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AJR 2004; 182:919-925
© American Roentgen Ray Society


Pictorial Essay

Spectrum of Imaging Findings After Pancreas Transplantation with Enteric Exocrine Drainage: Part 2, Posttransplantation Complications

Martin C. Freund1, Wolfgang Steurer2, Eva M. Gassner1, Karin M. Unsinn1, Michael Rieger1, Alfred Koenigsrainer2, Raimund Margreiter2 and Werner R. Jaschke1

1 Department of Radiology, Leopold-Franzens University, Anichstrasse 35, Innsbruck A-6020, Austria.
2 Department of General Surgery and Transplant Surgery, Leopold-Franzens University, Innsbruck A-6020, Austria.

Received May 21, 2003; accepted after revision July 24, 2003.

 
Address correspondence to M. C. Freund (martin.freund{at}uibk.ac.at).


Introduction
Top
Introduction
Imaging Techniques
Imaged Abnormalities
Vascular Graft Complications...
Pancreatic Graft Complications...
Other Transplantation-Associated...
References
 
Pancreas transplantation has emerged as an effective treatment for patients with long-standing type 1 diabetes mellitus resulting in an insulin-independent euglycemic state and normalization of glycosylated hemoglobin levels. In most cases, pancreas transplantation is performed at the same time as kidney transplantation from the same donor as simultaneous pancreas–kidney transplantation in patients with coexisting end-stage diabetic nephropathy, less frequently as sequential pancreas-after-kidney transplantation or pancreas transplantation alone. Various transplantation procedures exist, including transplantation of a whole pancreatic graft with a duodenal segment and enteric exocrine drainage via a duodenojejunostomy and systemic venous endocrine drainage via vascular anastomoses to the iliac vessels. In all modifications of pancreas transplantation, the recipient's own pancreas is left untouched.

Knowledge of the transplantation procedure and postoperative imaging anatomy of the pancreas allograft are basic requirements for radiologists. Graft survival, among other factors, corresponds to early diagnosis and therapy for specific graft-related complications including thrombosis, leakage of enteric anastomosis, hematoma, abscess, pancreatitis, pseudocyst formation, rejection, and posttransplantation lymphoproliferative disorder.

This pictorial essay uses various imaging techniques to show the imaging spectrum of diseases after pancreas transplantation with systemic venous endocrine and enteric exocrine drainage.


Imaging Techniques
Top
Introduction
Imaging Techniques
Imaged Abnormalities
Vascular Graft Complications...
Pancreatic Graft Complications...
Other Transplantation-Associated...
References
 
Various imaging techniques are routinely used to detect early and late posttransplantation complications. In contrast to imaging of other solid organ transplants—for instance, liver and kidney—imaging of the pancreas allograft with sonography and color-coded sonography is hampered by superposition of intestinal gas. This results from the heterotopic position of the graft in the right pelvis adjacent to the iliac vessels and surrounded by air-filled intestinal loops. For this reason, complete evaluation of the vascular and enteric anastomoses as well as the parenchyma of the pancreatic graft can be best accomplished by contrast-enhanced helical CT [1]. Additionally, contrast-enhanced MDCT enables 3D reconstruction of the vascular anatomy with respect to neighboring anatomic structures. MRI without contrast application [2], with static [3], and especially with dynamic [4] contrast enhancement enables better evaluation of the pancreatic parenchymal graft. However, MR angiography is inferior to CT angiography because of its limited spatial resolution. Moreover, evaluation of the enteric anastomosis on MRI is difficult. Additionally, renal function also determines the selection of an appropriate cross-sectional imaging technique after simultaneous pancreas–kidney transplantation. In cases of decreased renal function, contrast-enhanced MRI and unenhanced CT represent the preferred examination to preserve the renal graft. MR pancreatography is a complementary examination for detection of duct abnormalities. Catheter angiography is used to confirm vascular complications while permitting immediate endovascular therapy. Other imaging-guided interventions are used to percutaneously treat localized fluid collections, such as seromas, hematomas, and abscesses. Occasionally, small-bowel follow-up studies are performed to detect complications of the enteral anastomosis.


