Diagnosis, Management, and Outcome of Late Duodenal Complications in Portal–Enteric Pancreas Transplantation: Case Reports

Diagnosis, Management, and Outcome of Late Duodenal Complications in Portal–Enteric Pancreas Transplantation: Case Reports Trine Nymann, MD, M. Hosein Shokouh-Amiri, MD, Debra S. Elmer, Robert J. Stratta, MD, FACS, and A. Osama Gaber, MD, FACS

in the 1980s because of complications occurring with the initial attempts at enteric drainage (ED). At this time, ED was associated with a high incidence of intraabdominal infections and graft loss (1). During the last decade, BD has remained the preferred exocrine drainage technique. Despite the uniform success of BD in improving the results of pancreatic transplantation (2), it has been associated with numerous complications, including hematuria, acidosis, dehydration, reflux pancreatitis, recurrent urinary tract infection, duodenal segment or bladder leaks, and the need for enteric conversion in 10 –20% of the cases (2– 4). Because of the unique morbidity of BD, increasing numbers of transplant centers are now returning to ED (5, 6). In 1995, 15% of all pancreas transplants performed in the United States were drained entericly (7), increasing to 27% in 1996 (8). At our center, we have performed pancreas transplantation with ED in combination with portal venous drainage since 1991 (9). The portal– enteric (PE) technique results in elimination of hyperinsulinemia and removal of the bladder-related complications (10). Refinements in the PE technique have led to an improvement in early surgical outcomes. In the last few years, the graft survival rate has improved substantially and now exceeds 85% at 1 year for the pancreas graft transplanted simultaneously with a kidney (11). Although overcoming initial postoperative technical problems significantly influences the early success rate, longterm success with PE drainage may be dependent on the identification and management of late complications associated with this technique. Duodenal segment complications, particularly duodenal segment leaks, are known to occur in 5–20% of BD pancreas transplants (12). In addition, these duodenal segment complications occur even after the first year after transplantation (12, 13). Because of the location of the pancreas transplant and the difficulty in recognizing duodenal complications after ED, we attempt to describe, in detail, the clinical presentation, diagnosis, and treatment of these complications.

Background: Enteric drainage (ED) of pancreas allografts is an alternative to the bladder drainage (BD) technique and eliminates unique metabolic complications seen in the BD pancreas transplant recipients. Little longterm data has been reported in ED pancreas transplants. Study Design: Of 53 patients who underwent pancreas transplantations performed with ED drainage of the exocrine secretion to a Roux-en-Y limb, who had more than 6 months graft function, four patients were identified with late duodenal segment complications (more than 6 months after transplantation) and are presented as case reports. Results: The duodenal segment complications occurred between 8 and 48 months after simultaneous pancreas– kidney transplantation. Three patients were diagnosed with leakage from the duodenal segment. All were managed operatively. The fourth patient developed a distal stricture of the transplant duodenum occluding the anastomosis between the duodenum and the Roux-en-Y limb and also had a pancreatic pseudocyst. Drainage via a cyst-jejunostomy resulted in graft salvage. The mean followup after operative management of the duodenalrelated complications was 15 months (range, 3–24 months). The patient, pancreas and kidney graft survival are 100%. Conclusions: Late duodenal complications occurred in 8% of pancreas transplant recipients with ED. Operative intervention in all four patients resulted in excellent graft and patient outcome and is recommended for these complications. ( J Am Coll Surg 1997;185:560 –566. © 1997 by the American College of Surgeons)

Exocrine drainage of the pancreas allograft to the bladder (bladder drainage, or BD) was developed Received July 1, 1997; Revised August 27, 1997; Accepted August 27, 1997. From the Division of Transplantation, Department of Surgery, The University of Tennessee, Memphis, TN 38163. Correspondence address: A. Osama Gaber, MD, FACS, Division of Transplantation, Department of Surgery, The University of Tennessee, 956 Court Avenue, Suite A202, Memphis, TN 38163. © 1997 by the American College of Surgeons Published by Elsevier Science Inc.

