Bowel Complications Seen on CT After Pancreas Transplantation with Enteric Drainage

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1 Lall et al. owel Complicatio ns on CT fter Pancreas Transplantati on Gastrointestinal Imaging Pictorial Essay C M E D E N T U R I C L I M G I N G JR 2006; 187: X/06/ merican Roentgen Ray Society Y Chandana G. Lall 1 Kumaresan Sandrasegaran 1 Dean T. Maglinte 1 Jonathan. Fridell 2 O F Lall CG, Sandrasegaran K, Maglinte DT, Fridell J Keywords: CT, diabetes mellitus, enteric drainage, gastrointestinal imaging, pancreas transplantation, small bowel DOI: /JR Received June 24, 2005; accepted after revision ugust 8, Department of Radiology, UH 0279, Indiana University School of Medicine, 550 N University lvd., Indianapolis, IN ddress correspondence to K. Sandrasegaran (ksandras@iupui.edu). 2 Department of Surgery, Indiana University School of Medicine, Indianapolis, IN. owel Complications Seen on CT fter Pancreas Transplantation with Enteric Drainage OJECTIVE. owel-related complications from pancreas transplantation account for much of the postsurgical morbidity. In a review of 98 pancreas transplant recipients, we found 19 (19.4%) with such complications. CONCLUSION. The most common problems were small-bowel obstruction and anastomotic leaks. dhesions and internal hernias accounted for most postoperative bowel obstructions. ancreatic transplantation offers P the potential for normalization of blood sugar levels in patients with diabetes mellitus. The procedure helps to stabilize or reverse many of the complications associated with diabetes, such as neuropathy [1], and improves quality of life. With refinement of surgical and immunosuppressant techniques, graft survival is as high as 95% at 1 year [2]. major barrier to the success of pancreas transplantation is the high rate, approximately 30%, of surgical complications, often requiring a second operation [3, 4]. Prior reports have focused on vascular complications, rejection, and pancreatitis [5 7]. In this pictorial essay we describe the bowel complications occurring with enteric drainage of exocrine secretions as a result of pancreas transplantation. Technique of Pancreas Transplantation with Enteric Drainage To understand the complications, it is essential to have a good understanding of the surgical technique. In the past, pancreas transplantation was often performed with exocrine secretions draining into the urinary bladder. This technique resulted in several complications such as metabolic alkalosis and urinary calculi. Drainage of exocrine secretions into the small intestine, or enteric drainage, has recently become more widely used because it overcomes many of these problems. Simultaneous renal transplantation improves survival of the pancreas allograft. oth organs are placed intraperitoneally. Enteric exocrine drainage is performed using a staple technique, in which the donor duodenum is anastomosed side to side to native jejunum, cm distal to the ligament of Treitz [2]. The portal vein of the pancreatic allograft is anastomosed to the recipient right external iliac vein. The donor common iliac artery is anastomosed to the recipient right external iliac artery (Fig. 1). This technique is called systemic enteric pancreatic transplantation. This report deals exclusively with patients who had this surgery. n alternative procedure for venous outflow is to anastomose the donor portal vein to the recipient superior mesenteric vein, rather than to the iliac veins. This procedure is called portal enteric drainage. Postoperative ppearances CT is performed when clinical findings suggest bowel obstruction or abdominal infection. ecause of the simultaneous kidney and pancreas transplantations it is our usual practice to perform CT examinations without administering IV contrast material in the early postoperative period; if vascular disease or transplant necrosis is suspected, Doppler sonography or gadolinium-enhanced MRI examination is typically performed. Positive oral contrast material is used in CT studies to discern bowel from collections. The donor duodenum is identified by a circular staple line (Fig. 2). The donor duodenum may be thick-walled. It is often unfilled with orally introduced contrast material, even when the adjacent native jejunum contains contrast material. The donor duodenum can be misinterpreted as an abscess (Fig. 2). Mild self-limited pancreatitis occurs in the early posttransplantation period in nearly 1288 JR:187, November 2006

