Advertisement

Pancreas-preserving total duodenectomy for advanced duodenal polyposis in patients with familial adenomatous polyposis: short and long-term outcomes

  • Arthur S. Aelvoet
    Affiliations
    Amsterdam UMC location University of Amsterdam, Department of Gastroenterology and Hepatology, Amsterdam, the Netherlands

    Cancer Center Amsterdam, Amsterdam, the Netherlands

    Amsterdam Gastroenterology Endocrinology Metabolism, Amsterdam, the Netherlands
    Search for articles by this author
  • Barbara A.J. Bastiaansen
    Affiliations
    Amsterdam UMC location University of Amsterdam, Department of Gastroenterology and Hepatology, Amsterdam, the Netherlands

    Cancer Center Amsterdam, Amsterdam, the Netherlands

    Amsterdam Gastroenterology Endocrinology Metabolism, Amsterdam, the Netherlands
    Search for articles by this author
  • Paul Fockens
    Affiliations
    Amsterdam UMC location University of Amsterdam, Department of Gastroenterology and Hepatology, Amsterdam, the Netherlands

    Cancer Center Amsterdam, Amsterdam, the Netherlands

    Amsterdam Gastroenterology Endocrinology Metabolism, Amsterdam, the Netherlands
    Search for articles by this author
  • Marc G. Besselink
    Affiliations
    Amsterdam UMC location University of Amsterdam, Department of Surgery, Amsterdam, the Netherlands

    Cancer Center Amsterdam, Amsterdam, the Netherlands
    Search for articles by this author
  • Olivier R. Busch
    Affiliations
    Amsterdam UMC location University of Amsterdam, Department of Surgery, Amsterdam, the Netherlands

    Cancer Center Amsterdam, Amsterdam, the Netherlands
    Search for articles by this author
  • Evelien Dekker
    Correspondence
    Correspondence: Evelien Dekker, Department of Gastroenterology and Hepatology, Amsterdam UMC, Meibergdreef 9, 1105 AZ, Amsterdam, the Netherlands.
    Affiliations
    Amsterdam UMC location University of Amsterdam, Department of Gastroenterology and Hepatology, Amsterdam, the Netherlands

    Cancer Center Amsterdam, Amsterdam, the Netherlands

    Amsterdam Gastroenterology Endocrinology Metabolism, Amsterdam, the Netherlands
    Search for articles by this author
Open AccessPublished:April 25, 2022DOI:https://doi.org/10.1016/j.hpb.2022.04.004

      Abstract

      Background

      In patients with familial adenomatous polyposis (FAP), extensive nonmalignant duodenal polyposis not amenable to endoscopic management demands surgical resection for which pancreas-preserving total duodenectomy (PPTD) offers a pancreatic parenchyma sparing approach.

      Methods

      This is a retrospective cohort study including consecutive patients who underwent PPTD for FAP. Reconstruction involved a Billroth II anastomosis with a short isolated jejunal limb to facilitate future endoscopic surveillance. Short and long-term outcomes were evaluated.

      Results

      Overall, 30 patients underwent PPTD for Spigelman stage III (n = 6) or IV (n = 24). Sixteen patients experienced a severe complication (Clavien–Dindo grade III/IV) including postoperative pancreatic fistula (ISGPS grade B/C) in twelve. There was no all cause in-hospital and 90-day mortality. During follow-up (median 125 months), five patients developed acute pancreatitis, one new-onset diabetes and one exocrine pancreatic insufficiency. During endoscopic surveillance in 27 patients, jejunal adenomas were detected in 22 and advanced adenomas in 11. An additional surgical resection was required in four patients with extensive jejunal polyposis. None developed jejunal cancer. The 10-year overall survival rate was 93.3%.

      Conclusion

      Postoperative morbidity after PPTD is substantial but on the long-term, rates of pancreatic insufficiencies are low. Most patients develop jejunal adenomas at follow-up, highlighting the need for endoscopic surveillance.