Imaged Abnormalities
Top
Introduction
Imaging Techniques
Imaged Abnormalities
Vascular Graft Complications...
Pancreatic Graft Complications...
Other Transplantation-Associated...
References
 
The following complications after pancreas transplantation with enteric anatomosis can be observed: vascular graft complications, including rejection; pancreatic graft complications, including infection; and other transplantation-associated complications.


Vascular Graft Complications Including Rejection
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Introduction
Imaging Techniques
Imaged Abnormalities
Vascular Graft Complications...
Pancreatic Graft Complications...
Other Transplantation-Associated...
References
 
The most serious vascular complication is venous and arterial graft thrombosis and results in pancreatic graft necrosis and pancreatectomy in most cases. Typically, contrast-enhanced CT displays an intraluminal filling defect in the larger graft veins (Fig. 1A, 1B). Arterial thrombosis results in complete occlusion of the vessel with nonenhancement of the parenchymal graft indicating graft necrosis (Fig. 2A, 2B). Further progression can result in an emphysematous transformation of the pancreatic graft; in a patient without clinical signs of local infection or sepsis, this is described as an innocuous gas collection in the pancreatic graft [5]. Imaging-guided biopsy represents the only definite test to distinguish an infected from noninfected pancreatic graft with gas collection (Fig. 3). Risk factors for early graft loss due to arterial occlusion after pancreas transplantation are mainly posed by technical complications involving back-table preparation or the vascular anastomosis in the recipient. In the later course, graft loss due to arterial occlusion represents the end point of graft rejection due to alloimmune vasculitis, resulting in occlusion of small vessels, progressing to larger vessels, and finally involving the donor's anastomosed greater vessels [4]. For this reason, dynamic contrast-enhanced MRI appears to be a promising means of assessing parenchymal enhancement to detect early changes of vascular rejection [4]; other MRI protocols or other imaging techniques, including sonography, color-coded sonography, and contrast-enhanced CT, did not meet expectations. However, considering the absence of reliable clinical markers and the persistent uncertainty regarding imaging examinations, imaging-guided biopsy of the pancreatic graft (Fig. 4) still represents the gold standard for the diagnosis of graft rejection [6].



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Fig. 1A. 43-year-old woman with abdominal discomfort 12 days after simultaneous pancreas–kidney transplantation. Contrast-enhanced MDCT scans show acute thrombosis of superior mesenteric vein (arrowheads) and splenic vein (arrowhead) but homogeneous contrast enhancement of pancreatic graft (arrow, B) with donor's duodenum (arrows, A) and renal graft (asterisk). d = donor's, r = right, l = left, CIA = common iliac artery, CIV = common iliac vein, SA = splenic artery, IPDA = inferior pancreaticoduodenal artery, SMA = superior mesenteric artery.

 


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Fig. 1B. 43-year-old woman with abdominal discomfort 12 days after simultaneous pancreas–kidney transplantation. Contrast-enhanced MDCT scans show acute thrombosis of superior mesenteric vein (arrowheads) and splenic vein (arrowhead) but homogeneous contrast enhancement of pancreatic graft (arrow, B) with donor's duodenum (arrows, A) and renal graft (asterisk). d = donor's, r = right, l = left, CIA = common iliac artery, CIV = common iliac vein, SA = splenic artery, IPDA = inferior pancreaticoduodenal artery, SMA = superior mesenteric artery.

 


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Fig. 2A. 36-year-old woman 8 months after pancreas transplantation alone with newly developed hyperglycemia, graft necrosis, and subsequent graft pancreatectomy. Contrast-enhanced MDCT scan obtained during dominant arterial phase shows enhancement of donor's arterial conduit (arrowhead) but nonvisualization of graft arteries and nonenhancement of pancreas graft (arrow) indicating arterial occlusion and absent parenchymal perfusion. r = right, l = left, CIA = common iliac artery.

 


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Fig. 2B. 36-year-old woman 8 months after pancreas transplantation alone with newly developed hyperglycemia, graft necrosis, and subsequent graft pancreatectomy. Angiogram verifying CT findings shows residual enhancement of donor's arterial conduit (arrowhead) but nonvisualization of graft arteries and absent parenchymal enhancement of pancreatic graft.

