include pancreatitis and fluid collections such as hematomas, lymphoceles, urinomas, pseudocysts, diffuse pancreatic ascites, and leaks at the exocrine anastomoses. Posttransplantation complications are most easily considered in terms of three categories related to diagnostic imaging: parenchymal abnormalities, pancreatic or peripancreatic fluid, and vascular complications. The goal of imaging of the transplanted pancreas is to characterize complications and to guide percutaneous aspi-
Box 292 UMHC,
Ray Society
420 Delaware
St. SE., Minneapolis, MN
55455.
Address
Downloaded from www.ajronline.org by 117.253.182.228 on 10/27/15 from IP address 117.253.182.228. Copyright ARRS. For personal use only; all rights reserved
14
LOW
Fig. 1.-Drawing shows technique of segmental pancreas graft transplantation. Pancreatic segment is obtained from live donor or cadaveric donor from whom liver is also harvested. Pancreas is divided at level of donor portal vein. Body and tail of graft are harvested with splenic artery and vein, which are anastomosed to recipient iliac vessels (arrows). Cut end of graft is intussuscepted into Roux-en-Y limb of recipient jejunum. Pancreatic stent is placed in the duct and eventually will pass through the intestine.
Techniques
transplants
studies and because frequently is needed.
DTPA are administered
distension,
present
or
because study Twenty
it can be used for perfusion of coexisting renal transplants millicuries (740 MBq) of mTc-
IV, and 16 serial 2-sec
images
are
followed by an immediate 500,000-count static image. Image variables examined are (1) time delay from peak iliac arterial to peak pancreatic activity; (2) relative intensities of arterial and pancreatic peak activity on perfusion and static images; and (3) changes in size, homogeneity, and definition of the pancreas over serial studies. Sonography is used frequently for noninvasive imaging of pancreas transplants when fever, abdominal pain, abdominal
laboratory
is performed. the sonographic
evidence
of graft
and transverse
dysfunction
is
sonography
of
Distension of the urinary examination by elevating
loops out of the pelvis and distending
the donor
bladder bowel
duodenal
if one was used. Visualization of the graft may be when enteric drainage has been used, as bowel loops
often completely can be used to differenallografts. 00mTc-sulfur 99mTc..DTPA have some other pathologic changes used frequently to study
July 1990
Fig. 3.-Drawing shows whole pancreas graft from cadaveric liver donor. Small patch of aorta containing superior mesenteric artery is anastomosed to recipient iliac artery. Donor splenic artery is anastomosed to donor superior mesenteric artery (open arrow). Gastroduodenal artery is ligated at its origin. Portal vein is eectioned just beyond termination of splenic vein. Segment of donor iliac vein is anastomosed to donor portal vein stump (solid arrow) to provide venous conduit of sufficient length for anastomosis to recipient iliac vein. Whole segment of donor duodenum is anastomosed to bladder.
[2, 1 1]. Longitudinal
the graft facilitates stump, difficult
Several scintigraphic techniques tiate normal from abnormal pancreas colloid, 1ln-labeled platelets, and value in differentiating rejection from in the graft [7-10]. 99mTc-DTPA is
pancreas
AJA:i55,
Fig. 2.-Drawing shows whole pancreas graft from cadaveric nonliver donor. Carrel aortic patch (straight arrow), including origins of celiac axis and superior mesenteric artery, is anastomosed to recipient iliac artery; native pancreatic arterial supply is left intact. Portal vein (curved arrows) drains to recipient iliac vein. Patch of donor duodenum is anastomosed to bladder.
ration or drainage of associated fluid collections. Nuclear medicine, sonography, CT, MR imaging, and angiography have been used to evaluate posttransplant complications. In this review, we summarize the often complementary capabilities of these imaging techniques.
Imaging
ET AL.
surround
the graft. The peripancreatic
region
and the remainder of the pelvis and abdomen are examined to detect the presence of free or loculated fluid. Sonography of pancreas transplants should include DoppIer evaluation of the graft vasculature. Arterial and venous
Doppler signals are obtained throughout the length of the extraparenchymal vascular pedicle and within the pancreatic parenchyma. Knowledge of the vascular reconstruction of a given graft and the use of color Doppler technology facilitates this portion of the examination. Abdominal and pelvic CT, used primarily to detect fluid collections, is done with complete intestinal opacification, which aids in separating graft parenchyma or fluid collections from adjacent bowel loops [11-14]. IV contrast material is administered infrequently, to avoid the risk of nephrotoxicity, if native renal function is impaired or if there is a coexisting renal transplant. Rescanning the pelvis with retrograde bladder or rectal contrast material may aid in differentiating graft
Downloaded from www.ajronline.org by 117.253.182.228 on 10/27/15 from IP address 117.253.182.228. Copyright ARRS. For personal use only; all rights reserved
AJA:155,
PANCREAS
July i990
TRANSPLANT
Fig. 4.-Scintigrams of normally functioning transplant. A, Dynamic-phase scintigrams are taken every 2 sec. Pancreatic radioactivity equal. B, Static scintigram. Pancreas is homogeneous and well marginated (arrows).
15
IMAGING
peak
(arrow)
occurs
2 sec after
arterial
peak
and peak
or fluid from adjacent bowel and bladder and in detecting an exocrine leak. MR imaging of pancreas allografts generally is performed in the coronal plane, permitting simultaneous long-axis imaging of the renal transplant, if present. Ti and T2-weighted spin-echo (SE) images are obtained with a 5-mm slice thickness. Supplemental Ti -weighted axial scans may aid in localizing the graft. Respiratory gating of the sequences is usually not necessary because of the low pelvic location of most pancreas transplants. To date, no systematic evaluation of variable flip-angle or other pulse sequences in pancreas transplants has been reported. Angiography is used primarily to confirm or clarify suspected vascular thrombosis, anastomotic stricture, or pseudoaneurysm detected by other imaging techniques [9, 15-
is characterized by a delay of the peak pancreatic than 4 sec from the arterial peak and by equal
18]. Both intraarterial
homogeneous
medium
muscle
5).
-
and IV digital
subtraction
techniques
can be used to evaluate graft vasculature. Conventional transfemoral angiography can be performed either from contralateral or ipsilateral approaches. Conventional angiography with a balloon-occlusioncatheter is currently the preferred technique for evaluation of pancreas transplants at our institution; this technique minimizes contrast dose to the patient and maximizes opacification of the pancreas transplant vasculature.
pancreatic function
Transplant
Imaging
(Fig. 4); however,
reported
when
activity arterial
clinically
no perfusion
are
less and
normal
is detectable
scintigraphically [9]. A normally functioning, complication-free transplant is suggested by serial studies that show constant peak timing geneity.
and peak
intensity,
The early posttransplantation
pancreatic
size,
appearance
and homo-
of the graft on
sonography, CT, and MR does not correlate well with endocrine function [9, 13, 14, i 7, 19-22], presumably because of the effects of preservation injury and the trauma of surgical handling. Graft appearance normalizes within several weeks
after transplantation, tion is stabilized, (Fig.
asymptomatic
if no complications sonographically
intervene.
normal
level of echogenicity
Although
experience
Once func-
parenchyma
has a
similar to that of is limited
because
recipients
ance of the normal
are studied rarely, the CT appeartransplant has been described as homo-
geneous and well marginated, with a density similar to that of native pancreas (Fig. 6) [1 3, 14]. Parenchymal signal intensity similar to that of normal renal cortex and greater than that of muscle on Ti -weighted images, and similar to that of fat but less than that of urine on T2-weighted images, is seen on MR of uncomplicated allografts (Fig. 7A) [9, i 7, 22]. The
pancreatic Pancreas
peak intensities has been
intensities
duct is typically
eter and frequently
5C). Both injections
no greater
is demonstrable
of polymer
than 2-3 mm in diam-
only sonographically
and stents
within
Normal Appearance
creatic staples
Isolated 9smTcDTPA studies are less accurate in evaluating pancreas transplants than are serial studies. A normal study
duodenocystostomy may be seen on sonography metallic artifacts may be seen on MR.
(Fig.
the pan-
duct are detectable with sonography and CT. Surgical at the ligated ends of the donor duodenum and at the
and CT and
Downloaded from www.ajronline.org by 117.253.182.228 on 10/27/15 from IP address 117.253.182.228. Copyright ARRS. For personal use only; all rights reserved
i6
LOW
ET AL.