2 owel Complications on CT fter Pancreas Transplantation Fig. 1 llustration of systemic-enteric pancreatic transplantation procedure where exocrine secretions drain into small intestine. Donor Y graft is anastomosed to recipient right common iliac artery. Donor portal vein is anastomosed to recipient common iliac vein. Enteric anastomosis for exocrine pancreatic drainage is between donor duodenum and recipient jejunum. Renal artery and vein from donor kidney are anastomosed to recipient external iliac artery and vein, respectively. Inset shows construction of Y graft (using donor vessels) by end-to-end attachment of splenic to internal iliac arteries and superior mesenteric to external iliac arteries. Used with permission from the Office of Visual Media, Indiana University. all cases (Fig. 3), resulting from reperfusion injury, and typically involves the entire graft [6]. Mural thickening of surrounding bowel loops may occur. This finding is seen frequently and usually resolves 3 4 weeks after transplantation. owel Complications We reviewed 99 enteric drainage pancreas transplantations performed in 98 patients at our institution between January 1, 2003, and December 31, Nineteen of these patients (19.4%) had bowel complications. Some of the complications, such as anastomotic leaks, abscess, and adhesions, are common to any major abdominal surgical procedure. Intraperitoneal placement of the pancreas allograft creates the potential for internal hernia and bowel strangulation. The frequency of bowel complications is summarized in Table 1. For this report, we have categorized bowel complications as small-bowel obstruction, anastomotic complications, colonic complications, and miscellaneous complications. Small-owel Obstruction The two main reasons for postoperative small-bowel obstruction (SO) after pancreas transplantation are adhesions and internal hernias. Other less common causes for bowel obstruction include obturation by bezoar, intussusception, and external hernia. In our series, 10 patients (10.2%) presented with high-grade SO. Three of these patients had internal hernias, and the remaining seven were found to have adhesion-related high-grade obstruction. Fig year-old man with donor duodenum simulating abscess., xial unenhanced CT image shows fluid collection (arrowhead) that did not opacify with addition of oral contrast agent, contained gas bubbles, and was incorrectly interpreted as perigraft abscess. Drains (arrows) are noted adjacent to this structure., Subsequent contrast-enhanced CT scan at similar level shows orally administered contrast agent within structure surrounded by ring of staples (arrowhead), confirming normal donor duodenum. JR:187, November

3 Lall et al. Fig year-old man 5 days after kidney pancreas transplantation. xial CT shows moderate amount of fluid (black arrowheads) around pancreas allograft (white arrow). llograft shows enhancement. Note peritoneal gas bubble (white arrowhead) in keeping with recent surgery and renal transplant (black arrow). Such fluid collections are commonly seen in first few weeks after transplantation and do not correlate with graft survival. Fig. 4 Sagittal view line drawing shows internal hernia. Drawing shows potential for internal hernia between donor duodenum/ pancreatic allograft and posterior peritoneum. Hernia occurs through mesenteric defect used to attach donor duodenum to recipient jejunum. Used with permission from the Office of Visual Media Indiana University) Internal Hernia The intraperitoneal placement of the pancreas creates a potential site for an internal hernia (Fig. 4). lthough an internal hernia could occur after other major abdominal surgery, such as roux-en-y gastric bypass, we have found a relatively high incidence of this complication after enteric drainage pancreas transplantation. The mesenteric defect after this transplantation is defined by the aorta and iliac artery posteriorly, the small-bowel mesentery superiorly, the pancreas and enteric anastomosis anteriorly, and the pancreatic vascular anastomoses inferiorly. Jejunum adjacent to the anastomosis with donor duodenum may become trapped posteriorly in relation to the pancreas transplant. In our experience, CT enteroclysis is the best technique for investigating posttransplantation SO. The major findings on conventional CT or CT enteroclysis (Fig. 5) are distended