      Introduction

      In patients with familial adenomatous polyposis (FAP), colorectal cancer can be prevented by colectomy and intensive endoscopic surveillance, contributing to an almost normal life-expectancy nowadays.
      • Mallinson E.K.
      • Newton K.F.
      • Bowen J.
      • Lalloo F.
      • Clancy T.
      • Hill J.
      • et al.
      The impact of screening and genetic registration on mortality and colorectal cancer incidence in familial adenomatous polyposis.
      ,
      • Karstensen J.G.
      • Burisch J.
      • Pommergaard H.C.
      • Aalling L.
      • Højen H.
      • Jespersen N.
      • et al.
      Colorectal cancer in individuals with familial adenomatous polyposis, based on analysis of the Danish polyposis registry.
      Subsequently, challenges in the care for patients with FAP have shifted from colorectal disease towards extra-colonic manifestations, of which duodenal polyposis and desmoid tumors are the most important. In FAP, the lifetime risk of developing duodenal polyps approaches 100%,
      • Bülow S.
      • Björk J.
      • Christensen I.J.
      • Fausa O.
      • Järvinen H.
      • Moesgaard F.
      • et al.
      Duodenal adenomatosis in familial adenomatous polyposis.
      ,
      • Spigelman A.D.
      • Williams C.B.
      • Talbot I.C.
      • Domizio P.
      • Phillips R.K.
      Upper gastrointestinal cancer in patients with familial adenomatous polyposis.
      while the risk of developing duodenal cancer is substantial at 4–10%.
      • Björk J.
      • Akerbrant H.
      • Iselius L.
      • Bergman A.
      • Engwall Y.
      • Wahlström J.
      • et al.
      Periampullary adenomas and adenocarcinomas in familial adenomatous polyposis: cumulative risks and APC gene mutations.
      • Bülow S.
      • Christensen I.J.
      • Højen H.
      • Björk J.
      • Elmberg M.
      • Järvinen H.
      • et al.
      Duodenal surveillance improves the prognosis after duodenal cancer in familial adenomatous polyposis.
      • Lepistö A.
      • Kiviluoto T.
      • Halttunen J.
      • Järvinen H.J.
      Surveillance and treatment of duodenal adenomatosis in familial adenomatous polyposis.
      • Wallace M.H.
      • Phillips R.K.
      Upper gastrointestinal disease in patients with familial adenomatous polyposis.
      The severity of duodenal polyposis is reflected by Spigelman stage, ranging from 0 to IV, and correlates with the risk of duodenal cancer.
      • Spigelman A.D.
      • Williams C.B.
      • Talbot I.C.
      • Domizio P.
      • Phillips R.K.
      Upper gastrointestinal cancer in patients with familial adenomatous polyposis.
      In prospective studies, patients with the most advanced Spigelman stage (IV) had a risk up to 36% of developing duodenal cancer.
      • Bülow S.
      • Björk J.
      • Christensen I.J.
      • Fausa O.
      • Järvinen H.
      • Moesgaard F.
      • et al.
      Duodenal adenomatosis in familial adenomatous polyposis.
      ,
      • Groves C.J.
      • Saunders B.P.
      • Spigelman A.D.
      • Phillips R.K.
      Duodenal cancer in patients with familial adenomatous polyposis (FAP): results of a 10 year prospective study.
      To eliminate the risk of developing duodenal cancer, a radical resection of the affected duodenum can be offered to patients with an advanced Spigelman stage. Within the last decades however, endoscopic resection techniques for duodenal adenomas evolved and appeared to be safe and effective with a low incidence of cancer development and duodenal surgery.
      • Moussata D.
      • Napoleon B.
      • Lepilliez V.
      • Klich A.
      • Ecochard R.
      • Lapalus M.G.
      • et al.
      Endoscopic treatment of severe duodenal polyposis as an alternative to surgery for patients with familial adenomatous polyposis.
      ,
      • Roos V.H.
      • Bastiaansen B.A.
      • Kallenberg F.G.J.
      • Aelvoet A.S.
      • Bossuyt P.M.M.
      • Fockens P.
      • et al.
      Endoscopic management of duodenal adenomas in patients with familial adenomatous polyposis.
      In patients with FAP and extensive duodenal polyposis without possibility for endoscopic treatment, total duodenectomy will prevent duodenal cancer. This can be performed either by pancreatoduodenectomy (PD) or pancreas-preserving total duodenectomy (PPTD). PD is related with a considerable 16% risk of endocrine and 74% risk of exocrine pancreatic insufficiency
      • Scholten L.
      • Mungroop T.H.
      • Haijtink S.A.L.
      • Issa Y.
      • van Rijssen L.B.
      • Koerkamp B.G.
      • et al.
      New-onset diabetes after pancreatoduodenectomy: a systematic review and meta-analysis.
      ,
      • Tseng D.S.
      • Molenaar I.Q.
      • Besselink M.G.
      • van Eijck C.H.
      • Borel Rinkes I.H.
      • van Santvoort H.C.
      Pancreatic exocrine insufficiency in patients with pancreatic or periampullary cancer: a systematic review.
      and respectively 11–12% and 30–75% in studies specifically focusing on PD in patients with FAP.
      • Walsh R.M.
      • Augustin T.
      • Aleassa E.M.
      • Simon R.
      • El-Hayek K.M.
      • Moslim M.A.
      • et al.
      Comparison of pancreas-preserving total duodenectomy (PPTD) and pancreatoduodenectomy (PD) for the management of duodenal polyposis syndromes.
      • de Castro S.M.
      • van Eijck C.H.
      • Rutten J.P.
      • Dejong C.H.
      • van Goor H.
      • Busch O.R.
      • et al.
      Pancreas-preserving total duodenectomy versus standard pancreatoduodenectomy for patients with familial adenomatous polyposis and polyps in the duodenum.
      • Müller M.W.
      • Dahmen R.
      • Köninger J.
      • Michalski C.W.
      • Hinz U.
      • Hartel M.
      • et al.
      Is there an advantage in performing a pancreas-preserving total duodenectomy in duodenal adenomatosis?.
      • Caillié F.
      • Paye F.
      • Desaint B.
      • Bennis M.
      • Lefèvre J.H.
      • Parc Y.
      • et al.
      Severe duodenal involvement in familial adenomatous polyposis treated by pylorus-preserving pancreaticoduodenectomy.
      Therefore, PPTD is typically offered to patients with premalignant duodenal polyposis only, whereas PD is reserved for patients where pre-operative pathology shows duodenal or ampullary cancer requiring an oncologic resection including adequate lymphadenectomy. Since most patients will develop jejunal adenomas,
      • Alderlieste Y.A.
      • Bastiaansen B.A.
      • Mathus-Vliegen E.M.
      • Gouma D.J.
      • Dekker E.
      High rate of recurrent adenomatosis during endoscopic surveillance after duodenectomy in patients with familial adenomatous polyposis.
      ,
      • Yoon J.Y.
      • Mehta N.
      • Burke C.A.
      • Augustin T.
      • O'Malley M.
      • LaGuardia L.
      • et al.
      The prevalence and significance of jejunal and duodenal bulb polyposis after duodenectomy in familial adenomatous polyposis: retrospective cohort study.
      postoperative endoscopic surveillance should be facilitated by maintaining access to the jejunum after reconstruction. Therefore, several authors reporting on PPTD advocate for a straight anastomosis to the proximal jejunum, such as Billroth I (BI) reconstruction, instead of reconstruction with an indirect route to an isolated blind-ending jejunal limb with biliary and pancreatic anastomosis as usually performed after PD.
      • Walsh R.M.
      • Augustin T.
      • Aleassa E.M.
      • Simon R.
      • El-Hayek K.M.
      • Moslim M.A.
      • et al.
      Comparison of pancreas-preserving total duodenectomy (PPTD) and pancreatoduodenectomy (PD) for the management of duodenal polyposis syndromes.
      ,
      • Sarmiento J.M.
      • Thompson G.B.
      • Nagorney D.M.
      • Donohue J.H.
      • Farnell M.B.
      Pancreas-preserving total duodenectomy for duodenal polyposis.
      • Watanabe Y.
      • Ishida H.
      • Baba H.
      • Iwama T.
      • Kudo A.
      • Tanabe M.
      • et al.
      Pancreas-sparing total duodenectomy for Spigelman stage IV duodenal polyposis associated with familial adenomatous polyposis: experience of 10 cases at a single institution.
      • Chung R.S.
      • Church J.M.
      • vanStolk R.
      Pancreas-preserving total duodenectomy: indications, surgical technique, and results.
      • Penninga L.
      • Svendsen L.B.
      Pancreas-preserving total duodenectomy: a 10-year experience.
      However, a PPTD with Billroth II (BII) reconstruction with a short (approximately 30 cm) isolated blind-ending jejunal limb will allow postoperative endoscopic surveillance. To our knowledge, there are no studies reporting on PPTD with BII reconstruction.
      In this study, we evaluated the postoperative outcomes and long-term complications of PPTD. In addition, we investigated whether BII reconstruction enables adequate endoscopic surveillance and we studied the course of postoperative adenoma development in the jejunum.

      Methods

      Design and study population

      We conducted a single-center retrospective cohort study including patients with FAP who underwent PPTD between 2000 and 2021 at Amsterdam UMC, a tertiary referral center for patients with FAP as well as for pancreatic surgery. A diagnosis of FAP was defined as having a genetic diagnosis with a germline mutation in the APC gene and/or having a clinical diagnosis with more than hundred colorectal adenomas.
      The Institutional Review Board of Amsterdam UMC, location AMC, judged that this study it not subjected to the legislation Medical Research Involving Human Subjects Act, and no official ethical review was needed.

      Data collection

      Patient demographics as well as data on colorectal surgery, endoscopic duodenal intervention history and pre-operative Spigelman stage were collected, based on endoscopy and pathology reports. Perioperative outcomes included data on duration of surgery (minutes), intra and postoperative complications documented in the medical charts, duration of hospital stay (days), readmissions and early reoperations (within 30 days of surgery or during postoperative hospital stay). Postoperative pancreatic fistulas were assessed according to the definition and grading suggested by the International Study Group for Pancreatic Surgery (ISGPS). Long-term complications were identified, with special interest for pancreatitis, cholangitis, endocrine and exocrine pancreatic insufficiency and reoperations more than 30 days after PPTD. Information on postoperative endoscopic surveillance was extracted from endoscopy and pathology reports. Completeness of endoscopy was assessed by documentation on reaching the end of the blind-ending jejunal limb and visualization of the neo-ampulla. We collected data on the type of endoscope used, number and location of jejunal adenomas, histopathology in terms of type of adenomas (tubular, tubulovillous or villous) and grade of dysplasia, and endoscopic interventions.

