Journal of Medical Imaging and Radiation Oncology

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1 Journal of Medical Imaging and Radiation Oncology 62 (2018) MEDICAL IMAGING PICTORIAL ESSAY Imaging in pancreas transplantation complications: Temporal classification Paula Gallego Ferrero and Juan Crespo Del Pozo Department of Radiology, Hospital Universitario Marques de Valdecilla, Santander, Spain P Gallego Ferrero MD; J Crespo Del Pozo MD, PhD. Correspondence Dr Paula Gallego Ferrero, Department of Radiology, Hospital Universitario Marques de Valdecilla, Avda. Valdecilla n 25, Santander, Spain. paulagallegof@yahoo.es Conflict of interest: None. Submitted 17 February 2018; accepted 19 April doi: / Introduction The first pancreas transplantation was performed in the University of Minnesota (USA) in 1966, 1 and since then it has been a successful treatment for diabetes mellitus and advanced diabetic nephropathy. Surgical techniques The pancreas is harvested together with the duodenum and vascular support from the donor and it is usually placed in the right lower quadrant or pelvis of the recipient. The arterial Y graft consists of the donor common, internal and external iliac arteries, and the following anastomoses are performed: the donor superior mesenteric artery is attached to the donor external iliac artery (to supply the head of the pancreas) and the donor splenic artery is attached to the donor internal iliac artery (to supply the body and tail of the pancreas). The common iliac artery is anastomosed to the recipient common or external iliac artery. The donor portal vein drains the donor splenic and superior mesenteric veins, and it can be anastomosed to the recipient superior mesenteric vein in portal venous drainage or to the recipient iliac vein in systemic venous drainage. 2 There are three main types of Summary Pancreatic transplantation is a therapeutic option for both poorly controlled cases of diabetes mellitus and patients with advanced diabetic nephropathy. It is important for radiologists to know the different surgical techniques as well as the typical radiological appearance after pancreatic transplantation, in order to accurately identify the complications. These complications can be classified according to the period of time after the transplantation in which they typically occur: immediate (first 24 hours), early (24 72 hours), intermediate (72 hours to weeks) and late (months). An accurate and early diagnosis of pancreas transplantation complications is essential to start the adequate treatment and increase the chances of graft survival. Key words: diagnostic imaging; graft survival; pancreas transplantation; postoperative complications; time factors. pancreas transplantations depending on the type of drainage (Fig. 1): systemic venous and bladder exocrine drainage, systemic venous and enteric exocrine drainage, and portal venous and enteric exocrine drainage. Normal post-operative imaging appearance The radiological evaluation of the pancreas grafts is usually performed using different imaging techniques, depending on the time lapse after the surgery and the complication suspected. 3 Ultrasound is normally performed in the first 24 hours, and a normal pancreas graft has a homogeneous echotexture, lower than the mesenteric fat. With the colour and power Doppler ultrasonography (US), we can visualize the arterial and venous supply. Arterial waveforms normally show a rapid systolic upstroke and continuous diastolic blood flow, while venous waveforms show a monophasic flow (Fig. 2). If clinicians suspect fluid collections or bowel complications, computed tomography (CT) is performed. Now, we are going to describe the radiologic features of pancreas transplantation complications, classified according to the period of time in which they typically appear: Journal of Medical Imaging and Radiation Oncology 504