proximal jejunal loops filled with orally or enterally introduced contrast medium; distended small-bowel loops, which are usually not filled with contrast medium, lying between TLE 1: owel Complications Seen on CT in 98 Patients fter Enteric Drainage Pancreatic Transplantation No. Complication of Patients dhesive small-bowel obstruction 7 Internal hernia 3 owel necrosis 2 nastomotic leak with abscess 3 Enterocutaneous fistula 2 Peritonitis 1 owel hemorrhage 1 Cytomegalovirus colitis 1 Pseudomembranous colitis 3 Note These complications were seen in 19 patients; some presented with more than one bowel abnormality. Intestinal abnormalities seen on CT that did not require specific therapy, such as nonobstructive adhesions, are discussed in the text but not included in the table. the donor duodenum or pancreatic allograft and the iliac vessels; and nondistended pelvic small-bowel loops, which may also be seen in adhesion-related obstructions. In addition, it may be possible to discern beaking of the herniated loop and twisting of adjacent mesenteric vessels. It is important to make a timely diagnosis of an internal hernia, which is essentially a closed-loop obstruction. The rate of strangulation is much higher than with an adhesion-related SO [8]. Prompt surgery with repositioning of herniated loops was sufficient to ensure bowel and allograft viability in our patients. dhesions Intraperitoneal placement of the transplanted pancreas with resultant pancreatitis may lead to bowel adhesions. The adhesions causing SOs were in the anterior abdomen (n = 4) or to the anterior aspect of the transplanted kidney (n = 2). In cases of adhesive obstruction, unlike with an internal hernia, distended loops were not seen posteriorly in relation to the donor duodenum (Figs. 6 and 7). fter other abdominal surgery, the timing of a postoperative SO has been suggested as a helpful criterion in determining if an adhesion or an internal hernia is the likely cause [9]. In our experience, the chronologic onset of obstruction was not helpful in determining the cause. dhesion-related high-grade SOs presented within a mean of 170 days after surgery, with the earliest presentation 1290 JR:187, November 2006

4 owel Complications on CT fter Pancreas Transplantation on the 21st postoperative day. Internal hernias presented between 57 and 367 days after surgery. Intermittent low-grade obstructions or nonobstructive adhesions are seen on conventional CT or CT enteroclysis more frequently than are high-grade adhesive SOs. Features of nonobstructive adhesions include acute angulation of small-bowel C Fig year-old woman with internal hernia 8 months after pancreas transplantation., Fluoroscopic part of CT enteroclysis shows beaked end at site of small-bowel obstruction (arrowhead). Donor duodenum (arrow) is attached to jejunum just proximal to obstruction. and C, Reformats in coronal () and sagittal (C) planes of isotropically acquired CT enteroclysis show contrast-filled distended proximal jejunum (white arrows). More distal distended bowel loops (white arrowhead, C) lie posterior to donor duodenum (black arrows). Pelvic small-bowel loops (curved arrows) are nondistended. Internal hernia, through mesenteric defect, was noted during surgery on same day images were obtained. Fig year-old man with adhesive small-bowel obstruction 8 months after pancreas transplantation. and, xial CT images show dilated small-bowel loops (white arrow, ) with nondistended loops in anterior abdomen (black arrows) adherent to parietal peritoneum. Note absence of distended small-bowel loops between donor duodenum (black arrowhead, ) and iliac vessels (white arrowhead, ). (Fig. 6 continues on next page) JR:187, November

5 Lall et al. Fig. 6 (continued) 20-year-old man with adhesive small-bowel obstruction 8 months after pancreas transplantation. C, CT enteroclysis performed next day with positive enteral contrast enhancement shows long segment narrowing of anterior loop of small bowel (black arrow) closely applied to anterior peritoneum. Proximal bowel (white arrow) is distended. ppearances were of adhesive obstruction confirmed during surgery on same day image was obtained. C Fig year-old man with adhesive small-bowel obstruction 3 weeks after pancreas transplantation. and, xial CT images show distended small-bowel loops (solid white arrows) and nondistended anterior loop (white arrowhead, ). On image, no bowel is seen between