AJR:i55,
July 1990
Fig. 5.-Sonograms of normal pancreas transplant with bladder drainage. A, Longitudinal sonogram of graft lying medial and anterior to illopsoas muscle shows homogeneous texture (straight arrows). Iliac wing (curved arrows) is posterior. B, Transverse sonogram shows similar sonographic features (solid arrows). Venous anastomosis is marginated by bright echoes (open arrows) representing surgical sutures. C, Longitudinal sonogram shows papilla of Vater (white arrow) projecting into distended donor duodenum. Pancreatic duct (black arrows) courses superiorly from papilla.
Fig. 6.-CT appearance of normal pancreas transplant. A, Axis of graft is horizontal. Parenchyma is homogeneous with distinct margins (arrows). Renal transplant is seen on left. B, Lower CT scan shows duodenum filled with contrast material (arrows) refluxed from urinary bladder. Uterus is posterior to donor duodenal stump.
Parenchymal
Abnormalities
mation intensity,
Changes in graft size may be noted with serial imaging by nuclear medicine, sonography, CT, and MR. An increase in graft size has been associated with both acute rejection and pancreatitis (Figs. 8A and 9) [9, 1 1 , 13, 22-24]. Posttransplantation recovery, resolution of acute rejection, gradual loss
of exocrine tissue in endocrine functional grafts, and chronic rejection have been cited as causes of decreased allograft size [9, 1 3, i 4, 20, 22-25]. Small grafts have been seen with normal endocrine function. Scintigraphic
hallmarks
of transplant
pathologic
changes
are decreased pancreas intensity in both the perfusion and static portions of the study, increased delay between arterial and pancreatic intensity peaks in serial perfusion images, decreased homogeneity of graft activity, and a change in the apparent
size of the pancreas
[9]. Both
rejection
and inflam-
may cause a delayed increased
graft
pancreatic
peak of decreased
size, and decreased
homogeneity
of
graft activity (Fig. 9) [7, 9, 1 0, 13]. However, a sensitivity of 86% has been reported for the diagnosis of rejection in a small series [9]. An anechoic or hypoechoic graft may be seen sonographically in the immediate postoperative period. This appearance is nonspecific; it may occur because of rejection or pancreatitis but also may be seen in a normally functioning pancreas. Acute
rejection
reportedly
results
in an enlarged
organ
with
diffuse or patchyfoci of decreased echogenicity or anechoicity [9, 13, 24]. A sensitivity of 82% has been reported for the sonographic diagnosis of acute rejection [9]. Inhomogeneous parenchymal echo texture and ductal dilatation have been cited as more specific sonographic features. The first is seen only in rejection and the second is seen exclusively in pancreatitis [13]. Increased parenchymal echogenicity, particu-
Downloaded from www.ajronline.org by 117.253.182.228 on 10/27/15 from IP address 117.253.182.228. Copyright ARRS. For personal use only; all rights reserved
AJA:155,
July 1990
PANCREAS
TRANSPLANT
17
IMAGING
Fig. 7.-MR appearance of acute pancreas graft rejection. A, Coronal Ti-weighted MR Image, SE 850/20 (TR/TE), of normally functioning whole pancreas graft 3 weeks after transplantation. Pancreas lies obliquely (straight solid arrows), with homogeneous parenchymal signal. Focus of high signal intensity (curved arrow) also had high T2 signal and represents subacute hemorrhage. Signal void (open arrow) in graft vasculature is due to flowing blood. Large amount of low-signal pelvic ascites surrounds graft. B, MR image, SE 850/20, 15 days later shows acute rejection. Focal patch of decreased Ti signal (straight arrow) is present. Focal hemorrhage is no longer apparent. Metal artifact (curved arrow) is due to duodenal staples. Free fluid is still present. C, T2-weighted MR image, SE 2000/90, corresponding to B shows focal patch of high signal (arrows) in same area as low Ti signal
Fig. 8.-CT appearance of acute rejection and loculated peritranspiant fluid. A, Pancreas (arrows) is enlarged and Inhomogeneous. Soft-tissue infiltration of peripancreatic fat is minimal and graft margins are fairly distinct. Graft pancreatectomy showed acute rejection with necrosis. B, Lower scan several days earlier shows staple line (straight arrows) at duodenocystostomy. Loculated fluid, a sterile abscess anterior to pancreas (curved arrows), was percutaneously drained under sonographic guidance.
vA1 A
B
Ir
...-1
..,-.‘..‘
--,.‘j-
Fig. 9.-Scintlgrams of pancreas transplant rejection show enlarged, poorly defined, inhomogeneous, left-sided pancreas graft (arrows). Renal transplant is present on right. A, Early perfusion scintigram. B, Immediate static scintigram.
A
B
18
LOW
ET AL.
AJR:155,
July 1990
Downloaded from www.ajronline.org by 117.253.182.228 on 10/27/15 from IP address 117.253.182.228. Copyright ARRS. For personal use only; all rights reserved
Fig. 10.-Normal Doppler findings of pancreas graft vasculature. A, Arterial waveform is typical of low-impedance system with continuous diastolic flow. B, Venous flow within vascular pedicle of graft is continuous.
larly when chronic
associated
rejection.
with
decreased
Pancreatic
identified as brightly echogenic shadowing. The use of Doppler technology rejection.
Analogous
to the
flow
graft
calcifications
size, indicates occasionally
foci with posterior
may indicate
in renal
impaired
diastolic
rejection specificity
(Fig. i 0). Unfortunately, this technology in the diagnoses of renal transplant
and has been assessed
acoustic
may aid in diagnosing
situation
are
acute
transplants,
the presence
of acute has limited dysfunction
in only small series of pancreas
grafts
in which histopathologic correlation has been minimal. Two recent reports [26, 27] suggest that an increase in the Doppler
resistive index, a quantitative measure of vascular impedance, may be valuable in the diagnosis of acute pancreas transplant rejection. A parenchymal resistive index of 0.70 or greater had a sensitivity of 76% and a specificity of 100% in diagnosing acute
rejection.
Early reports on CT of pancreatic transplants variable success in visualizing duct-occluded drained
grafts
that were
placed
high within
described
and
the pelvis
bowel[1 2, 24,
25]. When bladder drainage is used, poor or no visualization of the graft is uncommon. Parenchymal abnormalities seen on CT include variable degrees of graft inhomogeneity, focal areas of increased attenuation and inhomogeneity, and softtissue infiltration of the peripancreatic fat (Fig. 8A) [1 1-14]. These
findings,
typically
suggestive
of pancreatitis,
are non-
specific and may be seen with peripancreatic infection, hemorrhage, exocrine leakage, graft thrombosis, and even rejection. However, pathologically proved parenchymal infarction and necrosis, pancreatic abscess, and a large pseudocyst were seen to evolve on serial scans in three patients with acute rejection diagnosed clinically; the end-stage graft appeared as a pancreatiform mass of water attenuation [i 4]. Focal areas of decreased attenuation have been shown pathologically to represent abscesses and parenchymal infarction with cystic necrosis [12, i 4]. Focal areas of increased attenuation have been attributed to intraparenchymal hemorrhage, though no pathologic verification was included (Fig. ii C)
[1 1]. Pancreatic duct calcification seen on CT also has been described. In contrast to the lack of specificity of CT, initial results in a small group of patients suggest that MR may be capable of making more specific diagnoses. Vahey et aI. [20] reported an increase in the mean T2 value of the graft parenchyma during acute rejection, presumably because of tissue edema. However, in their study, all scans were obtained within 1.5 months after transplantation, when persistent postoperative edema might be expected. In another study, patterns of parenchymal signal change on MR were correlated with the clinical diagnoses [22]. Acutely rejecting grafts showed decreased Ti signal similar to that of muscle and increased T2 signal equal to or greater than that of urine (Fig. 7). These abnormal signal intensities were usually multifocal, although these findings were seen also in several patients without clinical manifestations of rejection.