2 Pancreas transplant complications Immediate complications (<24 hours) Hyperacute graft rejection It occurs right after the surgery and is caused by the presence of cytotoxic antibodies in the recipient s blood. The US findings are non-specific: graft enlargement and increased parenchymal heterogeneity, also seen in acute pancreatitis and ischemia (Fig. 3). 2 Haemorrhage On US, the typical findings are free fluid, fluid collections with internal echoes and fluid fluid level. On unenhanced CT studies, we can visualize high-attenuation intraperitoneal free fluid or collections, with a fluid fluid level (Fig. 4). If we visualize extravasation of contrast in a contrastenhanced-ct, it means there is active bleeding (Fig. 5). Arterial complications Graft arterial thrombosis is the most severe vascular complication that often results in graft dysfunction and failure. 4 Although it is a typical immediate complication, it can occur within the first 3 months following transplantation. 5 The ultrasound findings are tardus parvus waveforms of the intrapancreatic arteries, absent arterial signal in the Y graft (Fig. 6), parenchymal heterogeneity and enlargement and of the graft without colour Doppler flow in pancreatic infarction. 6 On CT, we can visualize intraluminal filling defects in the graft vessels and a nonenhancing pancreas (Fig. 7). If it progresses to parenchymal necrosis, we can find emphysematous changes. An early diagnosis is very important, because an immediate thrombectomy may be successful. Early complications (24 72 hours) Fig. 1. (a) Pancreas transplantations surgical technique with systemic venous and bladder exocrine drainage. The graft vein and the recipient external iliac vein are attached together for systemic venous drainage. And the pancreatic ductal secretions drain into the duodenal stump, which is anastomosed to the bladder. (b) Pancreas transplantations surgical technique with systemic venous and enteric exocrine drainage. The graft vein and the recipient external iliac vein are attached together for systemic venous drainage, and the pancreatic duct drains into the duodenal stump, which is anastomosed to the jejunum, for the exocrine drainage. Bowel drainage emerged as a more physiologic alternative to bladder drainage to drain the pancreatic duodenal secretions into the small bowel. (c) Pancreas transplantations surgical technique with portal venous and enteric exocrine drainage. The graft vein and the recipient superior mesenteric vein are attached together for portal venous drainage, and the pancreatic duct drains into the duodenal stump, which is anastomosed to the jejunum, for the exocrine drainage. This technique combined bowel drainage of the pancreatic ductal secretions with portal venous delivery of insulin. Venous thrombosis Venous thrombosis is much more common that arterial thrombosis and it is the second most common cause of graft failure after rejection. 2,7 The ultrasound findings of venous thrombosis are the absence of venous flow and a high resistance arterial waveform, with reversed diastolic flow. 8 On an unenhanced CT, we may see the venous thrombus as a high-attenuation portal vein or splenic vein, and after the administration of intravenous contrast the thrombus is visualized as a filling defect 9 (Fig. 8). Graft pancreatitis A mild pancreatitis is commonly seen after surgery due to reperfusion injury, 3 and it usually is self-limited. With US and CT, the graft may show non-specific enlargement and 505

3 P Gallego Ferrero and J Crespo Del Pozo Fig. 2. Normal ultrasound appearance of a pancreas transplant. (a) Grey-scale US of a normal pancreas graft with an homogeneous echotexture, lower than the surrounding mesenteric fat. (b) Colour and power Doppler US where we can visualize the vascularity of the graft. (c) Normal arterial waveforms show a rapid systolic upstroke and continuous diastolic blood flow. (d) Normal venous waveforms are monophasic. Fig. 3. (a) Grey-scale US image of a 63-year-old man less than 24 hours after pancreas kidney transplantation, where we visualize non-specific findings of pancreatic graft enlargement and parenchymal heterogeneity (white arrow). Hyperacute graft rejection was suspected. (b,c) Ultrasound and non-enhanced CT performed 2 days later where we cannot identify clearly the pancreatic graft, as it has become a heterogeneous collection (white arrows). The pancreatic graft had to be removed afterwards. 506