donor duodenum (straight black arrow) and iliac vessels (curved black arrow), confirming absence of internal hernia. On image, pancreas allograft (dashed white arrow) is edematous, which is consistent with pancreatitis. Patient subsequently underwent adhesionolysis. Incidental note of thrombosed vessel (black arrowhead, ) is seen adjacent to transplant. This is common postoperative finding, caused by thrombosis of distal donor superior mesenteric artery, and is of no clinical significance. loops, stretching of loops with air trapped in valvulae conniventes, asymmetric thickening of the small-bowel wall, small-bowel loops closely applied to the anterior peritoneum, and thickening of the anterior peritoneum [8] (Fig. 8). We routinely comment on these findings because some of these patients have intermittent abdominal pain that improves after surgical adhesionolysis. nastomotic Complications Leakage at the duodenojejunal anastomosis with peritonitis (Fig. 9) or localized abscess formation is an uncommon but serious complication. Occasionally, difficulty occurs in separating fluid collections as a result of anastomotic leaks from pancreatitis-related collections. Presence of an orally administered contrast medium in a collection is highly suggestive of the former. n enterocutaneous fistula may occur if the 1292 JR:187, November 2006

6 owel Complications on CT fter Pancreas Transplantation Fig year-old man with nonobstructive bowel adhesions 9 weeks after pancreas transplantation. Contrast-enhanced axial CT, with orally administered contrast agent, shows multiple loops of small bowel closely applied to anterior abdominal wall. Parietal peritoneum is thickened in parts (black arrowhead). symmetric thickening of small-bowel loops (white arrowhead) is shown. Fig year-old woman with peritonitis 6 weeks after pancreas transplantation. Patient had stormy postoperative course characterized by anastomotic leak, drainage of fluid collections, repeat laparotomy, and continued fever. Contrastenhanced axial CT image, with IV-administered contrast agent, shows fluid collection (arrows) surrounded by enhancing peritoneum. bdominal wound was left open after prior surgery, to prevent abdominal compartment syndrome. Note donor duodenum surrounded by staples (arrowhead). Peritonitis was diagnosed and confirmed during surgery on same day image was obtained. Fig year-old man with enterocutaneous fistula 6 weeks after pancreas transplantation., Contrast-enhanced axial CT image, with orally and IV-administered contrast media, shows possible track (arrow) through abdominal wall extending into open wound. Edema is seen in head of allograft (arrowhead), which is consistent with pancreatitis., xial image from CT enteroclysis performed next day, at same level as in, shows enterally introduced contrast material has extravasated into subcutaneous tissue (arrow) indicating enterocutaneous fistula. Note pancreatic allograft (white arrowhead) and surgical drain (black arrowhead). JR:187, November

7 Lall et al. Fig year-old man with pseudomembranous colitis 4 weeks after pancreas transplantation. Patient had diarrhea and right colon (arrowhead) is considerably thickened. Stool cultures were positive for Clostridium difficile. Incidentally, smallbowel loops are closely applied to anterior abdominal wall (black arrow) and thickening of normally invisible anterior parietal peritoneum (white arrow) is seen, which indicates nonobstructive adhesions. Fig year-old woman with bowel necrosis 5 weeks after pancreas transplantation., Contrast-enhanced axial CT image, with IV-administered contrast agent, shows diffuse small-bowel mural thickening (solid black arrow) and ascites (arrowhead). ubble of free peritoneal (white arrow) gas is noted, which may have been caused by focal bowel perforation, but was clinically thought to be introduced via surgical drain. CT features, although nonspecific, raise suspicion of early bowel ischemia. Patient also had necrotic pancreatic allograft. Note donor duodenum (dashed arrow) anterior to iliac vessels., Unenhanced axial CT obtained 2 weeks later, after further surgical intervention, shows diffuse pneumatosis (arrowheads) and high-density hemorrhagic ascites (arrows). Patient died 1 day later, and postmortem examination showed extensive small-bowel infarction. leak is not diagnosed and treated promptly. In our experience, CT enteroclysis is more likely to depict an anastomotic leak or a small-bowel fistula (Fig. 10) than conventional CT. Colonic Complications Colonic complications after transplantation are uncommon and include cytomegalovirus colitis (n = 1) and antibiotic-associated Clostridium difficile colitis (n = 3) (Fig. 11). Miscellaneous Complications owel necrosis may occur after a strangulation obstruction. Early CT findings of bowel ischemia are nonspecific and include wall thickening, mesenteric vessel engorge JR:187, November 2006