 


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Fig. 3. 44-year-old man 9 months after simultaneous pancreas–kidney transplantation with graft necrosis but without local infection or sepsis and subsequent graft extirpation. Contrast-enhanced MDCT scan shows absent parenchymal enhancement and emphysematous transformation of pancreatic graft (arrows) consistent with innocuous gas collection. Note renal graft (black asterisk) and ascites (white asterisk).

 


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Fig. 4. 33-year-old man 20 months after simultaneous pancreas–kidney transplantation with pancreatic graft dysfunction and acute rejection verified by histopathologic examination. Helical CT scan is used for image-guided percutaneous biopsy (double arrows) of pancreatic graft (single arrows) adjacent to contrast medium–filled small bowel (arrowhead) and renal graft (asterisk).

 


Pancreatic Graft Complications Including Infection
Top
Introduction
Imaging Techniques
Imaged Abnormalities
Vascular Graft Complications...
Pancreatic Graft Complications...
Other Transplantation-Associated...
References
 
Complications of the pancreatic graft itself are an important cause of morbidity in the early posttransplantation period. These complications include pancreatitis; pseudocyst formation, including expansion; infection with abscess formation; pseudoaneurysm formation; leakage of the enteric anastomosis or duodenal stump; and small-bowel obstruction. Self-limited edematous pancreatitis (Fig. 5A, 5B) occurs preferentially in the early posttransplantation period because of reperfusion injury and typically involves the entire graft. Focal edematous swelling of the donor's remaining mesenteric fat attached to the superior mesenteric arterial stump should not be misdiagnosed as focal edematous pancreatitis (Fig. 6); presumably this condition results from ligation of the donor's lymphatic vessels. Necrotizing pancreatitis is the most severe form of pancreatitis (Fig. 7) and necessitates graft pancreatectomy. Pseudocyst formation develops later in the clinical course after onset of graft pancreatitis and can occur in various sizes, contours, and septa inside or outside the pancreatic graft. Sonography is the imaging technique of choice for large pseudocysts (Fig. 8), whereas complex pseudocysts (Fig. 9), infected pseudocysts (Fig. 10A), and percutaneous catheter drainage of pseudocysts (Fig. 10B) are best imaged on contrast-enhanced CT [7]. Infection of pseudocysts after pancreas transplantation is a frequent occurrence and can cause pseudoaneurysm formation in arteries (Fig. 11A, 11B, 11C, 11D) and veins [8]. Finally, fistula formation can result from pancreatitis with communication to the skin (Fig. 10C) or peritoneal cavity (Fig. 12), and sinus tract formation can involve the retroperitoneum (Figs. 12 and 13A, 13B) and gut (Fig. 13A, 13B).



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Fig. 5A. 40-year-old man 16 days after simultaneous pancreas–kidney transplantation and graft pancreatitis. Donor's duodenum (arrowhead), renal graft (black asterisk), and perirenal fluid (white asterisk) are seen. Contrast-enhanced MDCT scan shows homogeneous contrast enhancement of pancreatic graft (arrows).

 


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Fig. 5B. 40-year-old man 16 days after simultaneous pancreas–kidney transplantation and graft pancreatitis. Donor's duodenum (arrowhead), renal graft (black asterisk), and perirenal fluid (white asterisk) are seen. Contrast-enhanced MDCT scan obtained 5 days after initial CT shows inhomogeneous contrast enhancement and increasing size of pancreatic graft (arrows) indicating edematous pancreatitis.

 


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Fig. 6. 51-year-old man 4 weeks after simultaneous pancreas–kidney transplantation. Contrast-enhanced MDCT scan shows edematous swelling of donor's remaining mesenteric fat (double arrows) and lymph nodes (white asterisks) attached to unremarkable, homogeneous contrast-enhancing pancreatic graft (single arrow). Condition presumably results from ligation of donor's lymphatic vessels. CT also shows normal enhancement of donor's (d) vessels including superior mesenteric artery (SMA), external iliac artery (EIA), splenic artery (SA), and renal graft (black asterisk).

 


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Fig. 7. 38-year-old man 5 weeks after simultaneous pancreas–kidney transplantation with necrotizing graft pancreatitis and subsequent graft extirpation. Contrast-enhanced helical CT scan displays remnants of contrast-enhanced pancreatic graft (arrow) surrounded by fluid and thin-walled membrane (arrowheads) representing pseudocyst formation due to necrotizing pancreatitis. Ascites (white asterisk) and renal graft (black asterisk) are also seen.