      Preoperative endoscopic assessment

      Since PPTD does not provide an oncologic resection, it is of utmost importance to rule out duodenal or ampullary cancer before surgery. Patients with advanced duodenal polyposis undergo half to yearly endoscopic surveillance performed on a dedicated endoscopy program in an expert center for FAP. High definition endoscopes with advanced imaging techniques, such as narrow band imaging, are used for meticulous assessment of the size and mucosal pattern of adenomas. With this policy, we have been able to distinguish between premalignant and malignant disease before patients undergo PPTD whereas so far no cancers have been found in the resection specimens.

      Surgical technique

      In order to determine the level of jejunal transection, it is important to know whether patients have jejunal polyps at time of surgery. In some patients, this was difficult to assess due to limited endoscope intubation in the jejunum preoperatively. In those cases, a jejunoscopy during surgery was performed to determine the optimal transection site of the jejunum. No frozen sections were needed to assess the transaction plane. Subsequently, the jejunum is transected distal to the ligament of Treitz, followed by meticulous dissection of the duodenum from the pancreas, controlling all the small vessels between pancreas and duodenum, until the ampulla is reached. At this point the submucosal dissection plane is chosen and the orifice of the pancreatic duct as well as the common bile duct is identified. If the gallbladder is still in situ, cholecystectomy is performed, followed by a catheter cannulation of the cystic duct up to the ampulla. Usually the pylorus and one to two centimeters of the antrum are resected especially when polyps are present in the bulb close to the pylorus. Then the upper part of the duodenum is dissected from the pancreas approaching the ampulla. The common bile duct and pancreatic duct are both transected and the specimen is removed.
      Subsequently, a blind-ending jejunal loop is placed behind the mesenteric route on the original location of the resected duodenum. Reconstruction is accomplished by merging the common bile duct and pancreatic duct with PDS 5.0 followed by re-insertion into the blind-ending jejunal loop, also with PDS 5.0, resulting in an end-to-side combined bilio-pancreatic anastomosis to the jejunum as a “neo-ampulla”. Preoperative MR imaging is performed to rule out a pancreas divisum. In case of a pancreas divisum, both pancreatic ducts should be re-inserted into the jejunum or the procedure should be converted into PD. Approximately 30 cm distally to the bilio-pancreatic anastomosis, BII reconstruction is performed with end-to-side gastrojejunostomy or duodenojejunostomy depending on whether the pylorus is preserved or not. Fig. 1 shows the schematic reconstruction after PPTD as performed in Amsterdam UMC. The cystic duct catheter is secured intra-abdominally with Vicryl 4.0 and is left for external drainage of bile and stenting of the anastomoses, and an abdominal drain is placed near the bilio-pancreatic anastomosis. Octreotide is prophylactically administered for 7 days post-operatively. The cystic duct catheter is removed percutaneously after a minimum of 6 weeks at the outpatient clinic when Vicryl is resolved. After this period, no intra-abdominal leakage is to be expected.
      Figure 1
      Figure 1Schematic representation of anatomy after PPTD as performed in Amsterdam UMC

      Postoperative endoscopic surveillance

      As we proposed in a previous study, endoscopic surveillance was performed from 2 years after PPTD and subsequent surveillance intervals were determined based on “neo-Spigelman stage”, but not exceeding a 3 years interval.
      • Alderlieste Y.A.
      • Bastiaansen B.A.
      • Mathus-Vliegen E.M.
      • Gouma D.J.
      • Dekker E.
      High rate of recurrent adenomatosis during endoscopic surveillance after duodenectomy in patients with familial adenomatous polyposis.
      Endoscopies were performed at a dedicated endoscopy program by endoscopists having extensive experience with FAP patients using Olympus gastroscopes (Q160, Q180, H180, H190 or HQ190) or pediatric colonoscopes (PCF 160/180, PCF-H190D or PCF-PH190) (Olympus, Tokyo, Japan).

      Statistical analysis

      Descriptive statistics were used for demographics, peri-operative outcomes, long-term outcomes and findings of postoperative endoscopic procedures. Categorical variables are presented as numbers and percentages (n/%), continuous variables with normal distribution as means with standard deviation and continuous variables with skewed distribution as medians with interquartile ranges (IQR). Categorical variables are compared using the Pearson Chi-square statistic or Fisher's exact test. The cumulative probability of events (development of jejunal adenomas and reoperations) is estimated using the Kaplan–Meier method. All analyses were performed using SPSS 26 (IBM Corp. Released 2019. IBM SPSS Statistics for Windows, Version 26.0. Armonk, NY: IBM Corp).

      Results

      Patient characteristics

      Overall, 30 consecutive patients with FAP who underwent PPTD between 2000 and 2021 were included. Baseline characteristics are summarized in Table 1. Median age at time of PPTD was 53 (IQR 43–60) and all patients had previously undergone total colectomy, at a median age of 28 years. Based on combining pre-operative endoscopy and pathology reports, 6 patients had Spigelman stage III and 24 patients stage IV with high-grade dysplasia in 13 patients, all in the Spigelman stage IV group. The median size of the largest duodenal adenoma was 33 mm (IQR 24–50). In 7 patients, an endoscopic duodenal polypectomy was performed earlier. Two patients with synchronous gastric cancer and extensive duodenal polyposis underwent PPTD combined with total gastrectomy followed by reconstruction with Roux-Y esophagojejunostomy. Three patients (10%) were known to have intra abdominal desmoid tumors pre-operatively or a desmoid tumor was found during PPTD. These tumors did not hamper the resection or reconstruction. No patients were withheld from PPTD due to desmoid disease. No patients were found to have a pancreas divisum on preoperative MR imaging.
      Table 1Baseline characteristics
      PPTD (n = 30)
      Age at PPTD, median (IQR)53 (43–60)
      Male sex16 (53%)
      Type of FAP diagnosis
       Clinical diagnosis7 (23%)
       Clinical diagnosis and proven APC mutation23 (77%)
      History of colectomy30 (100%)
      Age at colectomy, median (IQR)28 (22–36)
      Intra-abdominal desmoid tumor3 (10%)
      Pre-operative assessment
       Spigelman stage III6 (20%)
       Spigelman stage IV24 (80%)
       Low-grade dysplasia17 (57%)
       High-grade dysplasia13 (43%)
       Size of largest adenoma in mm, median (IQR)33 (24–50)
      History of endoscopic duodenal polypectomy7 (23%)

      Perioperative outcomes

      Table 2 summarizes the short-term outcomes. No intraoperative complications occurred. In the majority of patients (67%), reconstruction with gastrojejunostomy was performed, while in 8 patients (27%) the pylorus was preserved resulting in duodenojejunostomy. Postoperative complications occurred in 22 patients (73%) with 16 patients (53%) having one or more severe complications defined as Clavien–Dindo III or IV. All severe complications comprised grade III complications except for one grade IV complication in a patient who required ICU admission due to cholangiosepsis after pancreatic fistula. The most common severe complication was postoperative pancreatic fistula, ISGPS grade B/C, appearing in 12 patients (40%), which resulted usually in a combination of pancreatic and biliary leakage due to the nature of the reconstruction. Treatment required percutaneous drainage in all patients except for one who underwent relaparotomy to oversew the defect. The second most common complications were leakage of the gastro-, duodeno- or esophagojejunostomy in 4 patients (13%) and delayed gastric emptying in 5 patients (17%), with endoscopic placement of a nasogastric tube in all patients. One patient (3%) experienced infected necrotizing pancreatitis, requiring Video-Assisted Retroperitoneal Debridement (VARD). The median duration of hospital stay was 15 days (IQR 10–33). Histopathology of the resection specimens did not reveal any (unexpected) cancers. All cause in-hospital and 90-day mortality was 0%.
      Table 2Peri-operative outcomes
      PPTD (n = 30)
      Duration of surgery, minutes (IQR)312 (261–369)
      Intra-operative complications0 (0%)
      Reconstruction (anastomosis)
       Gastrojejunostomy20 (67%)
       Duodenojejunostomy8 (27%)
       Esophagojejunostomy2 (7%)
      Post-operative complications
       Clavien–Dindo grade I–IV22 (73%)
       Clavien–Dindo grade III or IV16 (53%)
       Pancreatic fistula grade B or C12 (40%)
       Leakage gastro-, duodeno or esophagojejunostomy4 (13%)
       Early acute pancreatitis1 (3%)
       Delayed gastric emptying5 (17%)
      Early re-operation (within 30 days or during postoperative hospital stay)2 (7%)
      Duration of hospital stay in days, median (IQR)15 (10–33)
      90-day mortality0 (0%)