RN, CCTC,

560

ISSN 1072-7515/97/$17.00 PII S1072-7515(97)000110-5

Nymann et al

DUODENAL COMPLICATIONS IN PANCREAS TRANSPLANT

561

Methods

Transplantation of the pancreas using the PE technique has been described in detail previously (9). Briefly, the portal vein of the pancreas graft is anastomosed end-to-side to a tributary of the superior mesenteric vein. As in the systemically drained pancreas grafts, the splenic and the superior mesenteric arteries are anastomosed to an arterial Y-graft procured from the same donor (common, internal, and external iliac artery). Through a window made in the mesentery, the reconstructed artery of the graft is anastomosed to the right common iliac artery. The duodenal segment, comprising the first, second, and third portion of the donor duodenum is anastomosed distally end-to-end to a Roux-en-Y limb in two layers. The proximal end of the graft duodenum is closed with a staple line followed by inversion with interrupted 3-0 silk sutures. We conducted a review of the records of all patients who received a pancreas transplant using this technique and had greater than 6 months pancreas graft function. In those patients, the incidence of late duodenal segment complications (. 6 months after transplantation) was 4 of 53 patients (8%) and included 3 patients (6%) with duodenal segment leaks and 1 patient (2%) with stricture of the duodenal outlet. The case of each patient is presented individually to emphasize the clinical presentation, management, and outcome associated with these complications. Case report 1. A 48-year-old man had insulindependent diabetes mellitus (IDDM) for 15 years with the development of several secondary complications including gastroparesis, retinopathy, and decreasing kidney function but was not requiring dialysis at the time of transplantation. He received a simultaneous pancreas– kidney transplant (SPK) with PE drainage in April 1992. After transplantation, he had an uneventful course. He did not experience any rejection episodes and returned to work full-time. Thirty months after transplantation, he presented with the acute onset of constant abdominal pain, nausea, and mild fever. Laboratory tests showed a moderate rise in serum amylase and lipase. A computerized tomography (CT) scan showed inflammatory pancreatitis with mesenteric pneumatosis consistent with an enteric leak (Fig. 1). At laparotomy, a 5-mm perforation with clear pancreatic fluid leakage was found. The perforation was located at the inferior corner of the staple line at the proximal duodenal closure. There was evidence of inflammation in the peripancreatic area and generalized peritoni-

FIG 1. Computed tomography scan from case report 1 showing pneumatosis in the mesentery (arrow) consistent with enteric leakage. The pancreas allograft is indicated (Tx P).

tis with fibrinous exudate. The perforation was closed in two layers, and a drain was placed in proximity of the repair. The patient subsequently developed a graft– duodenocutaneous fistula, which eventually required reexploration, at which time a 4-cm segment of the proximal duodenum was resected. A tube-jejunostomy was placed through the Roux-en-Y limb into the duodenum to create a controlled fistula. Microscopic examination of the resected duodenum showed mucosal atrophy with chronic polymorphic inflammation consistent with chronic ischemia. There were no signs of viral infection. Cultures grew out Candida albicans, and the patient was treated with intravenous amphotericin B for 4 weeks. The tube was removed a few weeks after the second operation, and the fistula promptly closed. Currently, the patient has excellent function of both the pancreas and the kidney graft 24 months later, and he is back to work full-time. Case report 2. A 37-year-old man with a 15-year history of IDDM and several secondary complications including retinopathy, neuropathy, and nephropathy requiring dialysis received an SPK transplant with PE drainage in June 1994. The patient received quadruple sequential immunosuppression with Orthoclone OKT3-induction (Ortho Biotech, Raritan, NJ), prednisone, cyclosporine, and azathioprine. His postoperative course was uneventful, and he had excellent function of both grafts. Sixteen months after transplant, he presented with acute mid-upper abdominal pain, nausea, vomiting, and increased temperature, with a leukocytosis of 18.2 K/uL.

562

J

AM COLL SURG

DECEMBER

1997

VOLUME

185:560 –566

FIG 2. Computed tomography scan from case report 2. The pancreas transplant (Tx P) appears edematous. A cystic formation is seen within the gland (straight arrow). The dilated graft duodenum is seen anteriorly to the pancreas graft (curved arrow).