During
recovery
from
rejection,
the
parenchymal
signal returned to normal or formed focal areas of high T2 signal, thought to represent pseudocysts. An earlier report [9] by this group cited a sensitivity of 1 00% and a specificity of 76% for MR in the diagnosis of acute rejection. Most importantly, the negative predictive value of a normal-appearing graft was 100%. False-positive examinations occurred in the immediate
postoperative
period
or with resolution
of acute
rejection. Thus, signal changes seen during acute rejection may persist beyond treatment. In contrast, chronic rejecting grafts were small, with both decreased Ti and T2 signal. These studies are limited by their dependence on the clinical diagnosis and the lack of histopathologic correlation for categorizing complications. Fluid Collections Detection of complicating abdominal or pelvic fluid can be accomplished with sonography, CT (Figs. 8 and 12), and MR (Fig. 7). Peripancreatic fluid is the most common abnormality seen on sonography or CT after pancreas transplantation [11,
Downloaded from www.ajronline.org by 117.253.182.228 on 10/27/15 from IP address 117.253.182.228. Copyright ARRS. For personal use only; all rights reserved
AJR:i55,
PANCREAS
July 1990
Fig. 11.-Graft thrombosis and parenchymal necrosis. A, Initial Tc-DTPA flow study shows normal flow to midline pancreas (arrows). B, Perfusion study 3 days later fails to show graft. C, CT scan obtained on same day as B shows graft Is enlarged and markedly inhomogeneous (straight arrows). Focal areas of high attenuation within graft are thought to represent hemorrhage. Small amount of peritransplant fluid (curved arrows) is present anterior and lateral to graft. D, Balloon-occlusion angiogram obtained on same day shows Internal iliac artery projecting to right of catheter on this steep oblique view. Proximal segments of donor celiac axis (straight arrow) and donor superior mesenteric artery (curved arrow) are minimally opacifled downstream from Carrel patch, reflecting high resistance to flow within graft. No arterial occlusion or thrombus was identified. Further opacification of graft arteries could not be obtained.
TRANSPLANT
19
IMAGING
-
31
‘4.
-
...,
.-..
.-.‘ ..,
.
...-..
..
-‘:“
.-1
t”’)’4.
..
-.
.
-
.
.
.‘4t‘..“..Pt.:
‘
#{149}-..,,;
.‘‘:
i.. ....
:‘“‘.
. ...
A
‘..
B
Fig. 12.-CT cystogram of duodenal stump leak. A, CT scan without bladder contrast material shows large amount of complex fluid in deep pelvis (straight arrows) and linear collection of fluid in anterior pelvis (curved arrows). Part of graft is seen in mid pelvis. Renal transplant is present on left. B, After administration of bladder contrast material, extravasation into anterior fluid collection (arrow) is seen from right side of donor duodenal stump. Fluid was drained and leak was repaired at surgery.
12, 14, 17, 19,22-24].
amounts;
the largest
commonly seen when rectly to the peritoneal
Free ascites may be present in various accumulations are pancreatic ascites exocrine secretions were drained dicavity. Frank intraparenchymal fluid is
shown occasionally, although its significance has not been well characterized. The character of extrapancreatic fluid often cannot be established. However, CT may show gas bubbles or focal
areas of relatively high attenuation within a fluid collection, suggesting abscess or hemorrhage, respectively. Additionally, a specific diagnosis of exocrine leak can be made on the basis of CT findings when extravasated bladder contrast material is detected either in a focal fluid collection or within ascites (Fig. i 2). Alternatively, fluoroscopic cystography may be performed for precise localization of the site of leakage [28].
Downloaded from www.ajronline.org by 117.253.182.228 on 10/27/15 from IP address 117.253.182.228. Copyright ARRS. For personal use only; all rights reserved
20
LOW
Specific characterization of certain posttransplantation fluid collections is possible with MR. Both intra- and extraparenchymal hemorrhage or hematoma can be diagnosed when the short Ti and long T2 signal of subacute blood is present (Fig. 7B). A recent report [22] describes the progression of intraparenchymal foci of high T2 signal, seen during acute rejection, to smoothly marginated areas of even higher T2 signal that presumably represent pseudocysts. The resorption of intraparenchymal hemorrhage or pseudocyst may result eventually in an area of low Ti and low T2 signal, probably due to either hemosiderin formation or fibrosis. Posttransplantation fluid collections ultimately require percutaneous aspiration and microbial analysis for precise characterization. Percutaneous catheter drainage of abdominal fluid collections
after pancreas
transplantation
was successful
in retaining a functional graft and avoiding repeat surgery in only 31 % of patients in one series [29]; sonographically or CT-guided
percutaneous
aspiration
obtained
diagnostic
ma-
terial in all cases, however. Vascular
Complications
Vascular creas graft 9, 1 0, i 3]. transplant “Tc-DTPA
thrombosis results in nonvisualization of the panon perfusion scintigraphy (Figs. 1 1A and i 1 B) [7, “Tc-labeled RBCs have been used for pancreas imaging but offer no significant advantage over except
with active
hemorrhage
[30].
On the other
ET AL.
AJR:155,
July 1990
due to other parenchymal processes, such as rejection or pancreatitis, or even to technical difficulties, such as obesity. In one case of proved graft thrombosis, no Doppler signal could be obtained from anywhere along the graft; in another, signals
were
obtained
from
the graft
vessels
in the anasto-
motic region but not from the parenchyma [27]. Two cases of pathologically proved venous thrombosis in nonfunctioning grafts have been reported [26], both of which had no venous Doppler signal in the presence of arterial flow. Studies showing high velocity or turbulence at the arterial or venous anastomoses suggest stenoses. Additionally, Doppler evidence of arterial flow within a perianastomotic fluid collection suggests a complicating pseudoaneurysm [18]. The larger vessels of the transplanted pancreas have been shown on both unenhanced and IV contrast-enhanced CT and are seen easily on MR. However, CT is of little value in assessing vascular patency [1 4]. Patency of the graft vessels is apparent on MR when a prominent flow void is shown, but thrombosis may be difficult to differentiate from slow flow in some instances (Fig. 7A) [31]. The usefulness of MR in the diagnosis of vascular complications has not been explored. Angiography of the transplanted pancreas has been described for small numbers of patients. Arterial irregularities and stenoses, diminished parenchymal opacification, and prolonged circulation of contrast material have been reported in two patients with rejection [32]. These abnormalities were unevenly distributed in one case. Another report [33] of 30
hand, Tc-labeled ABCs are theoretically inferior to “TcDTPA in evaluating edema associated with rejection or pancreatitis because of the nondiffusibility of RBCs.
arteriograms
Doppler sonography is capable of detecting major vascular complications in pancreatic grafts, such as vascular thrombosis, anastomotic strictures, and pseudoaneurysms [i 8]. Doppler identification of arterial and venous flow within the
cific for graft failure, as two of 12 patients with this pattern maintained normoglycemia (Fig. 1 1 D). Only normal arteriograms correlated with normal graft function.
vascular pedicle of the graft, and within the graft parenchyma, indicates that the graft vasculature is patent. Inability to detect arterial or venous flow with Doppler imaging may reflect primary vascular thrombosis (Fig. 13); alternatively, it may be
in duct-occluded
five angiographic rejection.
segmental
patterns,
Nonvisualization
none
allografts
of which
of the graft
vessels
described
correlated was
with
not spe-
Conclusions Pancreas therapeutically,
transplantation, has a relatively
although
increasingly
high complication
effective rate. As the
Fig. 13.-Arterial and venous thrombosis. A, Graft is markedly echogenic and inhomogeneous (straight arrows) on sonogram. Artery supplying graft (curved arrow) is anastomosed to recipient iliac artery. B, Doppler signal in graft artery shows sharp systolic peaks and reversal of diastolic flow (ar. rows) in contrast to normal arterial flow seen 3 days earlier. No Doppler signal could be obtained from graft vasculature 4 days later. Pancreatectomy revealed arterial and venous thrombosis with hemorrhagic necrosis.
AJR:155,
PANCREAS
July 1990
TRANSPLANT
clinical setting is commonly nonspecific, imaging is done to help characterize these complications. Nuclear medicine, so-
Downloaded from www.ajronline.org by 117.253.182.228 on 10/27/15 from IP address 117.253.182.228. Copyright ARRS. For personal use only; all rights reserved
nography,
CT, and MR are all sensitive
in detecting
parenchy-
mal abnormalities and changes in graft size and margination but currently are not capable of detecting rejection early enough in its development to have a meaningful impact on therapy. Some exceptions to this generalization may be evolving; preliminary results suggest that duplex Doppler sonography may be specific in the diagnosis of acute rejection, and, if clinical and imaging findings are ambiguous, a normal MR finding essentially excludes rejection. Sonography,
CT, and MR are all capable
of showing
post-
transplantation fluid. Specific characterization of fluid may be possible in certain instances, but diagnostic aspiration is required to exclude infection. Conventional or CT cystography permits diagnosis of leaks at the duodenal stump or anastomosis. Nuclear medicine, duplex sonography, and, potentially, MR can be used to diagnose vascular thrombosis, with angiography used to confirm suspected thrombosis. Pseudoaneurysms can be shown by using duplex sonographic techniques, but generally angiography is required for preoperative planning. Reports sonography,
evaluating the capabilities CT, MA, and angiography
of nuclear for accurate
medicine, diagnosis
of pancreas transplantation complications are scarce, and the majority share common flaws. Imaging findings usually are correlated with the clinical diagnosis or with histopathologic data from a coexisting renal transplant. Even the second method of diagnosis can be inaccurate, as recent evidence suggests that renal and pancreatic rejection can occur discordantly [22, 34]. Systematic correlation of radiologic findings with histopathologic data has not been possible, in part because safe percutaneous biopsy techniques for pancreas grafts have not been developed. Pathologic data obtained from later surgical resection of an end-stage graft may not reflect the underlying pathologic changes present at an earlier imaging study. Ultimately, delineation of the role of imaging awaits further characterization of the range of normal graft appearances, as well as pathologic correlation with large numbers of dysfunctional grafts.
surveillance
of the allografted
2i
pancreas.