 


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Fig. 8. 54-year-old man 5 months after simultaneous pancreas–kidney transplantation with graft pancreatitis and pseudocyst formation. Sonogram shows large, partly septated cyst (white asterisk) adjacent to pancreatic graft (not shown) consistent with peripancreatic pseudocyst.

 


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Fig. 9. 34-year-old woman 5 months after simultaneous pancreas–kidney transplantation with exudative pancreatitis and pseudocyst formation. Contrast-enhanced helical CT scan displays homogeneous enhancement of small pancreatic graft (arrow) surrounded by thin-walled peripancreatic pseudocyst (arrowheads) and various intraabdominal pseudocysts (white asterisks). Note renal graft (black asterisk). d = donor's, SMA = superior mesenteric artery, SMV = superior mesenteric vein, CIA = common iliac artery.

 


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Fig. 10A. 27-year-old man 4 weeks after simultaneous pancreas–kidney transplantation with infected peripancreatic pseudocyst requiring percutaneous drainage and subsequent development of pancreatocutaneous fistula. Contrast-enhanced helical CT scan shows homogeneous contrast enhancement of pancreatic graft (arrow) surrounded by septate, peripancreatic fluid collection (white asterisks) combined with air–fluid level (white arrowheads) and thin, contrast-enhanced wall (black arrowheads) consistent with infected pseudocyst. Note renal graft (black asterisk).

 


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Fig. 10B. 27-year-old man 4 weeks after simultaneous pancreas–kidney transplantation with infected peripancreatic pseudocyst requiring percutaneous drainage and subsequent development of pancreatocutaneous fistula. Contrast-enhanced helical CT scan obtained during performance of subsequent CT-guided percutaneous drainage with pigtail catheter (double arrows) for treatment of infected peripancreatic pseudocyst shows pancreatic graft (single arrow) and renal graft (asterisk).

 


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Fig. 11A. 50-year-old man 18 days after simultaneous pancreas–kidney transplantation and 5 days after pancreatic graft extirpation due to infected graft pancreatitis with localized retroperitoneal and intraabdominal abscesses and subsequent surgical arterial repair of symptomatic mycotic pseudoaneurysm. Contrast-enhanced helical CT shows residual donor's arterial conduit (arrow) after pancreatic graft extirpation surrounded by small fluid collection with thin-walled contrast-enhanced membrane (arrowhead). Also residual fluid collection (white asterisk) in perirenal location is seen. Note renal graft (black asterisk). r = right, l = left, CIA = common iliac artery, CIV = common iliac vein.

 


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Fig. 11B. 50-year-old man 18 days after simultaneous pancreas–kidney transplantation and 5 days after pancreatic graft extirpation due to infected graft pancreatitis with localized retroperitoneal and intraabdominal abscesses and subsequent surgical arterial repair of symptomatic mycotic pseudoaneurysm. Contrast-enhanced MDCT scan with dominant late parenchymal phase obtained 9 days after initial CT shows donor's residual arterial conduit (arrow) and newly developed emphysematous transformation (arrowhead) of adjacent fluid collection, indicating recurrent abscess. Decrease in fluid (white asterisk) adjacent to renal graft (black asterisk) is noted.

 


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Fig. 11C. 50-year-old man 18 days after simultaneous pancreas–kidney transplantation and 5 days after pancreatic graft extirpation due to infected graft pancreatitis with localized retroperitoneal and intraabdominal abscesses and subsequent surgical arterial repair of symptomatic mycotic pseudoaneurysm. Contrast-enhanced MDCT scans obtained 12 days after initial CT show newly developed mycotic pseudoaneurysm (double arrows) originating from donor's arterial conduit (arrow, C) and recently developed large retroperitoneal hematoma (arrowheads). Note renal graft (black asterisk).