Serum amylase and lipase were elevated to 186 IU/L and 1,026 U/dL, respectively. Abdominal examination demonstrated tenderness in the midabdominal region with no peritoneal signs. He had no evidence of impaired graft function, with a stable serum creatinine and normal fasting blood sugar. A CT scan revealed inflammation in the root of the mesentery and a cystic formation within the pancreas graft (Fig. 2). An exploratory laparotomy was performed, which revealed a dilated graft duodenum with a distal stricture of the transplant duodenum occluding the anastomosis between the duodenum and the Roux-en-Y limb. In addition, a pancreatic pseudocyst had developed in the graft. A cyst-jejunostomy was performed to the Roux-en-Y limb, and a tube-jejunostomy was placed through the duodenojejunal anastomosis. The patient grew out Citrobacter and Streptococcus viridans and was treated with intravenous antibiotics for 7 days, followed by oral treatment. After the operation, he recovered without any surgical complications. He was discharged 7 days after surgery and has maintained good function of both grafts for the last 20 months. Case report 3. A 35-year-old white woman with a 22-year history of IDDM had been on continuous ambulatory peritoneal dialysis for 1.5 years preceding transplantation. In addition to nephropathy, she also suffered from severe gastroparesis and retinopathy. Past surgical history included hysterosalpingooophorectomy. She underwent an SPK transplantation with PE drainage in September 1995. Postoperatively, the patient immediately experienced good function of both allografts. She

FIG 3. A Computed tomography scan from case report 3 showing a normal pancreas allograft (Tx P). This patient had a leakage from the duodenal segment when laparotomy was performed. B Computed tomography scan of the same patient as in A. There is a large fluid collection in the pelvis (FC). The patient had a previous hysterosalpingo oophorectomy. The transplanted kidney is seen to the right in the picture (arrow).

received quadruple sequential immunosuppression with OKT3-induction, tacrolimus, prednisone, and azathioprine, and did not experience any rejection episodes. Eight months after transplantation, she presented with right lower quadrant pain, fever, nausea, vomiting, and an elevated serum lipase and amylase. A CT scan revealed a normal pancreas (Fig. 3A) and a 7 3 7-cm fluid collection in the pouch of Douglas (Fig. 3B), which was drained percutaneously. Because of a high amylase content in the drained fluid, the patient underwent exploration. A small perforation of the transplanted duodenum was found just proximal to the duodenojejunostomy. The pancreas graft appeared normal. The area of perforation, together with the duodenojejunostomy, was excised, and reanastomosis was performed in a

Nymann et al

DUODENAL COMPLICATIONS IN PANCREAS TRANSPLANT

two-layer hand-sewn fashion. After surgery, the serum amylase and lipase immediately normalized. Cultures obtained from the pelvic fluid collection and peritoneal fluid were negative for both bacteria and fungi, and the patient was discharged 8 days after surgery with excellent function of both grafts. Histologic examination of the excised duodenum revealed a suture granuloma with chronic inflammation. There were no signs of cytomegalovirus (CMV) or other viral infections. The patient is now 12 months post– duodenal leak and is maintaining excellent graft function. Case report 4. A 38-year-old white woman had a history of IDDM for 20 years with nephropathy but was not on dialysis at the time of transplantation. She received an SPK transplant in April 1992 with quadruple sequential immunosuppression consisting of antithymocyte gamma-globulin (ATGAM) induction, prednisone, cyclosporine, and azathioprine. Her initial hospital course was complicated by an accelerated rejection with renal failure after initial function and severe pancreatitis. She was subsequently discharged with good organ function after a 3-week hospitalization with treatment of rejection, and she maintained stable function of both of her grafts for the next 4 years. She then presented with acute abdominal pain, fever, and leukocytosis. Serum lipase was 3,688 U/dL and amylase was 629 IU/L. A CT scan of the abdomen was performed on the day of admission, which showed a fluid collection around the transplanted pancreas with inflammation of the surrounding bowel loops (Fig. 4). At exploration, she was found to have diffuse peritonitis with high amylase content in the intraabdominal fluid. The lateral wall of the transplanted duodenum appeared to be deserosalized with a perforation in the middle. The perforation was closed in two layers after excision of a 0.5-cm margin around. A loop of bowel was used to construct a serosal patch over the deserosalized area, and a tube-jejunostomy through the Roux-en-Y limb was left in place. Intraabdominal cultures revealed Enterobacter and Enterococcus spp., and the patient received intravenous antibiotics postoperatively. She was discharged with excellent graft function. Eight months later, she presented again with abdominal pain, distention, and elevated serum amylase and lipase. A CT scan revealed intraperitoneal fluid collections, proximal small bowel distention, and poor visualization of the transplanted pancreas. At exploration, she was found to have diffuse peritonitis. A leak from the donor duodenum proximal to the duodenojejunostomy was identified. In addition, there appeared to be a