AJR 1988;i
50:811-816
8. Catafau AM, Lome#{241}aFJ, Ricart J, et al. Indium-il 1-labeled platelets in monitoring human pancreatic transplants. J Nucl Med 1989;30: 14701475 9. Yuh WTC, Wiese JA, Abu-YousefMM, etal. Pancreatic transplant imaging. Radiology 1988;i67:679-.683 10. Kuni CC, duCret RP, Boudreau RJ. Pancreas transplants: evaluation using perfusion scintigraphy. AJR 1989;i53:57-6i ii . Letoumeau JG, Maile CW, Sutherland DER, Feinberg SB. tJtrasound and computed tomography in the evaluation of pancreatic transplantation. Radiol Ciln North Am 1987;25:345-355 i2. Maile CW, Crass JR, Frick MP, Feinberg SB, Goldberg ME, Sutherland DER. CT of pancreas transplantation. Invest Radiol i985;20:609-6i2 i3. Patel B, Markivee CR, Mahanta B, vas W, George E, Garvin P. Pancreatic transplantation: scintigraphy, US and CT. Radiology 1988;167:685-687 14. Moulton JS, Munda R, Weiss MA, Lubbers DJ. Pancreatic transplants: CT with clinical and pathologic correlation. Radiology 1989;172:21-26 is. MarinCek B, Schlumpf R, Decurtins M, von Schulthess GK, Largiadbr F. Radiologische diagnostik nach pankreastransplantation. Radiologe 1988; 28: 560-565 16. Rasmussen K, Burcharth F, Thomson HS, Rygaard H. Monitoring of pancreas-graft perfusion by radionuclide and digital subtraction angiography. Diabetes 1989;38(suppl 1):21-23 17. Yuh WTC, Hunsicker LG, 5ato Y, Wright FH Jr, Smith JL, Cony RJ. Application of magnetic resonance imaging in pancreas transplant. Diabetes 1989;38(suppl i):27-29 18. Tobben PJ, Zajko AB, Sumkin JH, et al. Pseudoaneurysms complicating organ transplantation: roles of CT, duplex sonography, and angiography. Radiology 1988;i69:65-70 19. Toledo-Pereyra LH, Zeskind HJ, Mittal vK. (Jtrasound imaging of cliinical pancreatic organ transplants. JCU 1982;10: 12i -124 TN, Glazer GM, Francis IR, et al. MR diagnosis of pancreatic transplant rejection. AJR 1988;150:557-560 Jennerholm 5, Fr#{244}dinL, Hernmingsson A, Johansson G, Tufveson G. Magnetic resonance imaging of kidney and pancreatic transplants. Transplant Proc 1988;20:425-426 Yuh WTC, Hunsicker LG, Nghiem DD, et al. Pancreatic transplants: evaluation with MR imaging. Radiology 1989;1 70:171-177 Crass JR, Sutherland DER, Feinberg SB. Sonography of the segmental human pancreatic transplant. JCU 1982;1 0:149-152 Crass JR. Feinberg SB. Sutherland DER, Loken M, Gedgaudas EG. Radiology of the human segmental pancreatic transplant. Gastrointest Radiol 1982;7: 153-1 58 Schlumpf R, Manncek B, Schulthess Gv, Decurtins M, Largiad#{232}rF. Magnetic resonance imaging and computed tomography in long-term-functioning duct-occluded pancreas allotransplants. Diabetes 1989;38(suppl 1): 24-26 Gilabert R, Fern#{226}ndez-Cruz L, Bru C, Sans A, Andreu J. Duplex-Doppler ultrasonography in monitoring clinical pancreas transplantation. Transpllnt 1988;i :172-i 77 Patel B, Wolverson MK, Mahanta B. Pancreatic transplant rejection: assessment with duplex US. Radiology 1989;173: 13i -135 Woolsey EJ, Tauscher JR, Dafoe DC. Pancreas transplantation with pancreatico-duodeno-cystostomy for exocrine drainage. AJR 1987;149: 507-509 Letoumeau JG, Hunter DW, Crass JG, Thompson WM, Sutherland DER. Percutaneous aspiration and drainage of abdominal fluid collections after pancreatic transplantation. AJR i988;150:805-809 Kuni C, duCret R, Boudreau R. Perfusion scintigraphy in pancreas transplant patients. Presented at the International Congress of Radiology, Paris, July 1989 Zirinsky K, Markisz JA, Rubenstein WA, et al. MR imaging of portal venous thrombosis: correlation with CT and sonography. AJR 1988;i50:283-288 Svahn T, Lewander R, Hardstedt C, Lundgren G, Sundelin P, Groth C-G. Angiography and scintigraphy of human pancreatic allografts. Acta Radiol [Diagnj (Stockh) 1978;19:297-304 lllner W-D, Berger H, StablerA, Abendroth D, Landgraf R, Land W. Puzzling angiographic findings in pancreatic transplantation. Transplant Proc 1989;21 :2803 Sollinger HW, Stratta RJ, D’AlessandroAM, Kalayoglu M, Pirsch JD, Belzer FO. Experience with simultaneous pancreas-kidney transplantation- Ann Surg 1988;208:475-482
20. vahey 21
.
22. 23. 24.
25.
26.
27. 28.
REFERENCES 1 . Sutherland DER , Moudry KC, Najarian JS. Pancreas transplantation. In: Cerilli GJ, ed. Organ transplantation and replacement. Philadelphia: Lippincott, 1988:535-574 2. Hanto Dw, Sutherland DER. Pancreas transplantation: clinical considerations. Radiol Clin North Am i987;25:333-343 3. Moudry-Munns KC, ed. International pancreas transplant registry newsletfor, vol. 2, no. 3. Minneapolis: International Pancreas Transplant Registry, 1989 4. Sutherland DER, Chow SY, Moudry-Munns KC. International transplant registry report-i 988. Clin Transplant 1989;3: 129-1 49 5. Sutherland DER, Dunn DL, Goetz FC, et al. A ten year experience with 290 pancreas transplants at a single institution. Ann Surg 1989;2i0: 274-288 6. Simmons RL, Finch ME, Ascher NL, Najarian JS, eds. Manual of vascular access, organ donation and transplantation. New York: Springer-verlag, 1984:105-164, 237-254 7. George EA, Salimi Z, Camey K, Casta#{241}eda M, Garvin PJ. Radionuclide
IMAGING
29.
30.
31 32.
33.
34.
.
13
Progress
Pancreas Robert
A. Low,1
Transplant Christopher
Imaging:
diabetics
than 50% of type I diabetics have or neuropathy within 20 years of [1 ]. Pancreatic transplantation is
undertaken in selected patients in an attempt to prevent, arrest, or reverse progression of these complications [1 , 2]. The first human pancreas transplantation was performed in 1966. Through June 1989, 2004 pancreas transplantations have been reported at 128 institutions [3]. Improved surgical techniques combined with increasingly efficacious immunosuppression have led to continuous improvement in function of pancreatic grafts and survival rates of patients. For the 3year period 1 986 through 1 988, 1 -year graft function and recipent survival rates were 54% and 87%, respectively [4, 5]. Surgical techniques in pancreatic allografting have evolved considerably [1 , 2, 6]. All live donor grafts are necessarily segmental (Fig. 1). A whole or segmental graft may be obtamed from a cadaver (Figs. 1-3). Whole pancreas transplantation is preferred over segmental transplantation because of the theoretically lower risk of thrombosis in whole grafts, which have a higher blood flow, and because of the larger beta-cell mass available [1]. Revascularization of the pancreatic graft usually is accomplished through anastomoses with the iliac vessels (Figs. 13). However, revascularization of the graft is occasionally done with anastomoses made to the recipient splenic or inferior mesenteric vessels, permitting the venous effluent to drain
into the portal venous with these
has been shown
system; no metabolic variations [1].
advantage
Received November 17, 1989; accepted after revision February ‘All authors: Department of Radiology, University of Minnesota reprintrequests to J. G. Letoumeau. AJR 155:13-21,
An Overview
C. Kuni, and Janis Gissel Letourneau
There are more than one million insulin-dependent in the United States. More retinopathy, nephropathy, the onset of the disease
in Radiology
July 1990 036i-803X/90/i551-00i3
© American
Numerous techniques have been used to manage exocrine secretions in pancreas transplants, including duct ligation and free intraperitoneal drainage. These methods generally have been abandoned, as have synthetic polymer ductal injection and exocrine drainage to recipient ureter and stomach. Both segmental and whole pancreas grafts typically are drained to either small bowel (Fig. 1) or bladder (Figs. 2 and 3); bladder drainage is now the preferred technique [1 , 4, 5]. Bladder
exocrine drainage appears to minimize leaks and facilitates urinary monitoring of pancreatic exocrine function. Complications of pancreatic transplantation are common and are associated with a substantial risk of patient morbidity or mortality [2]; the clinical setting is often nonspecific and it is not uncommon
i4, i990. Hospital and Clinic, Roentgen
for there
to be coexisting
complications.