 


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Fig. 11D. 50-year-old man 18 days after simultaneous pancreas–kidney transplantation and 5 days after pancreatic graft extirpation due to infected graft pancreatitis with localized retroperitoneal and intraabdominal abscesses and subsequent surgical arterial repair of symptomatic mycotic pseudoaneurysm. Contrast-enhanced MDCT scans obtained 12 days after initial CT show newly developed mycotic pseudoaneurysm (double arrows) originating from donor's arterial conduit (arrow, C) and recently developed large retroperitoneal hematoma (arrowheads). Note renal graft (black asterisk).

 


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Fig. 10C. 27-year-old man 4 weeks after simultaneous pancreas–kidney transplantation with infected peripancreatic pseudocyst requiring percutaneous drainage and subsequent development of pancreatocutaneous fistula. Contrast-enhanced helical CT scan obtained 10 weeks after initial CT-guided percutaneous drainage and ultimate operative débridement of recurrently infected pseudocyst shows pancreatic–cutaneous fistula (arrowheads) originating from pancreatic graft (arrow). Note renal graft (asterisk).

 


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Fig. 12. 29-year-old man 3 weeks after simultaneous pancreas–kidney transplantation with infected peripancreatic pseudocyst and complex pancreatic cutaneous fistula. Drainage catheter (double arrows) was placed through cutaneous fistula opening, and sinogram displays large central cavity (single arrow) with communication to peritoneal cavity (black arrowheads) and sinus tracts (white arrowheads) in retroperitoneal location.

 


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Fig. 13A. 43-year-old man 10 weeks after simultaneous pancreas–kidney transplantation complicated by pancreatitis, infection of peripancreatic pseudocyst, and subsequent surgical débridement and drainage tube placement. Spot film image obtained during small-bowel follow-through examination shows contrast-filled small-bowel loops (SB), cecum (arrowheads), and two partly contrast-filled sinus tracts (arrows) opening to cecum.

 


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Fig. 13B. 43-year-old man 10 weeks after simultaneous pancreas–kidney transplantation complicated by pancreatitis, infection of peripancreatic pseudocyst, and subsequent surgical débridement and drainage tube placement. Contrast-enhanced helical CT scan confirms retroperitoneal location of partly contrast-filled sinus tracts (white arrows) adjacent to cecum (arrowheads) and pancreatic graft (black arrow), indicating previously existing pancreatocolic fistula. Note renal graft (asterisk).

 

Enteric complications manifest either as leakage of the duodenojejunostomy or duodenal stump with ensuing abscess and peritonitis or sometimes as volvulus of the small bowel around the longitudinal axis of the graft (Fig. 14A, 14B).



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Fig. 14A. 39-year-old woman 14 days after simultaneous pancreas–kidney transplantation with clinical signs of upper intestinal obstruction due to intermittent small-bowel volvulus and subsequent surgical reduction. Contrast-enhanced MDCT scan shows prestenotic, dilated, fluid-filled loops of small bowel (white asterisks), twisted segment of small bowel (between single white arrow and white arrowhead) consisting of collapsed loop of small intestine located adjacent to donor's duodenum (double black arrows) with hyperdense staple line (black arrowhead), and poststenotic, nondilated colon (black asterisks) filled with intraluminal contrast material from prior unremarkable small-bowel follow-through examination.

 


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Fig. 14B. 39-year-old woman 14 days after simultaneous pancreas–kidney transplantation with clinical signs of upper intestinal obstruction due to intermittent small-bowel volvulus and subsequent surgical reduction. Upright abdominal radiograph obtained after repeated small-bowel follow-through examination with water-soluble contrast material verifies mechanical small-bowel obstruction at level of presumed location of head of pancreatic graft (between arrow and arrowhead) with dilatation and abnormal air–fluid levels of partly contrast-filled, prestenotic, small intestinal loops (asterisks), including stomach.