563

FIG 4. Computed tomography scan from case report 4. A fluid collection is seen under the liver lobe (FC). The small bowel surrounding the pancreas transplant is inflamed and the graft is poorly visualized (arrows).

partial volvulus of the small intestine around the previous tube-jejunostomy limb, which was adherent to the abdominal wall. The duodenojejunostomy, including the leak, was excised and reanastomosed. The previous tube-jejunostomy was also excised from the abdominal wall, and a jejunojejunostomy was undertaken. Finally, peritoneal debridement followed by lavage of the entire peritoneal cavity were performed. Cultures grew out Enterococcus bacteroides, and she was treated with multiple intravenous antibiotics. The postoperative course was prolonged with delayed bowel movements and moderately elevated amylase and lipase. After 4 weeks in the hospital, she was discharged with good graft function and normalized serum amylase and lipase. Three months after the second duodenal leak, she is having excellent function of both the kidney and pancreas graft. Discussion

The four cases presented in this report are examples of duodenal segment complications occurring between 8 and 48 months after pancreas transplantation in recipients who have had an otherwise uncomplicated posttransplant course. To our knowledge, this is the first report in the literature presenting a series of late duodenal complications in ED pancreas transplants. In all four cases, surgical intervention was performed with excellent results. None of the grafts were lost, and all four patients currently have good graft function after a mean followup of 15 months (range, 3–24 months). The typical clinical presentation was acute abdominal pain located in the lower abdo-

564

J

AM COLL SURG

DECEMBER

1997

VOLUME

185:560 –566

Table 1. Preoperative Laboratory Values for Patients with Delayed Duodenal Complications Case report

Posttreatment (mo)

Time to surgery* (d)

WBC (K/mL)

Lipase† (U/dL)

Amylase† (IU/L)

Creatinine (mg/dL)

Glucose (mg/dL)

30 16 8 48

5 1 5 1

11.8 18.2 12.7 12.7

483 1,026 2,103 3,688

173 186 746 629

1.2 1.9 2.3 1.7

85 102 95 92

1 2 3 4

*Number of days from admission with clinical symptoms to surgical intervention. † Peak values in the preoperative period. WBC, white blood count.

men or midepigastric area, fever, nausea, vomiting, leukocytosis, and elevations in the serum amylase and lipase (Table 1). Although the serum amylase and lipase were elevated in all patients, the levels fluctuated, delaying the decision of surgical intervention in two patients (case nos. 1 and 3; Table 1). A CT scan was obtained in each of the four cases (Table 2). Findings on CT scanning indicated the need for intervention in all patients except case no. 3, which the abnormality was the presence of pelvic fluid; drainage of the fluid demonstrated high levels of amylase and lipase, which led to the decision to operate. All four patients had an upright abdominal x-ray taken on admission. None of these showed signs of perforation or other abnormalities related to the transplanted pancreas. One of the most important lessons learned in this experience (case nos. 1 and 4) was the need for resection with anastomosis to healthy tissue whenever technically possible. Initial attempts at

repairing the duodenal perforation by oversewing were unsuccessful (case no. 1) and resulted in the development of a duodenocutaneous fistula. When the proximal duodenal stump was reexcised and closed, the closure healed appropriately without any further complications. It was not technically possible to perform a resection and reanastomosis in the fourth patient because the leaking area was located in the second part of the duodenum. Instead, a serosal patch was used with good outcome. In such cases, a tube-jejunostomy was used to keep the duodenal loop decompressed for at least 2–3 months. This patient presented 8 months later with a small bowel obstruction, perforation of the duodenum, and peritonitis. She underwent surgical repair and continues to enjoy excellent pancreas function. We speculate that the entrapment of the small intestine around the previous tube-jejunostomy contributed to the development of a second leak by adding tension to the Roux-en-Y limb and donor duodenum.