8 owel Complications on CT fter Pancreas Transplantation ment, and ascites (Fig. 12). More advanced ischemia is heralded by mesenteric vessel blurring, hemorrhagic ascites, enhancement of thickened wall on delayed images, pneumatosis, and mesenteric or portal venous gas. We saw two cases of bowel necrosis (Fig. 12). The cause was unclear in both patients, who died despite surgical resection of the affected small bowel. Small-bowel hemorrhage was seen in one patient, who presented with abdominal pain and melena. CT scan showed marked recipient jejunal wall thickening. The patient was treated conservatively and improved without surgery. No cause of the bowel hemorrhage was identified. Rarely, an arterial graft duodenal fistula may be a source of massive gastrointestinal bleeding [10]. Isolated case reports have been published of graft-versus-host disease after pancreatic transplantation because of incompatibility of minor RC antigens [11, 12]. Exclusion of donor spleen has virtually eliminated the risk of this complication, and we saw no cases of this complication in our group of patients. Conclusion Prompt detection and treatment of bowel complications after pancreas transplantation are essential for graft survival. In this report, we have discussed a range of postoperative bowel complications. n internal hernia is a relatively common and important cause of SO after enteric drainage pancreas transplantation, and the risk for bowel ischemia is relatively high after an internal hernia. The radiologist needs to be able to distinguish this entity from simple adhesive SOs. lthough sonography and MR angiography are the main techniques for diagnosing vascular and allograft-related complications, CT and, occasionally, CT enteroclysis are the primary imaging techniques for diagnosing bowel-related complications. References 1. Robertson RP, Davis C, Larsen J, Stratta R, Sutherland DE. Pancreas and islet transplantation for patients with diabetes. Diabetes Care 2000; 23: Freund MC, Steurer W, Gassner EM, et al. Spectrum of imaging findings after pancreas transplantation with enteric exocrine drainage: part 1, posttransplantation anatomy. JR 2004; 182: aktavatsalam R, Little DM, Connolly EM, Farrell JG, Hickey DP. Complications relating to the urinary tract associated with bladder-drained pancreatic transplantation. r J Urol 1998; 81: Eckhoff DE, Sollinger HW. Surgical complications after simultaneous pancreas kidney transplant with bladder drainage. Clin Transpl 1993; Eubank W, Schmiedl UP, Levy E, Marsh CL. Venous thrombosis and occlusion after pancreas transplantation: evaluation with breath-hold gadolinium-enhanced three-dimensional MR imaging. JR 2000; 175: Freund MC, Steurer W, Gassner EM, et al. Spectrum of imaging findings after pancreas transplantation with enteric exocrine drainage: part 2, posttransplantation complications. JR 2004; 182: Hagspiel KD, Nandalur K, urkholder, et al. Contrast-enhanced MR angiography after pancreas transplantation: normal appearance and vascular complications. JR 2005; 184: Sandrasegaran K, Maglinte DD. Imaging of small bowel-related complications following major abdominal surgery. Eur J Radiol 2005; 53: lachar, Federle MP. Gastrointestinal complications of laparoscopic roux-en-y gastric bypass surgery in patients who are morbidly obese: findings on radiography and CT. JR 2002; 179: Lopez NM, Jeon H, Ranjan D, Johnston TD. typical etiology of massive gastrointestinal bleeding: arterio-enteric fistula following enteric drained pancreas transplant. m Surg 2004; 70: Kimball P, Ham J, Eisenberg M, et al. Lethal graft-versus-host disease after simultaneous kidney-pancreas transplantation. Transplantation 1997; 63: Sindhi R, Landmark J, Stratta RJ, Cushing K, Taylor RJ. Humoral graft-versus-host disease after pancreas transplantation with an O-compatible and Rh-nonidentical donor: case report and a rationale for preoperative screening. Transplantation 1996; 61: JR:187, November