 


Other Transplantation-Associated Complications
Top
Introduction
Imaging Techniques
Imaged Abnormalities
Vascular Graft Complications...
Pancreatic Graft Complications...
Other Transplantation-Associated...
References
 
Pseudothrombosis of the iliac vein (Fig. 15) has been described after simultaneous pancreas–kidney transplantation with bilateral revascularization to the respective iliac vessels [9]. Pseudothrombosis results from delayed venous opacification of the iliac vein ipsilateral to the pancreatic graft as compared with the contralateral side of the renal graft. This phenomenon results from longer transit time and reduced blood flow to the pancreas as compared with the kidney. Pseudothrombosis can also involve the ipsilateral iliac vein below the vascular anastomoses of the pancreatic graft because of more peripheral implantation of the renal graft on the contralateral side and longer transit time of the lower extremity as compared with the renal graft. Posttransplantation lymphoproliferative disorder is a serious but rare complication of pancreas transplantation. It manifests predominantly as a diffuse enlargement of the pancreatic graft, which is indistinguishable from acute pancreatitis for imaging techniques, or rarely as intra- or extraallograft focal masses, lymphadenopathy, or organomegaly [10].



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Fig. 15. 54-year-old man 9 months after simultaneous pancreas–kidney transplantation. Contrast-enhanced MDCT scan shows pseudothrombosis (double arrows) of right external iliac vein (EIV) as compared with left side. This is due to delayed venous opacification on right side resulting from longer transit time and reduced blood flow of right-sided pancreatic graft (single arrow) as compared with left-sided renal graft as well as more peripheral implantation of renal graft and longer transit time of the lower extremity as compared with renal graft. Homogeneous contrast enhancement of pancreatic graft and ascites (white asterisks) is seen. r = right, l = left, d = donor's, EIA = external iliac artery, SA = splenic artery, SV = splenic vein.

 


References
Top
Introduction
Imaging Techniques
Imaged Abnormalities
Vascular Graft Complications...
Pancreatic Graft Complications...
Other Transplantation-Associated...
References
 

  1. Dachman AH, Newmark GM, Thistlethwaite JR Jr, Oto A, Bruce DS, Newell KA. Imaging of pancreatic transplantation using portal venous and enteric exocrine drainage. AJR1998; 171:157 –163[Abstract/Free Full Text]
  2. Vahey TN, Glazer GM, Francis IR, et al. MR diagnosis of pancreatic transplant rejection. AJR 1988;150 : 557–560[Abstract/Free Full Text]
  3. Fernandez MP, Bernadino ME, Neylan JF, Olson RA. Diagnosis of pancreatic transplant dysfunction: value of gadopentetate dimeglumine-enhanced MR imaging. AJR1991; 156:1171 –1176[Abstract/Free Full Text]
  4. Krebs TL, Daly B, Wong-You-Cheong JJ, Carrol K, Bartlett ST. Acute pancreatic transplant rejection: evaluation with dynamic contrast-enhanced MR imaging compared with histopathologic analysis. Radiology1999; 210:437 –442[Abstract/Free Full Text]
  5. Vas W, Patel B, Mahanta B, Salimi Z, Markivee C, Garvin P. Innocuous gas collections in pancreatic allografts demonstrated by computed tomography. Gastrointest Radiol1989; 14:118 –122[Medline]
  6. Lee BC, McGahan JP, Perez RV, Boone JM. The role of percutaneous biopsy in detection of pancreatic transplant rejection. Clin Transplant 2000; 14:493 –498[Medline]
  7. Patel BK, Garvin PJ, Aridge DL, Chenoweth JL, Markivee CR. Fluid collections developing after pancreatic transplantation: radiologic evaluation and intervention. Radiology1991; 181:215 –220[Abstract/Free Full Text]
  8. Tan M, Di Carlo A, Stein LA, Cantarovich M, Tchervenkov J, Metrakos P. Pseudoaneurysm of the superior mesenteric artery after pancreas transplantation treated by endovascular stenting. Transplantation2001; 72:336 –338[Medline]
  9. Gupta R, Rottenberg G, Taylor J. Pseudothrombosis of the iliac vein in patients following combined kidney and pancreas transplantation. Br J Radiol2002; 75:692 –694[Abstract/Free Full Text]
  10. Meador TL, Krebs TL, Cheong JJ, Daly B, Keay S, Bartlett S. Imaging features of posttransplantation lymphoproliferative disorder in pancreas transplant recipients. AJR2000; 174;121 –124[Abstract/Free Full Text]

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C. G. Lall, K. Sandrasegaran, D. T. Maglinte, and J. A. Fridell
Bowel complications seen on CT after pancreas transplantation with enteric drainage.
Am. J. Roentgenol., November 1, 2006; 187(5): 1288 - 1295.
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