      Long-term complications

      During a median follow-up of 125 months (IQR 61–167), 11 patients (37%) experienced one or more late complications, occurring more than 30 days after PPTD (Table 3). Five patients (17%) had late acute pancreatitis, of which 3 had multiple recurrent exacerbations. In one patient the etiology was biliary, one patient had a stenotic bilio-pancreatic anastomosis and in one patient the etiology was unknown. One patient (3%) was diagnosed with a new onset diabetes 10 months after PPTD and in one (3%) an exocrine pancreatic insufficiency was suspected and treated by oral pancreatic enzymes. One patient (3%) had a history of proctocolectomy with end ileostomy followed by construction of a continent ileostomy and subsequent excision of the continent ileostomy, and appeared to have a short bowel syndrome with a remaining small bowel length of 2m after PPTD. Four patients (13%) underwent late reoperation related to PPTD due to perforation of the gastrojejunostomy, incisional hernia, a small bowel fistula nearby the duodenojejunostomy and recurrent acute pancreatitis requiring pancreatic head resection 17 months after PPTD.
      Table 3Long-term complications
      PPTD (n = 30)
      Late acute pancreatitis5 (17%)
      Cholangitis2 (7%)
      New onset diabetes mellitus1 (3%)
      Exocrine pancreatic insufficiency1 (3%)
      Short bowel syndrome1 (3%)
      Small bowel fistula1 (3%)
      Incisional hernia1 (3%)
      Perforation gastrojejunostomy1 (3%)
      Late re-operation related to PPTD4 (13%)

      Postoperative endoscopic surveillance

      During a median postoperative endoscopic follow-up of 119 months (IQR 55–148), 27 patients underwent a total of 176 endoscopies with a median of 6 procedures (IQR 2–10) per patient. Patients underwent their first postoperative surveillance endoscopy after a median of 14 months (IQR 10–22) after PPTD.
      Visualization of the end of the blind jejunal limb and neo-ampulla was documented at least once in 24 (96%) and 22 (85%) patients, respectively, when only taking into account procedures in which it was documented whether the blind end and/or neo-ampulla were assessed. The median percentage of procedures per patient in which the end of the blind jejunal limb and neo-ampulla was visualized, is 83% and 61%, respectively. Univariate analysis showed that in endoscopies performed after 2010, the end of the blind-ending jejunal limb was reached more frequently (p = 0.002) and the neo-ampulla was visualized more often (p = 0.001). During most of the endoscopies performed after 2010 a pediatric colonoscope was used.
      Jejunal polyps were found in 22 patients (81%) with a median time to diagnosis of the first polyp of 51 months (IQR 23–92). In these 22 patients, a cumulative number of 294 jejunal polyps was detected, of which 154 (52%) were located in the blind-ending afferent jejunal limb and 140 (48%) in the efferent jejunal limb. Per patient, a median of 7 jejunal polyps (IQR 2–21) were found. A total of 48 advanced jejunal adenomas, defined as an adenoma ≥10 mm and/or an adenoma containing high-grade dysplasia, was detected in 11 patients (41%) after a median of 44 months (IQR 14–19). Forty one of these advanced adenomas were located in the afferent limb and 7 in the efferent limb. In seven patients (26%), progression of jejunal polyposis to “neo-Spigelman stage IV” was observed after a median of 91 months (IQR 59–119) since PPTD (Fig. 2).
      Ten patients (37%) underwent a total of 28 endoscopic polypectomies in the jejunum, all performed after 2010. Twenty-two polypectomies were performed in the blind-ending afferent limb and 6 in the efferent limb and the mean size of resected polyps was 18 mm (range 2–80). All polyps were adenomas with low-grade dysplasia, except for one with high-grade dysplasia detected in a 25 mm polyp that was resected en bloc in the afferent limb. During follow-up endoscopies two recurrences (9%) were detected which were treated endoscopically, of which one showed a second recurrence with no options for endoscopic treatment followed by surgery. Four patients (15%) needed a total of 5 jejunal resections for polyps that could not be completely resected endoscopically (Fig. 2). Four procedures comprised resections of the blind-ending afferent limb and one a segmental resection of the efferent limb. None of the patients developed jejunal cancer.
      Signs of biliary reflux and/or gastritis were observed during endoscopy in 17 patients (57%), significantly more often in patients with resected pylorus compared to patients in which the pylorus was preserved (p = 0.028). Seven (26%) were diagnosed with an anastomotic ulcer located at the gastrojejunostomy (n = 6) or duodenojejunostomy (n = 1).

      Deaths during follow-up

      Four patients (13%) died during postoperative follow-up. One patient who underwent combined PPTD and total gastrectomy for extensive duodenal polyposis and gastric cancer, died 11 months postoperatively from metastatic disease. One patient died from cholangiosepsis 11 years after PPTD, one patient died from metastases from an unknown primary tumor 12 years after PPTD and one patient died from recurrent pancreatitis 13 years after PPTD. The 3-, 5- and 10- year overall survival rates were 96.0%, 95.6% and 93.3%, respectively.