Rejection is the most common cause of endocrine failure, occurring in up to 35% of pancreas transplants [1 , 2]. Pancreatic or peripancreatic abscess is a life-threatening problem, often requiring transplant pancreatectomy, and is seen in 822% of recipients [2, 4]. Thrombosis leads to graft failure in 12% of pancreas grafts [4]. Other complications include pancreatitis and fluid collections such as hematomas, lymphoceles, urinomas, pseudocysts, diffuse pancreatic ascites, and leaks at the exocrine anastomoses. Posttransplantation complications are most easily considered in terms of three categories related to diagnostic imaging: parenchymal abnormalities, pancreatic or peripancreatic fluid, and vascular complications. The goal of imaging of the transplanted pancreas is to characterize complications and to guide percutaneous aspi-
Box 292 UMHC,
Ray Society
420 Delaware
St. SE., Minneapolis, MN
55455.
Address
Downloaded from www.ajronline.org by 117.253.182.228 on 10/27/15 from IP address 117.253.182.228. Copyright ARRS. For personal use only; all rights reserved
14
LOW
Fig. 1.-Drawing shows technique of segmental pancreas graft transplantation. Pancreatic segment is obtained from live donor or cadaveric donor from whom liver is also harvested. Pancreas is divided at level of donor portal vein. Body and tail of graft are harvested with splenic artery and vein, which are anastomosed to recipient iliac vessels (arrows). Cut end of graft is intussuscepted into Roux-en-Y limb of recipient jejunum. Pancreatic stent is placed in the duct and eventually will pass through the intestine.
Techniques
transplants
studies and because frequently is needed.
DTPA are administered
distension,
present
or
because study Twenty
it can be used for perfusion of coexisting renal transplants millicuries (740 MBq) of mTc-
IV, and 16 serial 2-sec
images
are
followed by an immediate 500,000-count static image. Image variables examined are (1) time delay from peak iliac arterial to peak pancreatic activity; (2) relative intensities of arterial and pancreatic peak activity on perfusion and static images; and (3) changes in size, homogeneity, and definition of the pancreas over serial studies. Sonography is used frequently for noninvasive imaging of pancreas transplants when fever, abdominal pain, abdominal
laboratory
is performed. the sonographic
evidence
of graft
and transverse
dysfunction
is
sonography
of
Distension of the urinary examination by elevating
loops out of the pelvis and distending
the donor
bladder bowel
duodenal
if one was used. Visualization of the graft may be when enteric drainage has been used, as bowel loops
often completely can be used to differenallografts. 00mTc-sulfur 99mTc..DTPA have some other pathologic changes used frequently to study
July 1990
Fig. 3.-Drawing shows whole pancreas graft from cadaveric liver donor. Small patch of aorta containing superior mesenteric artery is anastomosed to recipient iliac artery. Donor splenic artery is anastomosed to donor superior mesenteric artery (open arrow). Gastroduodenal artery is ligated at its origin. Portal vein is eectioned just beyond termination of splenic vein. Segment of donor iliac vein is anastomosed to donor portal vein stump (solid arrow) to provide venous conduit of sufficient length for anastomosis to recipient iliac vein. Whole segment of donor duodenum is anastomosed to bladder.
[2, 1 1]. Longitudinal
the graft facilitates stump, difficult
Several scintigraphic techniques tiate normal from abnormal pancreas colloid, 1ln-labeled platelets, and value in differentiating rejection from in the graft [7-10]. 99mTc-DTPA is
pancreas
AJA:i55,
Fig. 2.-Drawing shows whole pancreas graft from cadaveric nonliver donor. Carrel aortic patch (straight arrow), including origins of celiac axis and superior mesenteric artery, is anastomosed to recipient iliac artery; native pancreatic arterial supply is left intact. Portal vein (curved arrows) drains to recipient iliac vein. Patch of donor duodenum is anastomosed to bladder.
ration or drainage of associated fluid collections. Nuclear medicine, sonography, CT, MR imaging, and angiography have been used to evaluate posttransplant complications. In this review, we summarize the often complementary capabilities of these imaging techniques.
Imaging
ET AL.
surround
the graft. The peripancreatic
region
and the remainder of the pelvis and abdomen are examined to detect the presence of free or loculated fluid. Sonography of pancreas transplants should include DoppIer evaluation of the graft vasculature. Arterial and venous
Doppler signals are obtained throughout the length of the extraparenchymal vascular pedicle and within the pancreatic parenchyma. Knowledge of the vascular reconstruction of a given graft and the use of color Doppler technology facilitates this portion of the examination. Abdominal and pelvic CT, used primarily to detect fluid collections, is done with complete intestinal opacification, which aids in separating graft parenchyma or fluid collections from adjacent bowel loops [11-14]. IV contrast material is administered infrequently, to avoid the risk of nephrotoxicity, if native renal function is impaired or if there is a coexisting renal transplant. Rescanning the pelvis with retrograde bladder or rectal contrast material may aid in differentiating graft
Downloaded from www.ajronline.org by 117.253.182.228 on 10/27/15 from IP address 117.253.182.228. Copyright ARRS. For personal use only; all rights reserved
AJA:155,
PANCREAS
July i990
TRANSPLANT
Fig. 4.-Scintigrams of normally functioning transplant. A, Dynamic-phase scintigrams are taken every 2 sec. Pancreatic radioactivity equal. B, Static scintigram. Pancreas is homogeneous and well marginated (arrows).
15
IMAGING
peak
(arrow)
occurs
2 sec after
arterial
peak
and peak
or fluid from adjacent bowel and bladder and in detecting an exocrine leak. MR imaging of pancreas allografts generally is performed in the coronal plane, permitting simultaneous long-axis imaging of the renal transplant, if present. Ti and T2-weighted spin-echo (SE) images are obtained with a 5-mm slice thickness. Supplemental Ti -weighted axial scans may aid in localizing the graft. Respiratory gating of the sequences is usually not necessary because of the low pelvic location of most pancreas transplants. To date, no systematic evaluation of variable flip-angle or other pulse sequences in pancreas transplants has been reported. Angiography is used primarily to confirm or clarify suspected vascular thrombosis, anastomotic stricture, or pseudoaneurysm detected by other imaging techniques [9, 15-
is characterized by a delay of the peak pancreatic than 4 sec from the arterial peak and by equal
18]. Both intraarterial
homogeneous
medium
muscle
5).
-
and IV digital
subtraction
techniques
can be used to evaluate graft vasculature. Conventional transfemoral angiography can be performed either from contralateral or ipsilateral approaches. Conventional angiography with a balloon-occlusioncatheter is currently the preferred technique for evaluation of pancreas transplants at our institution; this technique minimizes contrast dose to the patient and maximizes opacification of the pancreas transplant vasculature.
pancreatic function
Transplant
Imaging
(Fig. 4); however,
reported
when
activity arterial
clinically
no perfusion
are
less and
normal
is detectable
scintigraphically [9]. A normally functioning, complication-free transplant is suggested by serial studies that show constant peak timing geneity.
and peak
intensity,
The early posttransplantation
pancreatic
size,
appearance
and homo-
of the graft on
sonography, CT, and MR does not correlate well with endocrine function [9, 13, 14, i 7, 19-22], presumably because of the effects of preservation injury and the trauma of surgical handling. Graft appearance normalizes within several weeks
after transplantation, tion is stabilized, (Fig.
asymptomatic
if no complications sonographically
intervene.
normal
level of echogenicity
Although
experience
Once func-
parenchyma
has a
similar to that of is limited
because
recipients
ance of the normal
are studied rarely, the CT appeartransplant has been described as homo-
geneous and well marginated, with a density similar to that of native pancreas (Fig. 6) [1 3, 14]. Parenchymal signal intensity similar to that of normal renal cortex and greater than that of muscle on Ti -weighted images, and similar to that of fat but less than that of urine on T2-weighted images, is seen on MR of uncomplicated allografts (Fig. 7A) [9, i 7, 22]. The
pancreatic Pancreas
peak intensities has been
intensities
duct is typically
eter and frequently
5C). Both injections
no greater
is demonstrable
of polymer
than 2-3 mm in diam-
only sonographically
and stents
within
Normal Appearance
creatic staples
Isolated 9smTcDTPA studies are less accurate in evaluating pancreas transplants than are serial studies. A normal study
duodenocystostomy may be seen on sonography metallic artifacts may be seen on MR.