Table 2. Radiologic Examinations, Operative Findings, and Outcomes in Four Patients With Late Duodenal Leakage or Duodenal Stricture After Pancreas Transplantation With Enteric Drainage Case Abdominal report x-ray 1

Normal None

2

Normal

3

Normal

4

Normal

Normal

Abdominal CT-scan Inflamed, emphysematous mesentery None

Operative findings Leakage from the proximal duodenal stump

Surgical intervention Leak oversewn in two layer

Outcomes

Reoperation with Graft function excision of 24 mo proximal anastomosis Inflamed mesentery; Obstruction of the Cyst-jejunostomy; Graft function pancreatic duodenojejunostomy; tube-jejunostomy 20 mo pseudocyst pancreatic pseudocyst Fluid collection in the Leakage from the Resection and Graft function pouch of Douglas; duodenum, reanastomosis 12 mo pancreas normal proximal to duodenojejunostomy Fluid collection and Leakage from the Excision with Graft function 8 peripancreatic duodenum with closure in twomo following the inflammation deserosalized area layer jejunal second episode serosal patch of leakage Intraperitoneal fluid Second leakage from Resection and Graft function collections and the duodenum and reanastomosis 3 mo dilatation of the small bowel small bowel obstruction

CT, computed tomography.

Histology

Duodenocutaneous None fistula

Microbiology Citrobacter

Chronic ischemia

Candida albicans

Normal duodenum

Citrobacter Streptococcus viridans No growth

Suture granuloma and chronic inflammation None Enterobacter Enterococcus None

Enterococcus bacteroides

Nymann et al

DUODENAL COMPLICATIONS IN PANCREAS TRANSPLANT

Cultures obtained intraoperatively grew out pathogen microorganisms in five of six surgical procedures, and the patients were all treated with appropriate intravenous antibiotics (Table 2). None of the patients developed an intraabdominal abscess after surgery, which could be a favorable effect of the Roux-en-Y limb, avoiding passage of intestinal content through the anastomosis. Duodenal biopsies from three patients were available for histologic examination. None showed signs of CMV infection. The histologic diagnoses are shown in Table 2. The fear of ED of the pancreas graft is a remnant from the era of segmental pancreas grafts and the duodenal button technique. Both of these techniques resulted in a high rate of intraabdominal leakage, with abscess formation, sepsis, and subsequent graft or patient loss (1). Since then, improvements in organ retrieval and preservation, antibiotic therapy, immunosuppression, surgical techniques, postoperative management, and diagnostic methodology have made ED a viable alternative to the BD technique (5, 6, 10, 14, 15). Comparison between ED and BD using a duodenal segment now shows similar results (6, 8). The ED can be performed through either a Roux-en-Y limb as described in this series or through a sideto-side anastomosis between the donor duodenum and the proximal jejunum (6, 14). The latter technique is easier and faster and has not been associated with an increase in leakage or intraabdominal infections. In fact, Kuo and colleagues (6) reported no episodes of leakage in either ED (side-to-side enterotomy) or BD SPK transplants. Another disadvantage of ED drainage in the early era of pancreas transplantation was the inability to diagnose rejection (16). Elevation of blood sugar is known to be a late presentation of pancreatic rejection for which salvage of the graft usually is unsuccessful. With BD followed the ability to monitor urine amylase as a biochemical marker for rejection. Since then, several new diagnostic methods of pancreatic rejection have been developed, including serum lipase, human anodal trypsinogen (17), glucose disappearance rate (kG) (18), and serial fine needle aspiration (19), enabling diagnosis of pancreatic rejection regardless of drainage approach. In addition, the development of newer and more potent immunosuppressive agents has lowered the incidence of rejections from 80 –90% to 20 –30% and thereby also lowered the incidence of graft loss as a result of irreversible rejection. The reported incidence of duodenal segment– related complications in BD pancreas transplants