      Discussion

      In this relatively large series on pancreas-preserving total duodenectomy in patients with FAP we found considerable postoperative morbidity, albeit without in-hospital and 90-day mortality and a low risk (<5%) of endocrine and exocrine pancreatic insufficiency on the long-term compared to pancreatoduodenectomy. Despite Billroth II reconstruction with an isolated blind-ending jejunal limb, complete endoscopic examination of both jejunal limbs was possible in nearly all patients. This is crucial since most patients will develop jejunal adenomas by time which may require endoscopic or surgical re-interventions to prevent jejunal cancer.
      The most recent series of centers reporting on PPTD in patients with FAP are summarized in Table 4. In the present study, 16 patients (53%) experienced a severe postoperative complication defined as Clavien–Dindo III or IV including 12 patients (40%) with a postoperative pancreatic fistula (ISGPS grade B or C). This significant morbidity is comparable to other series on PPTD,
      • Walsh R.M.
      • Augustin T.
      • Aleassa E.M.
      • Simon R.
      • El-Hayek K.M.
      • Moslim M.A.
      • et al.
      Comparison of pancreas-preserving total duodenectomy (PPTD) and pancreatoduodenectomy (PD) for the management of duodenal polyposis syndromes.
      ,
      • Sarmiento J.M.
      • Thompson G.B.
      • Nagorney D.M.
      • Donohue J.H.
      • Farnell M.B.
      Pancreas-preserving total duodenectomy for duodenal polyposis.
      ,
      • Watanabe Y.
      • Ishida H.
      • Baba H.
      • Iwama T.
      • Kudo A.
      • Tanabe M.
      • et al.
      Pancreas-sparing total duodenectomy for Spigelman stage IV duodenal polyposis associated with familial adenomatous polyposis: experience of 10 cases at a single institution.
      ,
      • Ganschow P.
      • Hackert T.
      • Biegler M.
      • Contin P.
      • Hinz U.
      • Büchler M.W.
      • et al.
      Postoperative outcome and quality of life after surgery for FAP-associated duodenal adenomatosis.
      suggesting the technical difficulty of this uncommon procedure. Studies comparing PPTD to PD in patients with FAP did not find different incidences of pancreatic fistulas after PPTD (14–27%) versus PD (11–25%), however the incidence in the present study was higher (40%).
      • Walsh R.M.
      • Augustin T.
      • Aleassa E.M.
      • Simon R.
      • El-Hayek K.M.
      • Moslim M.A.
      • et al.
      Comparison of pancreas-preserving total duodenectomy (PPTD) and pancreatoduodenectomy (PD) for the management of duodenal polyposis syndromes.
      ,
      • de Castro S.M.
      • van Eijck C.H.
      • Rutten J.P.
      • Dejong C.H.
      • van Goor H.
      • Busch O.R.
      • et al.
      Pancreas-preserving total duodenectomy versus standard pancreatoduodenectomy for patients with familial adenomatous polyposis and polyps in the duodenum.
      The median duration of hospital stay was 15 days, comparable to the range of 9–27 days reported by other studies on PPTD.
      • Walsh R.M.
      • Augustin T.
      • Aleassa E.M.
      • Simon R.
      • El-Hayek K.M.
      • Moslim M.A.
      • et al.
      Comparison of pancreas-preserving total duodenectomy (PPTD) and pancreatoduodenectomy (PD) for the management of duodenal polyposis syndromes.
      ,
      • Sarmiento J.M.
      • Thompson G.B.
      • Nagorney D.M.
      • Donohue J.H.
      • Farnell M.B.
      Pancreas-preserving total duodenectomy for duodenal polyposis.
      ,
      • Ganschow P.
      • Hackert T.
      • Biegler M.
      • Contin P.
      • Hinz U.
      • Büchler M.W.
      • et al.
      Postoperative outcome and quality of life after surgery for FAP-associated duodenal adenomatosis.
      ,
      • Al-Sarireh B.
      • Ghaneh P.
      • Gardner-Thorpe J.
      • Raraty M.
      • Hartley M.
      • Sutton R.
      • et al.
      Complications and follow-up after pancreas-preserving total duodenectomy for duodenal polyps.
      Late onset acute pancreatitis occurred in 5 patients (17%) which is also consistent to the 8–22% observed in literature.
      • Sarmiento J.M.
      • Thompson G.B.
      • Nagorney D.M.
      • Donohue J.H.
      • Farnell M.B.
      Pancreas-preserving total duodenectomy for duodenal polyposis.
      ,
      • Ganschow P.
      • Hackert T.
      • Biegler M.
      • Contin P.
      • Hinz U.
      • Büchler M.W.
      • et al.
      Postoperative outcome and quality of life after surgery for FAP-associated duodenal adenomatosis.
      • Al-Sarireh B.
      • Ghaneh P.
      • Gardner-Thorpe J.
      • Raraty M.
      • Hartley M.
      • Sutton R.
      • et al.
      Complications and follow-up after pancreas-preserving total duodenectomy for duodenal polyps.
      • Naples R.
      • Simon R.
      • Moslim M.
      • Augustin T.
      • Church J.
      • Burke C.A.
      • et al.
      Long-term outcomes of pancreas-preserving total duodenectomy for duodenal polyposis in familial adenomatous polyposis syndrome.
      Walsh et al. found a higher incidence of late acute pancreatitis after PPTD (16%) compared to PD (0%).
      • Walsh R.M.
      • Augustin T.
      • Aleassa E.M.
      • Simon R.
      • El-Hayek K.M.
      • Moslim M.A.
      • et al.
      Comparison of pancreas-preserving total duodenectomy (PPTD) and pancreatoduodenectomy (PD) for the management of duodenal polyposis syndromes.
      Although believed to be a common cause of late acute pancreatitis, anastomotic stricture was only seen in one out of five patients in the present study, and in one out of twelve patients in a study performed by Naples et al.
      • Naples R.
      • Simon R.
      • Moslim M.
      • Augustin T.
      • Church J.
      • Burke C.A.
      • et al.
      Long-term outcomes of pancreas-preserving total duodenectomy for duodenal polyposis in familial adenomatous polyposis syndrome.
      In terms of postoperative pancreatic functional outcomes, only one patient (3%) developed exocrine pancreatic insufficiency in line with 0–11%
      • Walsh R.M.
      • Augustin T.
      • Aleassa E.M.
      • Simon R.
      • El-Hayek K.M.
      • Moslim M.A.
      • et al.
      Comparison of pancreas-preserving total duodenectomy (PPTD) and pancreatoduodenectomy (PD) for the management of duodenal polyposis syndromes.
      ,
      • Müller M.W.
      • Dahmen R.
      • Köninger J.
      • Michalski C.W.
      • Hinz U.
      • Hartel M.
      • et al.
      Is there an advantage in performing a pancreas-preserving total duodenectomy in duodenal adenomatosis?.
      ,
      • Ganschow P.
      • Hackert T.
      • Biegler M.
      • Contin P.