(Fig.
the pan-
duct are detectable with sonography and CT. Surgical at the ligated ends of the donor duodenum and at the
and CT and
Downloaded from www.ajronline.org by 117.253.182.228 on 10/27/15 from IP address 117.253.182.228. Copyright ARRS. For personal use only; all rights reserved
i6
LOW
ET AL.
AJR:i55,
July 1990
Fig. 5.-Sonograms of normal pancreas transplant with bladder drainage. A, Longitudinal sonogram of graft lying medial and anterior to illopsoas muscle shows homogeneous texture (straight arrows). Iliac wing (curved arrows) is posterior. B, Transverse sonogram shows similar sonographic features (solid arrows). Venous anastomosis is marginated by bright echoes (open arrows) representing surgical sutures. C, Longitudinal sonogram shows papilla of Vater (white arrow) projecting into distended donor duodenum. Pancreatic duct (black arrows) courses superiorly from papilla.
Fig. 6.-CT appearance of normal pancreas transplant. A, Axis of graft is horizontal. Parenchyma is homogeneous with distinct margins (arrows). Renal transplant is seen on left. B, Lower CT scan shows duodenum filled with contrast material (arrows) refluxed from urinary bladder. Uterus is posterior to donor duodenal stump.
Parenchymal
Abnormalities
mation intensity,
Changes in graft size may be noted with serial imaging by nuclear medicine, sonography, CT, and MR. An increase in graft size has been associated with both acute rejection and pancreatitis (Figs. 8A and 9) [9, 1 1 , 13, 22-24]. Posttransplantation recovery, resolution of acute rejection, gradual loss
of exocrine tissue in endocrine functional grafts, and chronic rejection have been cited as causes of decreased allograft size [9, 1 3, i 4, 20, 22-25]. Small grafts have been seen with normal endocrine function. Scintigraphic
hallmarks
of transplant
pathologic
changes
are decreased pancreas intensity in both the perfusion and static portions of the study, increased delay between arterial and pancreatic intensity peaks in serial perfusion images, decreased homogeneity of graft activity, and a change in the apparent
size of the pancreas
[9]. Both
rejection
and inflam-
may cause a delayed increased
graft
pancreatic
peak of decreased
size, and decreased
homogeneity
of
graft activity (Fig. 9) [7, 9, 1 0, 13]. However, a sensitivity of 86% has been reported for the diagnosis of rejection in a small series [9]. An anechoic or hypoechoic graft may be seen sonographically in the immediate postoperative period. This appearance is nonspecific; it may occur because of rejection or pancreatitis but also may be seen in a normally functioning pancreas. Acute
rejection
reportedly
results
in an enlarged
organ
with
diffuse or patchyfoci of decreased echogenicity or anechoicity [9, 13, 24]. A sensitivity of 82% has been reported for the sonographic diagnosis of acute rejection [9]. Inhomogeneous parenchymal echo texture and ductal dilatation have been cited as more specific sonographic features. The first is seen only in rejection and the second is seen exclusively in pancreatitis [13]. Increased parenchymal echogenicity, particu-
Downloaded from www.ajronline.org by 117.253.182.228 on 10/27/15 from IP address 117.253.182.228. Copyright ARRS. For personal use only; all rights reserved
AJA:155,
July 1990
PANCREAS
TRANSPLANT
17
IMAGING
Fig. 7.-MR appearance of acute pancreas graft rejection. A, Coronal Ti-weighted MR Image, SE 850/20 (TR/TE), of normally functioning whole pancreas graft 3 weeks after transplantation. Pancreas lies obliquely (straight solid arrows), with homogeneous parenchymal signal. Focus of high signal intensity (curved arrow) also had high T2 signal and represents subacute hemorrhage. Signal void (open arrow) in graft vasculature is due to flowing blood. Large amount of low-signal pelvic ascites surrounds graft. B, MR image, SE 850/20, 15 days later shows acute rejection. Focal patch of decreased Ti signal (straight arrow) is present. Focal hemorrhage is no longer apparent. Metal artifact (curved arrow) is due to duodenal staples. Free fluid is still present. C, T2-weighted MR image, SE 2000/90, corresponding to B shows focal patch of high signal (arrows) in same area as low Ti signal
Fig. 8.-CT appearance of acute rejection and loculated peritranspiant fluid. A, Pancreas (arrows) is enlarged and Inhomogeneous. Soft-tissue infiltration of peripancreatic fat is minimal and graft margins are fairly distinct. Graft pancreatectomy showed acute rejection with necrosis. B, Lower scan several days earlier shows staple line (straight arrows) at duodenocystostomy. Loculated fluid, a sterile abscess anterior to pancreas (curved arrows), was percutaneously drained under sonographic guidance.
vA1 A
B
Ir
...-1
..,-.‘..‘
--,.‘j-
Fig. 9.-Scintlgrams of pancreas transplant rejection show enlarged, poorly defined, inhomogeneous, left-sided pancreas graft (arrows). Renal transplant is present on right. A, Early perfusion scintigram. B, Immediate static scintigram.
A
B
18
LOW
ET AL.
AJR:155,
July 1990
Downloaded from www.ajronline.org by 117.253.182.228 on 10/27/15 from IP address 117.253.182.228. Copyright ARRS. For personal use only; all rights reserved
Fig. 10.-Normal Doppler findings of pancreas graft vasculature. A, Arterial waveform is typical of low-impedance system with continuous diastolic flow. B, Venous flow within vascular pedicle of graft is continuous.
larly when chronic
associated
rejection.
with
decreased
Pancreatic
identified as brightly echogenic shadowing. The use of Doppler technology rejection.
Analogous
to the
flow
graft
calcifications
size, indicates occasionally
foci with posterior
may indicate
in renal
impaired
diastolic
rejection specificity
(Fig. i 0). Unfortunately, this technology in the diagnoses of renal transplant
and has been assessed
acoustic
may aid in diagnosing
situation
are
acute
transplants,
the presence
of acute has limited dysfunction
in only small series of pancreas
grafts
in which histopathologic correlation has been minimal. Two recent reports [26, 27] suggest that an increase in the Doppler
resistive index, a quantitative measure of vascular impedance, may be valuable in the diagnosis of acute pancreas transplant rejection. A parenchymal resistive index of 0.70 or greater had a sensitivity of 76% and a specificity of 100% in diagnosing acute
rejection.
Early reports on CT of pancreatic transplants variable success in visualizing duct-occluded drained
grafts
that were
placed
high within
described
and
the pelvis
bowel[1 2, 24,
25]. When bladder drainage is used, poor or no visualization of the graft is uncommon. Parenchymal abnormalities seen on CT include variable degrees of graft inhomogeneity, focal areas of increased attenuation and inhomogeneity, and softtissue infiltration of the peripancreatic fat (Fig. 8A) [1 1-14]. These
findings,
typically
suggestive
of pancreatitis,
are non-
specific and may be seen with peripancreatic infection, hemorrhage, exocrine leakage, graft thrombosis, and even rejection. However, pathologically proved parenchymal infarction and necrosis, pancreatic abscess, and a large pseudocyst were seen to evolve on serial scans in three patients with acute rejection diagnosed clinically; the end-stage graft appeared as a pancreatiform mass of water attenuation [i 4]. Focal areas of decreased attenuation have been shown pathologically to represent abscesses and parenchymal infarction with cystic necrosis [12, i 4]. Focal areas of increased attenuation have been attributed to intraparenchymal hemorrhage, though no pathologic verification was included (Fig. ii C)
[1 1]. Pancreatic duct calcification seen on CT also has been described. In contrast to the lack of specificity of CT, initial results in a small group of patients suggest that MR may be capable of making more specific diagnoses. Vahey et aI. [20] reported an increase in the mean T2 value of the graft parenchyma during acute rejection, presumably because of tissue edema. However, in their study, all scans were obtained within 1.5 months after transplantation, when persistent postoperative edema might be expected. In another study, patterns of parenchymal signal change on MR were correlated with the clinical diagnoses [22]. Acutely rejecting grafts showed decreased Ti signal similar to that of muscle and increased T2 signal equal to or greater than that of urine (Fig. 7). These abnormal signal intensities were usually multifocal, although these findings were seen also in several patients without clinical manifestations of rejection.