565

varies from 20% to more than 50% (12, 20, 21), depending on whether urologic complications are included. Leakage from the duodenal segment has been reported in 5–20% of BD pancreas transplants (12, 20 –25). Duodenal leakage occurring early after transplantation is usually technical in nature and is located at the duodenocystotomy, whereas delayed leaks more often are related to the duodenal stump closures. The majority of cases require surgical intervention with either reanastomosis or conversion to ED (12), although conservative treatment with Foley catheter drainage has been reported (13, 20). The source of delayed, spontaneous duodenal leaks is not known. In the cases presented in this report, chronic ischemia was the only significant histologic finding in the resected part of the duodenal segments and may be an important causal factor in late spontaneous duodenal leaks. Cytomegalovirus infection and chronic rejection are other possible mechanisms. Another duodenal-related complication that can occur in both BD and ED pancreas transplants is bleeding. In the BD pancreas transplants, the patient will present with gross hematuria. The site of bleeding can be the duodenum, the anastomosis, or the bladder mucosa. The bleeding can usually be controlled with electrocoaculation during cystoscopy but may require enteric conversion in refractory cases (20, 23, 26, 27). Hematuria in BD pancreas transplants can be caused by factors such as CMV infection, enzymatic erosion, and chronic rejection. In the ED pancreas transplants, the patient will present with gastrointestinal (GI) bleeding, which may cause diagnostic problems in determining the site of bleeding, as the bleeding can be from either the duodenal segment or anywhere else in the GI tract. The incidence and management of bleeding from enterically drained segments are yet unknown; one reported source of bleeding from the duodenal segment in ED pancreas recipients has been invasive CMV infection (28). Duodenal segment complications can also occur early after transplantation. Only few descriptions have appeared of early duodenal segment complications in the modern era of enteric drainage (29). In our series of ED pancreas transplants including SPK, pancreas after kidney (PAK), and pancreas-alone transplants (n 5 67), we have experienced no duodenal segment complications in the early posttransplant period (, 6 months); particularly, there has been no leakage from the duodenal segment. Early complications related to our technique of ED have occurred in 4 of 67

566

J

AM COLL SURG

DECEMBER

1997

VOLUME

185:560 –566

(6%) and included 2 patients with small bowel obstruction (1 had an intestinal band away from the area of the enteric anastomosis, and the other had generalized adhesive intestinal obstruction); 1 developed an intestinal fistula in the Roux-en-Y limb draining the transplanted pancreas, and 1 had a leak from the jejunojejunostomy (stapler line defect). All four patients were managed surgically, and none of the pancreas grafts was lost. Longer series of ED need to be reported to examine whether a similar experience will be seen in other centers performing this technique. Several reports have shown that ED of the pancreas using a duodenal segment is a safe procedure and does not result in an increased incidence of intraabdominal infections (6, 11, 15). The patient and graft survival rates are comparable to those for BD pancreas transplantation, and in addition, the unique urologic complications associated with BD (5, 6, 8, 10, 14, 15) are eliminated. To date, only sequential comparison between ED and BD have been reported, and ED drainage still awaits validation in well-designed prospective studies. Only through such comparison can an exact determination be made of the relative morbidities of both procedures. Despite the lack of such studies, there have been gradual adoptions of this technique by various centers. As patients with ED pancreas transplants achieve longterm followup, it is increasingly important to be aware of delayed complications as described in this report.

9. 10.

11. 12. 13. 14. 15.

16. 17.

18. 19. 20.

21.

References 1. Hesse UJ, Sutherland DER, Najarian JS, and Simmons RL. Intraabdominal infections in pancreas transplant recipients. Ann Surg 1986;203:153–162. 2. Sollinger HW, Ploeg RJ, Eckhoff DE, et al. Two hundred consecutive simultaneous pancreas– kidney transplants with bladder drainage. Surgery 1993;114:736 –744. 3. Stephanian E, Gruessner RWG, Brayman KL, et al. Conversion of exocrine secretions from bladder to enteric drainage in recipients of whole pancreaticoduodenal transplants. Ann Surg 1992;216:663– 672. 4. Sindhi R, Stratta RJ, Lowell JA, et al. Experience with enteric conversion after pancreatic transplantation with bladder drainage. J Am Coll Surg 1997;184:281–289. 5. Corry RJ, Egidi MF, Shapiro R, et al. Enteric drainage of pancreas transplants revisited. Transplant Proc 1995;27: 3048 –3049. 6. Kuo PC, Johnson LB, Schweitzer EJ, Bartlett ST. Simultaneous pancreas/kidney transplantation: a comparison of enteric and bladder drainage of exocrine pancreatic secretion. Transplantation 1997;63:238 –243. 7. Sutherland DER, and Gruessner A. Pancreas transplantation in the United States of America (USA) as reported to the United Network for Organ Sharing (UNOS) and analyzed by the International Pancreas Transplant Registry. In: Terasaki PI, and Cecka JM, eds. Clinical Transplants 1995. Los Angeles: UCLA Tissue Typing Laboratory, 1996:47– 67. 8. Gruessner AC, Sutherland DER, and Gruessner RWG. Enteric (ED) versus bladder drainage (BD) in pancreas (PA)

22.

23.