      • Hinz U.
      • Büchler M.W.
      • et al.
      Postoperative outcome and quality of life after surgery for FAP-associated duodenal adenomatosis.
      in literature and one (3%) developed diabetes mellitus compared to 0–7% in literature.
      • Walsh R.M.
      • Augustin T.
      • Aleassa E.M.
      • Simon R.
      • El-Hayek K.M.
      • Moslim M.A.
      • et al.
      Comparison of pancreas-preserving total duodenectomy (PPTD) and pancreatoduodenectomy (PD) for the management of duodenal polyposis syndromes.
      ,
      • de Castro S.M.
      • van Eijck C.H.
      • Rutten J.P.
      • Dejong C.H.
      • van Goor H.
      • Busch O.R.
      • et al.
      Pancreas-preserving total duodenectomy versus standard pancreatoduodenectomy for patients with familial adenomatous polyposis and polyps in the duodenum.
      These are all relatively low percentages compared to 30–75% exocrine insufficiency and 11–12% diabetes in series of PD in FAP.
      • Walsh R.M.
      • Augustin T.
      • Aleassa E.M.
      • Simon R.
      • El-Hayek K.M.
      • Moslim M.A.
      • et al.
      Comparison of pancreas-preserving total duodenectomy (PPTD) and pancreatoduodenectomy (PD) for the management of duodenal polyposis syndromes.
      • de Castro S.M.
      • van Eijck C.H.
      • Rutten J.P.
      • Dejong C.H.
      • van Goor H.
      • Busch O.R.
      • et al.
      Pancreas-preserving total duodenectomy versus standard pancreatoduodenectomy for patients with familial adenomatous polyposis and polyps in the duodenum.
      • Müller M.W.
      • Dahmen R.
      • Köninger J.
      • Michalski C.W.
      • Hinz U.
      • Hartel M.
      • et al.
      Is there an advantage in performing a pancreas-preserving total duodenectomy in duodenal adenomatosis?.
      • Caillié F.
      • Paye F.
      • Desaint B.
      • Bennis M.
      • Lefèvre J.H.
      • Parc Y.
      • et al.
      Severe duodenal involvement in familial adenomatous polyposis treated by pylorus-preserving pancreaticoduodenectomy.
      Table 4Most recent series of centers reporting on short and long-term outcomes of PPTD describing at least 5 cases
      Number of patients with FAPReconstructionCD III/IVPOPF grade B/C90-day mortalityPancreatitisNew-onset DMExocrine PI
      Sarmiento 2002 (n = 8)5Billroth I50%38%0%NRNRNR
      Al-Sarireh 2008 (n = 12)6Billroth I50%17%0%8%NRNR
      Müller 2008 (n = 23)13Billroth INR17%3.4%6%0%0%
      Penninga 2011 (n = 13)10Billroth I46%23%0%10%0%NR
      Watanabe 2017 (n = 10)10Billroth I40%40%0%NR0%NR
      Ganschow 2018 (n = 27)27Billroth I44%33%0%22%NR0%
      Walsh 2019 (n = 44)44Billroth I30%14%0%16%7%11%
      Present series (n = 30)30Billroth II53%40%0%17%3%3%
      CD = Clavien–Dindo, POPF = post-operative pancreatic fistula, DM = diabetes mellitus, PI = pancreatic insufficiency, NR = not reported.
      During postoperative endoscopic surveillance, most patients (81%) developed jejunal polyps, more than the 59% of patients in Ji Yoon Yoon et al.
      • Yoon J.Y.
      • Mehta N.
      • Burke C.A.
      • Augustin T.
      • O'Malley M.
      • LaGuardia L.
      • et al.
      The prevalence and significance of jejunal and duodenal bulb polyposis after duodenectomy in familial adenomatous polyposis: retrospective cohort study.
      at an almost equal median duration of endoscopic follow-up (127 versus 119 months). In their study however, more patients underwent an endoscopic intervention (50 versus 37%) and less patients a surgical jejunal resection (3 versus 15%). In literature, one patient was diagnosed with jejunal cancer 16 years after PPTD.
      • Naples R.
      • Simon R.
      • Moslim M.
      • Augustin T.
      • Church J.
      • Burke C.A.
      • et al.
      Long-term outcomes of pancreas-preserving total duodenectomy for duodenal polyposis in familial adenomatous polyposis syndrome.
      None of the patients in the present cohort developed jejunal cancer. In most patients pre- or peroperative endoscopic evaluation of the jejunum was performed when the extent of polyposis reached beyond the ligament of Treitz.
      As patients might have a risk of unexpected cancer in the duodenal resection specimen, some authors advocate an oncologic resection (pancreatoduodenectomy) in patients with severe nonmalignant duodenal polyposis. Caillie et al. showed that in 33% of patients pre-operatively classified as nonmalignant, an invasive duodenal carcinoma was found in the resection specimen.
      • Caillié F.
      • Paye F.
      • Desaint B.
      • Bennis M.
      • Lefèvre J.H.
      • Parc Y.
      • et al.
      Severe duodenal involvement in familial adenomatous polyposis treated by pylorus-preserving pancreaticoduodenectomy.
      Augustin et al. found accidental cancers in 10% of patients.
      • Augustin T.
      • Moslim M.A.
      • Tang A.
      • Walsh R.M.
      Tailored surgical treatment of duodenal polyposis in familial adenomatous polyposis syndrome.
      In the present cohort however, no unexpected cancers were found after PPTD and also during follow up no small bowel malignancies occurred. These results show the oncologic safety of PPTD but also highlight the importance of high-quality endoscopy and patient selection for duodenal surgery.
      Besides choosing between PPTD and PD, attention should be paid to reconstruction allowing postoperative endoscopic surveillance. All centers reporting on PPTD in FAP therefore reconstruct the gastrointestinal tract with a straight anastomosis to the jejunum.
      • Müller M.W.
      • Dahmen R.
      • Köninger J.
      • Michalski C.W.
      • Hinz U.
      • Hartel M.
      • et al.
      Is there an advantage in performing a pancreas-preserving total duodenectomy in duodenal adenomatosis?.
      ,
      • Yoon J.Y.
      • Mehta N.
      • Burke C.A.
      • Augustin T.
      • O'Malley M.
      • LaGuardia L.
      • et al.
      The prevalence and significance of jejunal and duodenal bulb polyposis after duodenectomy in familial adenomatous polyposis: retrospective cohort study.
      • Sarmiento J.M.
      • Thompson G.B.
      • Nagorney D.M.
      • Donohue J.H.
      • Farnell M.B.
      Pancreas-preserving total duodenectomy for duodenal polyposis.
      • Watanabe Y.
      • Ishida H.
      • Baba H.
      • Iwama T.
      • Kudo A.
      • Tanabe M.
      • et al.
      Pancreas-sparing total duodenectomy for Spigelman stage IV duodenal polyposis associated with familial adenomatous polyposis: experience of 10 cases at a single institution.
      • Chung R.S.
      • Church J.M.
      • vanStolk R.
      Pancreas-preserving total duodenectomy: indications, surgical technique, and results.