During
recovery
from
rejection,
the
parenchymal
signal returned to normal or formed focal areas of high T2 signal, thought to represent pseudocysts. An earlier report [9] by this group cited a sensitivity of 1 00% and a specificity of 76% for MR in the diagnosis of acute rejection. Most importantly, the negative predictive value of a normal-appearing graft was 100%. False-positive examinations occurred in the immediate
postoperative
period
or with resolution
of acute
rejection. Thus, signal changes seen during acute rejection may persist beyond treatment. In contrast, chronic rejecting grafts were small, with both decreased Ti and T2 signal. These studies are limited by their dependence on the clinical diagnosis and the lack of histopathologic correlation for categorizing complications. Fluid Collections Detection of complicating abdominal or pelvic fluid can be accomplished with sonography, CT (Figs. 8 and 12), and MR (Fig. 7). Peripancreatic fluid is the most common abnormality seen on sonography or CT after pancreas transplantation [11,
Downloaded from www.ajronline.org by 117.253.182.228 on 10/27/15 from IP address 117.253.182.228. Copyright ARRS. For personal use only; all rights reserved
AJR:i55,
PANCREAS
July 1990
Fig. 11.-Graft thrombosis and parenchymal necrosis. A, Initial Tc-DTPA flow study shows normal flow to midline pancreas (arrows). B, Perfusion study 3 days later fails to show graft. C, CT scan obtained on same day as B shows graft Is enlarged and markedly inhomogeneous (straight arrows). Focal areas of high attenuation within graft are thought to represent hemorrhage. Small amount of peritransplant fluid (curved arrows) is present anterior and lateral to graft. D, Balloon-occlusion angiogram obtained on same day shows Internal iliac artery projecting to right of catheter on this steep oblique view. Proximal segments of donor celiac axis (straight arrow) and donor superior mesenteric artery (curved arrow) are minimally opacifled downstream from Carrel patch, reflecting high resistance to flow within graft. No arterial occlusion or thrombus was identified. Further opacification of graft arteries could not be obtained.
TRANSPLANT
19
IMAGING
-
31
‘4.
-
...,
.-..
.-.‘ ..,
.
...-..
..
-‘:“
.-1
t”’)’4.
..
-.
.
-
.
.
.‘4t‘..“..Pt.:
‘
#{149}-..,,;
.‘‘:
i.. ....
:‘“‘.
. ...
A
‘..
B
Fig. 12.-CT cystogram of duodenal stump leak. A, CT scan without bladder contrast material shows large amount of complex fluid in deep pelvis (straight arrows) and linear collection of fluid in anterior pelvis (curved arrows). Part of graft is seen in mid pelvis. Renal transplant is present on left. B, After administration of bladder contrast material, extravasation into anterior fluid collection (arrow) is seen from right side of donor duodenal stump. Fluid was drained and leak was repaired at surgery.
12, 14, 17, 19,22-24].
amounts;
the largest
commonly seen when rectly to the peritoneal
Free ascites may be present in various accumulations are pancreatic ascites exocrine secretions were drained dicavity. Frank intraparenchymal fluid is
shown occasionally, although its significance has not been well characterized. The character of extrapancreatic fluid often cannot be established. However, CT may show gas bubbles or focal
areas of relatively high attenuation within a fluid collection, suggesting abscess or hemorrhage, respectively. Additionally, a specific diagnosis of exocrine leak can be made on the basis of CT findings when extravasated bladder contrast material is detected either in a focal fluid collection or within ascites (Fig. i 2). Alternatively, fluoroscopic cystography may be performed for precise localization of the site of leakage [28].
Downloaded from www.ajronline.org by 117.253.182.228 on 10/27/15 from IP address 117.253.182.228. Copyright ARRS. For personal use only; all rights reserved
20
LOW
Specific characterization of certain posttransplantation fluid collections is possible with MR. Both intra- and extraparenchymal hemorrhage or hematoma can be diagnosed when the short Ti and long T2 signal of subacute blood is present (Fig. 7B). A recent report [22] describes the progression of intraparenchymal foci of high T2 signal, seen during acute rejection, to smoothly marginated areas of even higher T2 signal that presumably represent pseudocysts. The resorption of intraparenchymal hemorrhage or pseudocyst may result eventually in an area of low Ti and low T2 signal, probably due to either hemosiderin formation or fibrosis. Posttransplantation fluid collections ultimately require percutaneous aspiration and microbial analysis for precise characterization. Percutaneous catheter drainage of abdominal fluid collections
after pancreas
transplantation
was successful
in retaining a functional graft and avoiding repeat surgery in only 31 % of patients in one series [29]; sonographically or CT-guided
percutaneous
aspiration
obtained
diagnostic
ma-
terial in all cases, however. Vascular
Complications
Vascular creas graft 9, 1 0, i 3]. transplant “Tc-DTPA
thrombosis results in nonvisualization of the panon perfusion scintigraphy (Figs. 1 1A and i 1 B) [7, “Tc-labeled RBCs have been used for pancreas imaging but offer no significant advantage over except
with active
hemorrhage
[30].
On the other
ET AL.
AJR:155,
July 1990
due to other parenchymal processes, such as rejection or pancreatitis, or even to technical difficulties, such as obesity. In one case of proved graft thrombosis, no Doppler signal could be obtained from anywhere along the graft; in another, signals
were
obtained
from
the graft
vessels
in the anasto-
motic region but not from the parenchyma [27]. Two cases of pathologically proved venous thrombosis in nonfunctioning grafts have been reported [26], both of which had no venous Doppler signal in the presence of arterial flow. Studies showing high velocity or turbulence at the arterial or venous anastomoses suggest stenoses. Additionally, Doppler evidence of arterial flow within a perianastomotic fluid collection suggests a complicating pseudoaneurysm [18]. The larger vessels of the transplanted pancreas have been shown on both unenhanced and IV contrast-enhanced CT and are seen easily on MR. However, CT is of little value in assessing vascular patency [1 4]. Patency of the graft vessels is apparent on MR when a prominent flow void is shown, but thrombosis may be difficult to differentiate from slow flow in some instances (Fig. 7A) [31]. The usefulness of MR in the diagnosis of vascular complications has not been explored. Angiography of the transplanted pancreas has been described for small numbers of patients. Arterial irregularities and stenoses, diminished parenchymal opacification, and prolonged circulation of contrast material have been reported in two patients with rejection [32]. These abnormalities were unevenly distributed in one case. Another report [33] of 30
hand, Tc-labeled ABCs are theoretically inferior to “TcDTPA in evaluating edema associated with rejection or pancreatitis because of the nondiffusibility of RBCs.
arteriograms
Doppler sonography is capable of detecting major vascular complications in pancreatic grafts, such as vascular thrombosis, anastomotic strictures, and pseudoaneurysms [i 8]. Doppler identification of arterial and venous flow within the
cific for graft failure, as two of 12 patients with this pattern maintained normoglycemia (Fig. 1 1 D). Only normal arteriograms correlated with normal graft function.
vascular pedicle of the graft, and within the graft parenchyma, indicates that the graft vasculature is patent. Inability to detect arterial or venous flow with Doppler imaging may reflect primary vascular thrombosis (Fig. 13); alternatively, it may be
in duct-occluded
five angiographic rejection.
segmental
patterns,
Nonvisualization
none
allografts
of which
of the graft
vessels
described
correlated was
with
not spe-
Conclusions Pancreas therapeutically,
transplantation, has a relatively
although
increasingly
high complication
effective rate. As the
Fig. 13.-Arterial and venous thrombosis. A, Graft is markedly echogenic and inhomogeneous (straight arrows) on sonogram. Artery supplying graft (curved arrow) is anastomosed to recipient iliac artery. B, Doppler signal in graft artery shows sharp systolic peaks and reversal of diastolic flow (ar. rows) in contrast to normal arterial flow seen 3 days earlier. No Doppler signal could be obtained from graft vasculature 4 days later. Pancreatectomy revealed arterial and venous thrombosis with hemorrhagic necrosis.