4 Pancreas transplant complications thick wall and sometimes intralesional gas (Fig. 11). In up to 30% of patients, abscesses are associated with enteric leakage. 10 Apotentialpitfallexistswhenwevisualizeafluid collection adjacent to the head of the pancreas, because it may be associated with a distended duodenal bulb. 2,7 Colonic infections may occur related to antibiotic therapy and to the immunocompromised state of the patient. CT findings are colonic wall thickening with increased parietal contrast enhancement 3 (Fig. 12). Anastomotic leakage Fig. 4. Axial contrast-enhanced-ct image of a 36-year-old woman less than 24 hours after pancreas kidney transplantation, presenting a hyperdense collection in the abdominal wall, with a fluid fluid level (arrow). The diagnosis is a haematoma with acute bleeding. heterogeneity with adjacent fat stranding and fluid collections (Fig. 9). It is very important to look for possible complications, such as pseudocyst (Fig. 9), thrombosis, abscess or fistula formation, or pancreatic infarction and necrosis. 3 Intermediate complications (72 hour to weeks) Small bowel obstruction Intestinal adhesions are the most common cause of small bowel obstruction after abdominal surgery. 2 The typical findings are proximal dilated bowel (Fig. 10), a discrete transition point and non-dilated distal bowel. Infection Intra-abdominal fluid collections are the most common complication after surgery, and they could represent abscess, seroma, haematoma, lymphocele, urinoma or pseudocyst. Abscesses are complex fluid collections, with a Most bowel perforations and leaks typically occur at the enteric anastomosis and are secondary to dehiscence of the sutures. 11 We can visualize the leakage directly on a CT as an extravasation of orally administered contrast agent and the consequences of the leakage, such as peritonitis (Fig 13). Late complications (months) Graft rejection Graft rejection is the main cause of graft loss. The first imaging technique performed is US, but the US findings are not specific (graft enlargement and increased parenchymal heterogeneity) (Fig. 14). These findings may also be seen in acute pancreatitis and ischemia. Contrast-enhanced CT findings are also non-specific, showing heterogeneous or decreased parenchymal enhancement, with peripancreatic fluid and duodenal oedema. The only reliable test to diagnose graft rejection is graft biopsy. 2 Post-transplantation lymphoproliferative disease Post-transplantation lymphoproliferative disease (PTLD) is a rare late complication, and it can range from benign lymphoid hyperplasia to aggressive B-cell lymphoma. Most cases are related to primary Epstein virus Fig. 5. Axial contrast-enhanced-ct images (a): Arterial phase image, (b): Portal phase image of a 40-year-old woman less than 24 hours after pancreas kidney transplantation. Next to the pancreatic graft (black arrows) we can visualize a high-attenuation collection (white asterisks) associated with extravasation of contrast (white arrows) that increases in size on the portal phase image (b), consistent with active bleeding. 507

5 P Gallego Ferrero and J Crespo Del Pozo Fig. 6. Graft arterial thrombosis in a 37-year-old man one month after pancreas kidney transplantation. US image (a) of a thrombosis in the superior mesenteric artery (black arrow). Colour Doppler US (b) suggests no flow within the artery (white arrow). The axial contrast-enhanced-ct reconstructions in craniocaudal sequence (c e) confirm an intraluminal filling defect (black arrow in image e) inside the superior mesenteric artery (white arrows in images c and d). This patient had thrombosis in both the superior mesenteric artery and vein, as visualized in Figure 8. Fig. 7. Axial and coronal contrast-enhanced-ct images of a 38-year-old man less than 24 hours after pancreas kidney transplantation, where we visualize a splenic artery intraluminal filling defect (arrows) and a non-enhancing pancreas (asterisk), findings in keeping with splenic artery thrombosis. infection. 2 PTLD radiological findings include diffuse non-specific graft enlargement (Fig. 15), focal masses, inside or outside the graft, lymphadenopathy and other organomegaly. Conclusion An accurate and early diagnosis of pancreas transplantation complications is essential to start the adequate 508

6 Pancreas transplant complications Fig. 8. Graft venous thrombosis in a 37-year-old man one month after pancreas kidney transplantation. US image of a thrombosis in the superior mesenteric vein (white arrow in image a) with the absence of venous flow (white arrow in image b) in colour Doppler US. The superior mesenteric vein thrombosis is confirmed on a contrast-enhanced-ct (c and d), where the thrombus (white arrows) is visualized as a filling defect in the superior mesenteric vein. This patient had thrombosis in both the superior mesenteric artery and vein, as visualized in Figure 6. Fig. 9. Graft pancreatitis in a 47 year-old woman 2 days after pancreas kidney transplantation. Axial contrast-enhanced-ct image (a) of an enlarged and heterogeneous graft (large arrow) associated with peripancreatic free fluid (arrow) that correlates with the US image (b) showing enlargement and heterogeneity of the graft (asterisk). Axial contrast-enhanced-ct image obtained 6 months later (c), where we can visualize a pancreatic pseudocyst (arrow) as a fluid collection inside the pancreatic graft (asterisk), one of the complications of graft pancreatitis. Fig. 10. Axial and coronal contrast-enhanced-ct images of a 38 year-old woman one month after pancreas kidney transplantation. We can visualize proximal dilated small bowel loops (white asterisks) in keeping with small bowel obstruction. It is probably caused by the presence of intestinal adhesions in the area of the duodenal stump, which is more dilated (black asterisk), next to the pancreatic graft (black arrows). 509