      • Penninga L.
      • Svendsen L.B.
      Pancreas-preserving total duodenectomy: a 10-year experience.
      ,
      • Al-Sarireh B.
      • Ghaneh P.
      • Gardner-Thorpe J.
      • Raraty M.
      • Hartley M.
      • Sutton R.
      • et al.
      Complications and follow-up after pancreas-preserving total duodenectomy for duodenal polyps.
      Even after PD this is possible by performing an Imanaga reconstruction.
      • Caillié F.
      • Paye F.
      • Desaint B.
      • Bennis M.
      • Lefèvre J.H.
      • Parc Y.
      • et al.
      Severe duodenal involvement in familial adenomatous polyposis treated by pylorus-preserving pancreaticoduodenectomy.
      Some authors state that an isolated blind-ending jejunal limb would result in inadequate endoscopic surveillance.
      • Ganschow P.
      • Hackert T.
      • Biegler M.
      • Contin P.
      • Hinz U.
      • Büchler M.W.
      • et al.
      Postoperative outcome and quality of life after surgery for FAP-associated duodenal adenomatosis.
      However, we showed that complete endoscopic surveillance was achieved in 96% of patients that underwent PPTD with BII reconstruction with a relatively short jejunal limb. This percentage might even be higher, since we only scored endoscopies as complete when visualization of the end of the blind-ending loop was documented. Besides, no patients developed jejunal cancer. Therefore, BII reconstruction seems to be an acceptable option in terms of the ability for future endoscopic surveillance. After PD procedure, BII reconstruction is the standard approach in most centers, and it is hypothesized that after BI reconstruction the risk of pancreatic fistula is higher and its sequelae could be more devastating due to passage of gastric contents along the bilio-pancreatic anastomosis. However, we did not show a reduced risk after BII reconstruction when compared to series on PPTD with BI reconstruction.
      Whether the pylorus should be preserved is another subject of debate. In our center, the pylorus is resected if polyps are present in the bulb or when vascularization of the pylorus is deemed not sufficient. A pylorus-preserving PPTD was performed in 27% of our patients. In other centers, the pylorus and bulb are preserved in most patients with or without mucosectomy of the residual duodenal cuff.
      • Yoon J.Y.
      • Mehta N.
      • Burke C.A.
      • Augustin T.
      • O'Malley M.
      • LaGuardia L.
      • et al.
      The prevalence and significance of jejunal and duodenal bulb polyposis after duodenectomy in familial adenomatous polyposis: retrospective cohort study.
      ,
      • Sarmiento J.M.
      • Thompson G.B.
      • Nagorney D.M.
      • Donohue J.H.
      • Farnell M.B.
      Pancreas-preserving total duodenectomy for duodenal polyposis.
      An argument in favor of pylorus preservation might be that reflux of bile in the stomach will be less common. In the present series, endoscopic features of biliary reflux and/or gastritis were observed in 29% of patients with a preserved pylorus and 79% of patients in whom the pylorus was resected (p = 0.028). Little evidence is available to suggest a potential relation to bile exposure in the stomach and the presence of gastric polyps.
      • Mabrut J.Y.
      • Romagnoli R.
      • Collard J.M.
      • Saurin J.C.
      • Detry R.
      • Mion F.
      • et al.
      Familial adenomatous polyposis predisposes to pathologic exposure of the stomach to bilirubin.
      However, whether biliary reflux predisposes dysplasia in the stomach is unknown. No difference in terms of postoperative delayed gastric emptying between pylorus-preserving and pylorus-resecting procedures were observed in our cohort. A disadvantage of preserving the pylorus and bulb is the presence of remaining polyps or the future development of polyps in the bulb, that be difficult to remove endoscopically as shown by Ji Yoon Yoon et al.
      • Yoon J.Y.
      • Mehta N.
      • Burke C.A.
      • Augustin T.
      • O'Malley M.
      • LaGuardia L.
      • et al.
      The prevalence and significance of jejunal and duodenal bulb polyposis after duodenectomy in familial adenomatous polyposis: retrospective cohort study.
      Although attempted in 5 cases, a complete resection was achieved in 2 polyps of which one showed a recurrence on follow-up endoscopy that was eventually not amenable to complete endoscopic removal. One case-report described a patient with FAP who developed cancer in bulb after pylorus-preserving PD.
      • Murakami Y.
      • Uemura K.
      • Sasaki M.
      • Morifuji M.
      • Hayashidani Y.
      • Sudo T.
      • et al.
      Duodenal cancer arising from the remaining duodenum after pylorus-preserving pancreatoduodenectomy for ampullary cancer in familial adenomatous polyposis.
      In 8 patients with pylorus-preserving PPTD in our study, none developed polyps or cancer in the residual bulb suggesting that preservation of the pylorus is feasible and safe in a selection of patients.
      The main limitation of this study is its retrospective design. Especially extracting data from old endoscopy reports is prone for inaccuracy. Therefore, we were careful in presenting the data and drawing conclusions. Strengths of this study are that to our knowledge this is the only study specifically reporting on PPTD with Billroth II reconstruction and it describes one of the largest series on PPTD. This study provides long-term data with a median follow-up of 125 months, which is the longest follow-up of all studies reporting on PPTD.
      After precise patient selection including endoscopic assessment and a multidisciplinary approach, PPTD should be offered for patients with FAP and extensive nonmalignant duodenal polyposis when endoscopic treatment is deemed impossible. PPTD is a technically demanding and infrequently performed procedure with substantial morbidity and therefore should only be performed by surgeons experienced with this operation and with strict indication. Centers without experience in PPTD might consider still performing PD in these patients or refer them to centers experienced with PPTD when preferred. The advantage of PPTD compared to PD appears primarily on the long-term with preserved exocrine and endocrine pancreatic function. Patients will most likely develop jejunal adenomas over time and therefore life-long expert endoscopic surveillance is warranted. Similar to Billroth I reconstruction, Billroth II reconstruction with short isolated jejunal limb facilitates accurate endoscopic surveillance. Subsequently, next to duodenal cancer, jejunal cancer can be prevented in patients with FAP.