AJR:155,
PANCREAS
July 1990
TRANSPLANT
clinical setting is commonly nonspecific, imaging is done to help characterize these complications. Nuclear medicine, so-
Downloaded from www.ajronline.org by 117.253.182.228 on 10/27/15 from IP address 117.253.182.228. Copyright ARRS. For personal use only; all rights reserved
nography,
CT, and MR are all sensitive
in detecting
parenchy-
mal abnormalities and changes in graft size and margination but currently are not capable of detecting rejection early enough in its development to have a meaningful impact on therapy. Some exceptions to this generalization may be evolving; preliminary results suggest that duplex Doppler sonography may be specific in the diagnosis of acute rejection, and, if clinical and imaging findings are ambiguous, a normal MR finding essentially excludes rejection. Sonography,
CT, and MR are all capable
of showing
post-
transplantation fluid. Specific characterization of fluid may be possible in certain instances, but diagnostic aspiration is required to exclude infection. Conventional or CT cystography permits diagnosis of leaks at the duodenal stump or anastomosis. Nuclear medicine, duplex sonography, and, potentially, MR can be used to diagnose vascular thrombosis, with angiography used to confirm suspected thrombosis. Pseudoaneurysms can be shown by using duplex sonographic techniques, but generally angiography is required for preoperative planning. Reports sonography,
evaluating the capabilities CT, MA, and angiography
of nuclear for accurate
medicine, diagnosis
of pancreas transplantation complications are scarce, and the majority share common flaws. Imaging findings usually are correlated with the clinical diagnosis or with histopathologic data from a coexisting renal transplant. Even the second method of diagnosis can be inaccurate, as recent evidence suggests that renal and pancreatic rejection can occur discordantly [22, 34]. Systematic correlation of radiologic findings with histopathologic data has not been possible, in part because safe percutaneous biopsy techniques for pancreas grafts have not been developed. Pathologic data obtained from later surgical resection of an end-stage graft may not reflect the underlying pathologic changes present at an earlier imaging study. Ultimately, delineation of the role of imaging awaits further characterization of the range of normal graft appearances, as well as pathologic correlation with large numbers of dysfunctional grafts.
surveillance
of the allografted
2i
pancreas.
AJR 1988;i
50:811-816
8. Catafau AM, Lome#{241}aFJ, Ricart J, et al. Indium-il 1-labeled platelets in monitoring human pancreatic transplants. J Nucl Med 1989;30: 14701475 9. Yuh WTC, Wiese JA, Abu-YousefMM, etal. Pancreatic transplant imaging. Radiology 1988;i67:679-.683 10. Kuni CC, duCret RP, Boudreau RJ. Pancreas transplants: evaluation using perfusion scintigraphy. AJR 1989;i53:57-6i ii . Letoumeau JG, Maile CW, Sutherland DER, Feinberg SB. tJtrasound and computed tomography in the evaluation of pancreatic transplantation. Radiol Ciln North Am 1987;25:345-355 i2. Maile CW, Crass JR, Frick MP, Feinberg SB, Goldberg ME, Sutherland DER. CT of pancreas transplantation. Invest Radiol i985;20:609-6i2 i3. Patel B, Markivee CR, Mahanta B, vas W, George E, Garvin P. Pancreatic transplantation: scintigraphy, US and CT. Radiology 1988;167:685-687 14. Moulton JS, Munda R, Weiss MA, Lubbers DJ. Pancreatic transplants: CT with clinical and pathologic correlation. Radiology 1989;172:21-26 is. MarinCek B, Schlumpf R, Decurtins M, von Schulthess GK, Largiadbr F. Radiologische diagnostik nach pankreastransplantation. Radiologe 1988; 28: 560-565 16. Rasmussen K, Burcharth F, Thomson HS, Rygaard H. Monitoring of pancreas-graft perfusion by radionuclide and digital subtraction angiography. Diabetes 1989;38(suppl 1):21-23 17. Yuh WTC, Hunsicker LG, 5ato Y, Wright FH Jr, Smith JL, Cony RJ. Application of magnetic resonance imaging in pancreas transplant. Diabetes 1989;38(suppl i):27-29 18. Tobben PJ, Zajko AB, Sumkin JH, et al. Pseudoaneurysms complicating organ transplantation: roles of CT, duplex sonography, and angiography. Radiology 1988;i69:65-70 19. Toledo-Pereyra LH, Zeskind HJ, Mittal vK. (Jtrasound imaging of cliinical pancreatic organ transplants. JCU 1982;10: 12i -124 TN, Glazer GM, Francis IR, et al. MR diagnosis of pancreatic transplant rejection. AJR 1988;150:557-560 Jennerholm 5, Fr#{244}dinL, Hernmingsson A, Johansson G, Tufveson G. Magnetic resonance imaging of kidney and pancreatic transplants. Transplant Proc 1988;20:425-426 Yuh WTC, Hunsicker LG, Nghiem DD, et al. Pancreatic transplants: evaluation with MR imaging. Radiology 1989;1 70:171-177 Crass JR, Sutherland DER, Feinberg SB. Sonography of the segmental human pancreatic transplant. JCU 1982;1 0:149-152 Crass JR. Feinberg SB. Sutherland DER, Loken M, Gedgaudas EG. Radiology of the human segmental pancreatic transplant. Gastrointest Radiol 1982;7: 153-1 58 Schlumpf R, Manncek B, Schulthess Gv, Decurtins M, Largiad#{232}rF. Magnetic resonance imaging and computed tomography in long-term-functioning duct-occluded pancreas allotransplants. Diabetes 1989;38(suppl 1): 24-26 Gilabert R, Fern#{226}ndez-Cruz L, Bru C, Sans A, Andreu J. Duplex-Doppler ultrasonography in monitoring clinical pancreas transplantation. Transpllnt 1988;i :172-i 77 Patel B, Wolverson MK, Mahanta B. Pancreatic transplant rejection: assessment with duplex US. Radiology 1989;173: 13i -135 Woolsey EJ, Tauscher JR, Dafoe DC. Pancreas transplantation with pancreatico-duodeno-cystostomy for exocrine drainage. AJR 1987;149: 507-509 Letoumeau JG, Hunter DW, Crass JG, Thompson WM, Sutherland DER. Percutaneous aspiration and drainage of abdominal fluid collections after pancreatic transplantation. AJR i988;150:805-809 Kuni C, duCret R, Boudreau R. Perfusion scintigraphy in pancreas transplant patients. Presented at the International Congress of Radiology, Paris, July 1989 Zirinsky K, Markisz JA, Rubenstein WA, et al. MR imaging of portal venous thrombosis: correlation with CT and sonography. AJR 1988;i50:283-288 Svahn T, Lewander R, Hardstedt C, Lundgren G, Sundelin P, Groth C-G. Angiography and scintigraphy of human pancreatic allografts. Acta Radiol [Diagnj (Stockh) 1978;19:297-304 lllner W-D, Berger H, StablerA, Abendroth D, Landgraf R, Land W. Puzzling angiographic findings in pancreatic transplantation. Transplant Proc 1989;21 :2803 Sollinger HW, Stratta RJ, D’AlessandroAM, Kalayoglu M, Pirsch JD, Belzer FO. Experience with simultaneous pancreas-kidney transplantation- Ann Surg 1988;208:475-482
20. vahey 21
.
22. 23. 24.
25.
26.
27. 28.
REFERENCES 1 . Sutherland DER , Moudry KC, Najarian JS. Pancreas transplantation. In: Cerilli GJ, ed. Organ transplantation and replacement. Philadelphia: Lippincott, 1988:535-574 2. Hanto Dw, Sutherland DER. Pancreas transplantation: clinical considerations. Radiol Clin North Am i987;25:333-343 3. Moudry-Munns KC, ed. International pancreas transplant registry newsletfor, vol. 2, no. 3. Minneapolis: International Pancreas Transplant Registry, 1989 4. Sutherland DER, Chow SY, Moudry-Munns KC. International transplant registry report-i 988. Clin Transplant 1989;3: 129-1 49 5. Sutherland DER, Dunn DL, Goetz FC, et al. A ten year experience with 290 pancreas transplants at a single institution. Ann Surg 1989;2i0: 274-288 6. Simmons RL, Finch ME, Ascher NL, Najarian JS, eds. Manual of vascular access, organ donation and transplantation. New York: Springer-verlag, 1984:105-164, 237-254 7. George EA, Salimi Z, Camey K, Casta#{241}eda M, Garvin PJ. Radionuclide
IMAGING
29.
30.
31 32.
33.
34.
.