24. 25. 26.

27. 28. 29.

transplantation: a registry report. American Society of Transplant Physicians, May 10 –14, 1997, Chicago, IL. Abstract 325. Gaber AO, Shokouh-Amiri MH, Grewal HP, and Britt LG. A technique for portal pancreatic transplantation with enteric drainage. Surg Gynecol Obstet 1993;177:417– 419. Gaber AO, Shokouh-Amiri MH, Hathaway DK, et al. Pancreas transplantation with portal venous drainage eliminates hyperinsulinemia and reduces postoperative complications. Transplant Proc 1993;25:1176 –1178. Nymann T, Elmer DS, Shokouh-Amiri MH, and Gaber AO. Improved outcome of patients with portal– enteric pancreas transplantation. Transplant Proc 1997;29:637– 638. Stratta RJ, Sindhi R, Sudan D, et al. Duodenal segment complications in vascularized pancreas transplantation. J Gastro Surg. In press. Mittal VK, and Toledo-Pereyra LH. Management of delayed complications of the duodenal loop in whole organ pancreatic duodenal transplantation. Transplant Proc 1990;22:580 –581. Tibell A, Brattstro¨m C, Wadstro¨m J, et al. Improved results using whole organ pancreatico– duodenal transplants with enteric exocrine drainage. Transplant Proc 1994;26:412– 413. Newell KA, Woodle ES, Millis JM, et al. Pancreas transplantation with portal venous drainage and enteric exocrine drainage offers early advantages without compromising safety and allograft function. Transplant Proc 1995;27:3002–3003. Prieto M, Sutherland DER, Goetz FC, et al. Pancreas transplant results according to the technique of duct management: bladder versus enteric drainage. Surgery 1987;102:680–691. Douzdjian V, Cooper JL, Abecassis MM, Corry RJ. Markers for pancreatic allograft rejection: comparison of serum anodal trypsinogen, serum amylase, serum creatinine and urinary amylase. Clin Transplant 1994;8:79 – 82. Elmer DS, Hathaway DK, Shokouh-Amiri H, et al. The relationship of glucose disappearance rate (kG) to acute pancreas allograft rejection. Transplantation 1994;57:1400–1405. Egidi MF, Shapiro R, Khanna A, et al. Fine-needle aspiration biopsy in pancreatic transplantation. Transplant Proc 1995; 27:3055–3056. Elkhammas EA, Henry ML, Tesi RJ, and Ferguson RM. Duodenal segment-associated complications following combined kidney/pancreas transplantation. Transplant Proc 1993;25: 2230 –2231. Ploeg RJ, Eckhoff DE, D’Alessandro AM, et al. Urological complications and enteric conversion after pancreas transplantation with bladder drainage. Transplant Proc 1994;26:458 – 459. Gruessner RWG, Dunn DL, Tzardis PJ, et al. Complications occurring after whole organ duodenopancreatic transplantation: relation to the allograft duodenal segment. Transplant Proc 1990;22:578 –579. Smith JL, See WA, Ames SA, et al. Lower urinary tract complications in patients with duodenocystostomies for exocrine drainage of the transplanted pancreas. Transplant Proc 1991; 23:1611–1612. Rayhill SC, Odorico JS, Heisey DM, et al. Clinical and laboratory features of pancreatic transplant bladder leaks. Transplant Proc 1995;27:3141–3142. Jones LW, Mizrahi SS, Bentley FR. Success and complications of pancreatic transplantation at one institution. Ann Surg 1996;223:757–764. Stratta RJ, Taylor RJ. Prevention and management of hematuria in combined pancreas– kidney transplant recipients with pancreaticoduodenocystostomy. Transplant Proc 1992; 24:788 –790. Han DJ, Kim IK, Park KC. Refractory graft duodenitis and bleeding following enteric diversion of transplanted pancreas with bladder drainage. Transplant Proc 1994;26:2292–2293. Dunn DL, Gruessner RWG, Tzardis PJ, et al. Pancreatic allograft loss secondary to periallograft gastrointestinal cytomegalovirus ulceration. Transplant Proc 1990;22:678 – 679. Bonham CA, Sugitani A, Gritsch HA, et al. Analysis and management of surgical complications in enterically drained pancreas transplant recipients. American Society of Transplant Surgeons, May 10 –14, 1997, Chicago, IL. Abstract 266.