      Declaration of interests

      The authors declare the following financial interests/personal relationships which may be considered as potential competing interests: Arthur S. Aelvoet: none to declare; Barbara A.J. Bastiaansen: none to declare; Paul Fockens: consultancy for Olympus and Cook Medical, research grant from Boston Scientific; Marc G. Besselink: none to declare; Olivier R. Busch: none to declare; Evelien Dekker: endoscopic equipment on loan of FujiFilm and Olympus, received a research grant from FujiFilm. Also received honorarium for consultancy from FujiFilm, Olympus, GI Supply, PAION and Ambu, and speakers' fees from Olympus, GI Supply, Norgine, PAION and FujiFilm.

      References

        • Mallinson E.K.
        • Newton K.F.
        • Bowen J.
        • Lalloo F.
        • Clancy T.
        • Hill J.
        • et al.
        The impact of screening and genetic registration on mortality and colorectal cancer incidence in familial adenomatous polyposis.
        Gut. Oct 2010; 59: 1378-1382https://doi.org/10.1136/gut.2010.212449
        • Karstensen J.G.
        • Burisch J.
        • Pommergaard H.C.
        • Aalling L.
        • Højen H.
        • Jespersen N.
        • et al.
        Colorectal cancer in individuals with familial adenomatous polyposis, based on analysis of the Danish polyposis registry.
        Clin Gastroenterol Hepatol. Oct 2019; 17 (2294–2300.e1)https://doi.org/10.1016/j.cgh.2019.02.008
        • Bülow S.
        • Björk J.
        • Christensen I.J.
        • Fausa O.
        • Järvinen H.
        • Moesgaard F.
        • et al.
        Duodenal adenomatosis in familial adenomatous polyposis.
        Gut. Mar 2004; 53: 381-386https://doi.org/10.1136/gut.2003.027771
        • Spigelman A.D.
        • Williams C.B.
        • Talbot I.C.
        • Domizio P.
        • Phillips R.K.
        Upper gastrointestinal cancer in patients with familial adenomatous polyposis.
        Lancet. Sep 30 1989; 2: 783-785https://doi.org/10.1016/s0140-6736(89)90840-4
        • Björk J.
        • Akerbrant H.
        • Iselius L.
        • Bergman A.
        • Engwall Y.
        • Wahlström J.
        • et al.
        Periampullary adenomas and adenocarcinomas in familial adenomatous polyposis: cumulative risks and APC gene mutations.
        Gastroenterology. Nov 2001; 121: 1127-1135https://doi.org/10.1053/gast.2001.28707
        • Bülow S.
        • Christensen I.J.
        • Højen H.
        • Björk J.
        • Elmberg M.
        • Järvinen H.
        • et al.
        Duodenal surveillance improves the prognosis after duodenal cancer in familial adenomatous polyposis.
        Colorectal Dis. Aug 2012; 14: 947-952https://doi.org/10.1111/j.1463-1318.2011.02844.x
        • Lepistö A.
        • Kiviluoto T.
        • Halttunen J.
        • Järvinen H.J.
        Surveillance and treatment of duodenal adenomatosis in familial adenomatous polyposis.
        Endoscopy. Jun 2009; 41: 504-509https://doi.org/10.1055/s-0029-1214719
        • Wallace M.H.
        • Phillips R.K.
        Upper gastrointestinal disease in patients with familial adenomatous polyposis.
        Br J Surg. Jun 1998; 85: 742-750https://doi.org/10.1046/j.1365-2168.1998.00776.x
        • Groves C.J.
        • Saunders B.P.
        • Spigelman A.D.
        • Phillips R.K.
        Duodenal cancer in patients with familial adenomatous polyposis (FAP): results of a 10 year prospective study.
        Gut. May 2002; 50: 636-641https://doi.org/10.1136/gut.50.5.636
        • Moussata D.
        • Napoleon B.
        • Lepilliez V.
        • Klich A.
        • Ecochard R.
        • Lapalus M.G.
        • et al.
        Endoscopic treatment of severe duodenal polyposis as an alternative to surgery for patients with familial adenomatous polyposis.
        Gastrointest Endosc. Nov 2014; 80: 817-825https://doi.org/10.1016/j.gie.2014.03.012
        • Roos V.H.
        • Bastiaansen B.A.
        • Kallenberg F.G.J.
        • Aelvoet A.S.
        • Bossuyt P.M.M.
        • Fockens P.
        • et al.
        Endoscopic management of duodenal adenomas in patients with familial adenomatous polyposis.
        Gastrointest Endosc. Feb 2021; 93: 457-466https://doi.org/10.1016/j.gie.2020.05.065
        • Scholten L.
        • Mungroop T.H.
        • Haijtink S.A.L.
        • Issa Y.
        • van Rijssen L.B.
        • Koerkamp B.G.
        • et al.
        New-onset diabetes after pancreatoduodenectomy: a systematic review and meta-analysis.
        Surgery. May 17 2018; https://doi.org/10.1016/j.surg.2018.01.024
        • Tseng D.S.
        • Molenaar I.Q.
        • Besselink M.G.
        • van Eijck C.H.
        • Borel Rinkes I.H.
        • van Santvoort H.C.
        Pancreatic exocrine insufficiency in patients with pancreatic or periampullary cancer: a systematic review.
        Pancreas. Mar 2016; 45: 325-330https://doi.org/10.1097/mpa.0000000000000473
        • Walsh R.M.
        • Augustin T.
        • Aleassa E.M.
        • Simon R.
        • El-Hayek K.M.
        • Moslim M.A.
        • et al.
        Comparison of pancreas-preserving total duodenectomy (PPTD) and pancreatoduodenectomy (PD) for the management of duodenal polyposis syndromes.
        Surgery. Oct 2019; 166: 496-502https://doi.org/10.1016/j.surg.2019.05.060
        • de Castro S.M.
        • van Eijck C.H.
        • Rutten J.P.
        • Dejong C.H.
        • van Goor H.
        • Busch O.R.
        • et al.
        Pancreas-preserving total duodenectomy versus standard pancreatoduodenectomy for patients with familial adenomatous polyposis and polyps in the duodenum.
        Br J Surg. Nov 2008; 95: 1380-1386https://doi.org/10.1002/bjs.6308
        • Müller M.W.
        • Dahmen R.
        • Köninger J.
        • Michalski C.W.
        • Hinz U.
        • Hartel M.
        • et al.
        Is there an advantage in performing a pancreas-preserving total duodenectomy in duodenal adenomatosis?.
        Am J Surg. Jun 2008; 195: 741-748https://doi.org/10.1016/j.amjsurg.2007.08.061
        • Caillié F.
        • Paye F.
        • Desaint B.
        • Bennis M.
        • Lefèvre J.H.
        • Parc Y.
        • et al.
        Severe duodenal involvement in familial adenomatous polyposis treated by pylorus-preserving pancreaticoduodenectomy.
        Ann Surg Oncol. Sep 2012; 19: 2924-2931https://doi.org/10.1245/s10434-012-2221-x
        • Alderlieste Y.A.
        • Bastiaansen B.A.
        • Mathus-Vliegen E.M.
        • Gouma D.J.
        • Dekker E.
        High rate of recurrent adenomatosis during endoscopic surveillance after duodenectomy in patients with familial adenomatous polyposis.
        Fam Cancer. Dec 2013; 12: 699-706https://doi.org/10.1007/s10689-013-9648-5
        • Yoon J.Y.
        • Mehta N.
        • Burke C.A.
        • Augustin T.
        • O'Malley M.
        • LaGuardia L.
        • et al.
        The prevalence and significance of jejunal and duodenal bulb polyposis after duodenectomy in familial adenomatous polyposis: retrospective cohort study.
        Ann Surg. Dec 16 2019; https://doi.org/10.1097/sla.0000000000003740
        • Sarmiento J.M.
        • Thompson G.B.
        • Nagorney D.M.
        • Donohue J.H.
        • Farnell M.B.
        Pancreas-preserving total duodenectomy for duodenal polyposis.
        Arch Surg. May 2002; 137 (discussion 562-3): 557-562https://doi.org/10.1001/archsurg.137.5.557
        • Watanabe Y.
        • Ishida H.
        • Baba H.
        • Iwama T.
        • Kudo A.
        • Tanabe M.
        • et al.
        Pancreas-sparing total duodenectomy for Spigelman stage IV duodenal polyposis associated with familial adenomatous polyposis: experience of 10 cases at a single institution.
        Fam Cancer. Jan 2017; 16: 91-98https://doi.org/10.1007/s10689-016-9932-2
        • Chung R.S.
        • Church J.M.
        • vanStolk R.
        Pancreas-preserving total duodenectomy: indications, surgical technique, and results.
        Surgery. Mar 1995; 117: 254-259https://doi.org/10.1016/s0039-6060(05)80198-9
        • Penninga L.
        • Svendsen L.B.
        Pancreas-preserving total duodenectomy: a 10-year experience.
        J Hepatobiliary Pancreat Sci. Sep 2011; 18: 717-723https://doi.org/10.1007/s00534-011-0382-9
        • Ganschow P.
        • Hackert T.
        • Biegler M.
        • Contin P.
        • Hinz U.
        • Büchler M.W.
        • et al.
        Postoperative outcome and quality of life after surgery for FAP-associated duodenal adenomatosis.
        Langenbecks Arch Surg. Feb 2018; 403: 93-102https://doi.org/10.1007/s00423-017-1625-2
        • Al-Sarireh B.
        • Ghaneh P.
        • Gardner-Thorpe J.
        • Raraty M.
        • Hartley M.
        • Sutton R.
        • et al.
        Complications and follow-up after pancreas-preserving total duodenectomy for duodenal polyps.
        Br J Surg. Dec 2008; 95: 1506-1511https://doi.org/10.1002/bjs.6412
        • Naples R.
        • Simon R.
        • Moslim M.
        • Augustin T.
        • Church J.
        • Burke C.A.
        • et al.
        Long-term outcomes of pancreas-preserving total duodenectomy for duodenal polyposis in familial adenomatous polyposis syndrome.
        J Gastrointest Surg. May 14 2020; https://doi.org/10.1007/s11605-020-04621-7
        • Augustin T.
        • Moslim M.A.
        • Tang A.
        • Walsh R.M.
        Tailored surgical treatment of duodenal polyposis in familial adenomatous polyposis syndrome.
        Surgery. Mar 2018; 163: 594-599https://doi.org/10.1016/j.surg.2017.10.035
        • Mabrut J.Y.
        • Romagnoli R.
        • Collard J.M.
        • Saurin J.C.
        • Detry R.
        • Mion F.
        • et al.
        Familial adenomatous polyposis predisposes to pathologic exposure of the stomach to bilirubin.
        Surgery. Nov 2006; 140: 818-823https://doi.org/10.1016/j.surg.2006.02.013
        • Murakami Y.
        • Uemura K.
        • Sasaki M.
        • Morifuji M.
        • Hayashidani Y.
        • Sudo T.
        • et al.
        Duodenal cancer arising from the remaining duodenum after pylorus-preserving pancreatoduodenectomy for ampullary cancer in familial adenomatous polyposis.
        J Gastrointest Surg. Mar 2005; 9: 389-392https://doi.org/10.1016/j.gassur.2004.07.010