7 P Gallego Ferrero and J Crespo Del Pozo Fig. 11. Axial and coronal contrast-enhanced-ct images of a 36-year-old woman 10 days after pancreas kidney transplantation. There is a retroperitoneum collection that extends through the psoas muscle with thick enhancing walls (asterisk) and air bubbles within the collection (arrow). This is the typical image of an abscess. Fig. 12. Coronal and axial contrast-enhanced-ct images of 45-year-old man 6 weeks after pancreas kidney transplantation. The radiological features visualized in this study are colonic wall thickening (white arrows) and increased mucosal contrast enhancement (black arrows), findings in keeping with colitis. Fig. 13. Axial and coronal contrast-enhanced-ct images of 32-year-old man 21 days after pancreas kidney transplantation (image a), where we can visualize directly an extravasation of orally administered contrast agent (arrow) in keeping with an anastomotic leakage at the duodenoenterostomy site, as well as one of the complications related to an anastomotic leakage, which is an abscess with gas (asterisks). Another of the complications related to an anastomotic leakage is peritonitis (image b), where we can visualize free intraperitoneal fluid (white asterisks), diffuse thickening and enhancement of the peritoneal lining (black arrows) and signs of enteritis with small bowel wall thickening (white arrows). 510

8 Pancreas transplant complications Fig. 14. US images of a 28 year-old man 1 year after pancreas transplantation, where we visualize a heterogeneous and hypoechoic pancreatic graft (arrows), suggestive of parenchymal fibrosis in a case of chronic rejection, confirmed after biopsy. Fig. 15. US image of diffuse graft enlargement (arrows), visualized in a patient whose pancreatic graft was biopsied with a result suggestive of lymphoproliferative disease. treatment and increase the chances of graft survival. It is an important and useful tool to know which complication to suspect in each phase of the post-transplantation period. Acknowledgements We thank Gonzalez Sanchez FJ, MD, Pellon Daben R, MD, Acebo Garcıa MM, MD and Sanchez Bernal S, MD for providing cases for this pictorial essay. References 1. Squifflet JP, Gruessner RW, Sutherland DE. The history of pancreas transplantation: past, present and future. Acta Chir Belg 2008; 108: Vandermeer FQ, Manning MA, Frazier AA et al. Imaging of whole-organ pancreas transplants. Radiographics 2012; 32: Francßa M, Certo M, Martins L et al. Imaging of pancreas transplantation and its complications. Insights Imaging 2010; 1: Hampson FA, Freeman SJ, Ertner J et al. Pancreatic transplantation: surgical technique, normal radiological appearances and complications. Insights Imaging 2010; 1: Low G, Crockett AM, Leung K et al. Imaging of vascular complications and their consequences following transplantation in the abdomen. Radiographics 2013; 33: O 0 Malley RB, Moshiri M, Osman S et al. Imaging of pancreas transplantation and its complications. Radiol Clin North Am 2016; 54: Tolat PP, Foley WD, Johnson C et al. Pancreas transplant imaging: how I do it. Radiology 2015; 275: Morgan TA, Smith-Bindman R, Harbell J et al. US findings in patients at risk for pancreas transplant failure. Radiology 2016; 280: Vincent M, Morla O, Branchereau J et al. Multi detector computed tomography (MDCT) for the diagnosis of early complications after pancreas transplantation. Abdom Imaging 2014; 39: Barrufet M, Burrel M, Garcıa-Criado MA et al. Pancreas transplants venous graft thrombosis: endovascular thrombolysis for graft rescue. Cardiovasc Intervent Radiol 2014; 37: Low G, Jaremko JL, Lomas DJ. Extravascular complications following abdominal organ transplantation. Clin Radiol 2015; 70: