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  • Endoscopic papillectomy versus surgical ampullectomy for adenomas and early cancers of the papilla: a retrospective Pancreas2000/European Pancreatic Club analysis

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Endoscopy
Original research
Endoscopic papillectomy versus surgical ampullectomy for adenomas and early cancers of the papilla: a retrospective Pancreas2000/European Pancreatic Club analysis
  1. Marcus Hollenbach1,2,
  2. Christian Heise3,4,
  3. Einas Abou-Ali5,
  4. Aiste Gulla6,7,
  5. Francesco Auriemma8,
  6. Kevin Soares9,
  7. Galen Leung10,
  8. Mark A Schattner11,
  9. William R Jarnagin9,
  10. Tiegong Wang9,12,
  11. Fabrice Caillol13,
  12. Marc Giovannini13,
  13. Yanis Dahel13,
  14. Thilo Hackert14,
  15. Woo Hyun Paik15,
  16. Alessandro Zerbi16,17,
  17. Gennaro Nappo16,17,
  18. Bertrand Napoleon18,
  19. Urban Arnelo19,20,
  20. Erik Haraldsson19,21,
  21. Asif Halimi19,20,
  22. Alexander Waldthaler22,23,
  23. Uwe Will24,
  24. Rita Saadeh25,
  25. Viliam Masaryk25,
  26. Sophia E van der Wiel26,
  27. Marco J Bruno26,
  28. Enrique Perez-Cuadrado-Robles27,28,
  29. Pierre Deprez28,
  30. Alain Sauvanet29,
  31. Louisa Bolm30,
  32. Tobias Keck30,
  33. Régis Souche31,
  34. Jean-Michel Fabre32,
  35. Nicolas Musquer33,
  36. Georg Kähler34,35,
  37. Steffen Seyfried34,35,
  38. Maria Chiara Petrone36,
  39. Alberto Mariani36,
  40. Piera Zaccari36,
  41. Giulio Belfiori37,
  42. Stefano Crippa37,
  43. Massimo Falconi37,
  44. Stefano Partelli37,
  45. Bengisu Yilmaz38,
  46. Ihsan Ekin Demir38,39,
  47. Güralp O Ceyhan40,
  48. Sohei Satoi41,42,
  49. Jean Marc Regimbeau43,
  50. Johan Gagniére44,45,
  51. Alessandro Repici46,47,
  52. Andrea Anderloni48,
  53. Charles Vollmer49,
  54. Fabio Casciani49,50,
  55. Marco Del Chiaro51,
  56. Atsushi Oba42,
  57. Richard D Schulick51,
  58. Arthur Berger52,
  59. Laura Maggino50,
  60. Roberto Salvia50,
  61. Peter Schemmer53,
  62. Doerte Wichmann54,
  63. Yosuke Inoue55,
  64. Mario Dinis-Ribeiro56,57,
  65. Ana Laranjo56,
  66. Diogo Libanio56,57,
  67. Tobias Kleemann58,
  68. Vasile Sandru59,60,
  69. Madaline Ilie60,61,
  70. Reea Ahola62,63,
  71. Johanna Laukkarinen62,63,
  72. Brigitte Schumacher64,
  73. David Albers64,
  74. Tiago Cúrdia Gonçalves65,66,67,
  75. Louise Barbier68,
  76. Ephrem Salamé68,
  77. Tobias J Weismüller69,70,
  78. Dominik Heling70,
  79. Arnaud Alves71,72,
  80. Elias Karam68,
  81. Nicolas Regenet73,
  82. Ana Dugic4,74,
  83. Steffen Muehldorfer74,
  84. Stéphanie Truant75,
  85. Karel Caca76,
  86. Benjamin Meier76,
  87. Bogdan P Miutescu77,
  88. Marcel Tantau78,79,
  89. David Birnbaum80,
  90. Rainer Christoph Miksch81,
  91. Edris Wedi82,83,
  92. Katrin Salzmann83,
  93. Matthieu Bruzzi84,
  94. Renato M Lupinacci85,
  95. Patrice David86,
  96. Charles De Ponthaud87,
  97. Arthur Schmidt88,89,
  98. Sara Regnér90,
  99. Sebastien Gaujoux91
  100. The ESAP study group
    1. 1 Department of Gastroenterology, Endocrinology, Metabolism and Clinical Infectiology, University Hospital of Giessen and Marburg Campus Marburg, Marburg, Germany
    2. 2 Division of Gastroenterology, Medical Department II, University of Leipzig Medical Center, Leipzig, Germany
    3. 3 Medical Department I, Martin-Luther-Universitat Halle-Wittenberg, Halle, Germany
    4. 4 Medical Department IV, Heidelberg University, Heidelberg, Germany
    5. 5 Department of Gastroenterology, Digestive Oncology and Endoscopy, Paris Descartes University Paris, Paris, France
    6. 6 Department of Surgery, George Washington University, School of Medicine and Health Sciences, Washington DC, District of Columbia, USA
    7. 7 Center of Abdominal Center, Vilnius University hospital Santaros clinics, Institute of Clinical Medicine, Faculty of Medicine, Vilnius University, Vilnius, Lithuania
    8. 8 Gastrointestinal Endoscopy, Humanitas Mater Domini, Castellanza, Italy
    9. 9 Hepatopancreatobiliary Service, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, New York, USA
    10. 10 Division of Gastroenterology and Hepatology, University of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania, USA
    11. 11 Gastroenterology, Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, New York, USA
    12. 12 Department of Surgery, Cangzhou Central Hospital, Hebei, China
    13. 13 Digestive Endoscopy Department, Institut Paoli Calmettes, Marseille, France
    14. 14 Department of General, Visceral and Transplantation Surgery, University of Heidelberg, Heidelberg, Germany
    15. 15 Division of Gastroenterology, Department of Internal Medicine, Seoul National University Hospital, Seoul, Korea
    16. 16 Department of Biochemical Sciences, Humanitas University, Pieve Emanuele, Milan, Italy
    17. 17 Pancreatic Surgery Unit, IRCCS Humanitas Research Hospital, Rozzano, Milan, Italy
    18. 18 Endoscopie Digestive, hopital privé Jean Mermoz, Générale de Santé, Lyon, France
    19. 19 Division of Surgery, CLINTEC, Karolinska Institutet, Stockholm, Sweden
    20. 20 Department of Surgical and Perioperative Sciences, Surgery, Umea University, Umea, Sweden
    21. 21 Department of Surgery, Skaraborg Hospital, Skovde, Sweden
    22. 22 Department of Upper Abdominal Diseases, Karolinska University Hospital, Stockholm, Sweden
    23. 23 Department of Medicine Huddinge, Karolinska University Hospital, Stockholm, Sweden
    24. 24 Department of Gastroenterology, Hepatology, Diabetology and General Internal Medicine, SRH Wald-Klinikum Gera GmbH, Gera, Germany
    25. 25 Department of Gastroenterology, Hepatology, Diabetes and General Internal Medicine, SRH Wald-Klinikum Gera, Gera, Germany
    26. 26 Department of Gastroenterology and Hepatology, Erasmus Medical Center, University Medical Center Rotterdam, Rotterdam, The Netherlands
    27. 27 Interventional Endoscopy, Department of Gastroenterology, Georges-Pompidou European Hospital, Paris, France
    28. 28 Department of Gastroenterology, Cliniques universitaires Saint-Luc, Bruxelles, Belgium
    29. 29 Departement of Digestive Surgery, Beaujon Hospital APHP, Clichy, France
    30. 30 Department of Surgery, University Medical Center Schleswig Holstein, Campus Luebeck, Luebeck, Germany
    31. 31 Department of Digestive Surgery, Centre Hospitalier Universitaire de Montpellier, Montpellier, France
    32. 32 Department of Digestive and Transplantation Surgery, Centre Hospitalier Universitaire de Montpellier, Montpellier, France
    33. 33 Clinique Santé Atlantique, Saint Herblain, France
    34. 34 Interdisziplinary Endoscopy Unit, Mannheim Medical Center, Ruprecht Karls University Heidelberg Faculty of Medicine, Mannheim, Germany
    35. 35 Department of Surgery, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
    36. 36 Pancreato-Biliary Endoscopy and Endosonography Division, Pancreas Translational & Clinical Research Center, San Raffaele Scientific Institute IRCCS, Vita-Salute San Raffaele University, Milan, Italy
    37. 37 Department of Pancreatic Surgery, Vita-Salute San Raffaele University, Milano, Italy
    38. 38 Department of Surgery, TUM University Hospital, Klinikum rechts der Isar, Munich, Germany
    39. 39 Else Kröner Clinician Scientist Professor for Translational Pancreatic Surgery, TUM University Hospital, Klinikum rechts der Isar, Munich, Germany
    40. 40 Department of General Surgery, HPB-Unit, School of Medicine, Acibadem Mehmet Ali Aydinlar University, Istanbul, Turkey
    41. 41 Department of Surgery, Kansai Medical University, Hirakata, Osaka, Japan
    42. 42 Department of Surgery, University of Colorado - Anschutz Medical Campus, Aurora, Colorado, USA
    43. 43 Departement of Digestive Surgery, Centre hospitalo-universitaire Amiens-Picardie, Amiens, France
    44. 44 Department of Digestive and Hepatobiliary Surgery, Estaing University Hospital, Clermont-Ferrand, France
    45. 45 U1071 Inserm, Clermont-Auvergne University, Clermont-Ferrand, France
    46. 46 Department of Biomedical Sciences, Humanitas University, Pieve Emanuele, Italy
    47. 47 Endoscopy Unit, Humanitas Clinical and Research Center - IRCCS, Rozzano, Italy
    48. 48 Gastroenterology and Digestive Endoscopy Unit, IRCCS Foundation Policlinico San Matteo, Pavia, Italy
    49. 49 Department of Surgery, University of Pennsylvania, Philadelphia, Pennsylvania, USA
    50. 50 Unit of General and Pancreatic Surgery, The Pancreas Institute, University of Verona Hospital Trust, Verona, Italy
    51. 51 Department of Surgery, University of Colorado School of Medicine - Anschutz Medical Campus, Aurora, Colorado, USA
    52. 52 Department of Gastroenterology and digestive endoscopy, CHU Bordeaux, Bordeaux, France
    53. 53 Department of General, Visceral and Transplantation Surgery, University of Graz, Graz, Austria
    54. 54 Department of General, Visceral and Transplantation Surgery, University Hospital of Tübingen, Tubingen, Germany
    55. 55 Department of Hepato-Biliary-Pancreatic Surgery, Cancer Institute Hospital, Tokyo, Japan
    56. 56 Department of Gastroenterology, Instituto Português de Oncologia do Porto, Porto, Portugal
    57. 57 RISE@CI-IPO (Health Research Network), Portuguese Oncology Institute of Porto (IPO Porto), Porto, Portugal
    58. 58 Department of Gastroenterology and Rheumatology, Carl-Thiem-Klinikum Cottbus, Cottbus, Germany
    59. 59 Department of Gastroenterology and Interventional Endoscopy, Clincal Emergency Hospital, Bucuresti, Romania
    60. 60 Carol Davila University of Medicine and Pharmacy, Bucuresti, Romania
    61. 61 Clinical Emergency Hospital, Bucuresti, Romania
    62. 62 Faculty of Medicine and Health Technology, Tampere University, Tampere, Finland
    63. 63 Department of Gastroenterology and Alimentary Tract Surgery, Tampere University Hospital, Tampere, Finland
    64. 64 Department of Medicine and Gastroenterology, Contilia Clinic Essen, Essen, Germany
    65. 65 Department of Gastroenterology, Unidade Local de Saúde do Alto Ave, Hospital de Guimarães, Guimaraes, Portugal
    66. 66 School of Medicine, Life and Health Sciences Research Institute, University of Minho, Braga, Portugal
    67. 67 ICVS/3B’s, PT Government Associate Laboratory, Braga, Portugal
    68. 68 Departement of Digestive Surgery, Centre hospitalo-universitaire de Tours, Tours, France
    69. 69 Department of Internal Medicine - Gastroenterology and Oncology, Vivantes Humboldt Hospital, Berlin, Germany
    70. 70 Department of Internal Medicine I, University Hospital Bonn, Bonn, Germany
    71. 71 Calvados Digestive Cancer Registry, INSERM U1086 ANTICIPE, Normandy Caen University, Caen, France
    72. 72 Department of Digestive Surgery, University Hospital Centre, Caen, France
    73. 73 Department of Digestive Surgery, Centre Hospitalier Universitaire de Nantes, Nantes, France
    74. 74 Department of Gastroenterology, Friedrich-Alexander-University Erlangen-Nuremberg, Medical Campus Oberfranken, Bayreuth, Germany
    75. 75 Deparment of Digestive Surgery, Centre hospitalo-universitaire de Lille, Lille, France
    76. 76 Department of Medicine, Gastroenterology, Hematology, Oncology, Pneumology, Diabetes and Infectious Diseases, RKH Clinic Ludwigsburg, Ludwigsburg, Germany
    77. 77 Department of Gastroenterology and Hepatology, Victor Babeș University of Medicine and Pharmacy, Timișoara, Romania
    78. 78 Hepatology Department, Regional Institute of Gastroenterology and Hepatology Prof Dr Octavian Fodor, Cluj-Napoca, Romania
    79. 79 3rd Medical Clinic, Iuliu Hagieganu University of Medicine and Pharmacy Faculty of Medicine, Cluj Napoca, Romania
    80. 80 Department of Digestive Surgery, Aix-Marseille University, Marseille, France
    81. 81 Department of General, Visceral, and Transplantation Surgery, Ludwig Maximilian University Munich, Munich, Germany
    82. 82 Department of Gastroenterology, Gastrointestinal Oncology and Interventional Endoscopy, Sana Clinic Offenbach, Offenbach, Germany
    83. 83 Department of Gastroenterology and Gastrointestinal Oncology, University of Göttingen, Gottingen, Germany
    84. 84 Department of Digestive Surgery, Hôpital Européen Georges Pompidou, APHP, Paris, France
    85. 85 Department of Digestive Surgery, Groupe hospitalier Diaconesses Croix Saint-Simon, Paris, France
    86. 86 Department of Digestive Surgery, Hopital Louis Pasteur, Colmar, France
    87. 87 Department of Pancreatic and Endocrine Surgery, Pitié-Salpetriere Hospital, Médecine Sorbonne Université, APHP, Paris, France
    88. 88 Department of Medicine II, Medical Center-University of Freiburg, Freiburg, Germany
    89. 89 Department of Gastroenterology, Robert Bosch Hospital / Bosch Health Campus, Stuttgart, Germany
    90. 90 Surgery Research Unit, Department of Clinical Sciences Malmö, Skåne University Hospital, Lund University, Malmö, Sweden
    91. 91 Department of Digestive and HBP Surgery, Groupe Hospitalier Pitié-Salpêtrière, Médecine Sorbonne Université APHP, Paris, France
    1. Correspondence to Dr Marcus Hollenbach; marcus.hollenbach{at}web.de

    Abstract

    Objective Ampullary neoplastic lesions can be resected by endoscopic papillectomy (EP) or transduodenal surgical ampullectomy (TSA) while pancreaticoduodenectomy is reserved for more advanced lesions. We present the largest retrospective comparative study analysing EP and TSA.

    Design Of all patients in the database, lesions with prior interventions, benign histology advanced malignancy (T2 and more), patients with hereditary syndromes and those undergoing pancreatoduodenectomy were excluded. All remaining cases as well as a subgroup of them, after propensity-score matching (nearest-neighbour-method) based on age, gender, anthropometrics, comorbidities, size and histological subtype, were analysed. The median follow-up was 21 months (IQR 10–47) after the primary intervention. Primary outcomes were rates of complete resection (R0) and complications. Groups were compared by Fisher’s exact or χ2 test, Mann-Whitney-U-test and log-rank test for survival.

    Results Of 1673 patients in the database, 1422 underwent EP and 251 TSA. Of them, 23.2% were excluded for missing or inconclusive data and 19.8% of patients for prior interventions or hereditary syndromes. Final histology showed in 24.2% of EP and 14.8% of TSA patients a histology other than adenoma or adenocarcinoma while advanced cancers were recorded in 10.9% of EP and 36.6% of TSA patients. Finally, 569 EP and 63 TSA were included in the overall analysis, with a higher rate of more advanced cases and higher R0 resection rates in the TSA groups (90.5% vs 73.1%; p<0.01), with additional ablation in the EP group in 14.4%. Severe adverse event rates were 3.2% (TSA) vs 1.9% (EP). Recurrence after histological R0 resection was 16% (EP) vs 3.2% (TSA; p=0.01), and additional therapy for R1 resection was applied in 67% of the 159 cases. Propensity-score-based matching identified 62 pairs of EP/TSA patients with comparable baseline patient and lesion characteristics. The initial R0-rate was 72.6% (EP) compared with 90.3% (TSA, p=0.02) with recurrences found in 8% (EP) vs 3.2% (TSA; p=0.07); reinterventions were more frequent in the EP group. Overall survival was comparable.

    Conclusions The rate of patients with poor indications due to non-neoplastic disease or advanced cancer is still high for both EP and TSA; multiple retreatments were necessary for EP. Although EP can be considered an appropriate primary therapy for certain ampullary adenomas, case selection for both therapies (especially with regard to the best step-up approach) should be studied further.

    • PANCREATICODUODENECTOMY
    • ENDOSCOPIC PROCEDURES
    • ENDOSCOPIC RETROGRADE PANCREATOGRAPHY
    • PANCREATIC CANCER
    • PANCREATIC TUMOURS

    Data availability statement

    Data are available on reasonable request. All data relevant to the study are included in the article or uploaded as online supplemental information.

    https://doi.org/10.1136/gutjnl-2022-327996

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      Data availability statement

      Data are available on reasonable request. All data relevant to the study are included in the article or uploaded as online supplemental information.

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      Footnotes

      • MH and CH are joint first authors.

      • SR and SG are joint senior authors.

      • X @KevinCSoaresMD, @steffen_sey, @StefanoCrippa6, @diogolibanio, @AnaDugic

      • MH and CH contributed equally.

      • SR and SG contributed equally.

      • Correction notice This article has been corrected since it published Online First. The equal contribution statement has been updated.

      • Collaborators Albrecht Hoffmeister (Division of Gastroenterology, Medical Department II, University of Leipzig Medical Center, Leipzig, Germany), Kien Vu Trung (Division of Gastroenterology, Medical Department II, University of Leipzig Medical Center, Leipzig, Germany), Jonas Rosendahl (Medical Department I, Martin-Luther University Halle-Wittenberg, Halle, Germany), Sebastian Krug (Medical Department I, Martin-Luther University Halle-Wittenberg, Halle, Germany; Medical Departmen IV—Gastroenterology, Hepatology, Infectious Diseases, Heidelberg University, Heidelberg, Germany), Lumir Kunovsky, Patrick Michl (Medical Department I, Martin-Luther University Halle-Wittenberg, Halle, Germany; Medical Departmen IV—Gastroenterology, Hepatology, Infectious Diseases, Heidelberg University, Heidelberg, Germany), Jens Werner (Department of General, Visceral and Transplantation Surgery, Ludwig Maximilian University Munich, Munich, Germany), Kestutis Strupas (Department of Surgery, Lithuanian University of Health Sciences, Santaros Klinikos, Kaunas, Lithuania), Lilian Schwarz (Department of Digestive Surgery, Hôpital Charles-Nicolle, Centre Hospitalier Universitaire de Rouen, Rouen, France), Moritz Schiemer (Department of Medicine II, University of Freiburg Medical Center, Freiburg, Germany), Tullio Piardi (Department of Digestive Surgery, Centre Hospitalier Universitaire de Reims, Reims, France), Martin Brunel (Department of Digestive Surgery, Hôpital André Mignot, Versailles, France), Jean C. Vaillant(Department of Digestive and HBP Surgery, Groupe Hospitalier Pitié-Salpêtrière APHP, Médecine Sorbonne Université, Paris, France), Celine Lejeune (Medical Department, Hôpital de la Salpêtrière, APHP, Paris, France), Raffaele Brustia (Department of Digestive and Hepato-Pancreatic-Biliary Surgery, DMU CARE, Assistance Publique-Hôpitaux de Paris (AP-HP), Hôpitaux Universitaires Henri Mondor, Créteil, France; Inserm U955, Team 'Pathophysiology and Therapy of Chronic Viral Hepatitis and Related Cancers', France-Assistance Publique-Hôpitaux de Paris, Créteil, France), Rim Cherif (Department of Digestive and Hepato-Pancreatic-Biliary Surgery, DMU CARE, Assistance Publique-Hôpitaux de Paris (AP-HP), Hôpitaux Universitaires Henri Mondor, Créteil, France; Inserm U955, Team 'Pathophysiology and Therapy of Chronic Viral Hepatitis and Related Cancers', France-Assistance Publique-Hôpitaux de Paris, Créteil, France), Paul-Noet Dumont (Department of Divbestive Surgery Hôpital de la Croix-Rousse, Lyon, France), Frederic Prat (Department of digestive, hepatobiliary and endocrine surgery, Cochin Hospital, APHP, and Université de Paris, Paris, France), J. Matthias Löhr (Division of Surgery, CLINTEC, Karolinska Institutet, Stockholm, Sweden)

      • Contributors MH and SG are guarantors and are responsible for overall content. MH and CH contributed equally and shared first authorship. SR and SG jointly supervised the project and shared senior authorship. MH designed the study, collected data, analysed data, interpreted data, wrote and submitted the manuscript. CH designed the study, collected data and revised the manuscript. EA-A designed the study, collected data and revised the manuscript. FA collected data and revised the manuscript. AG collected data and revised the manuscript. SR designed the study, collected data, interpreted data and revised the manuscript. SG designed the study, collected data, interpreted data and revised the manuscript. KSoares, GL, MAS, WRJ, TW, FCaillol, MG, YD, TH, WHP, AZ, GN, BN, UA, EH, AHalimi, AW, UW, RSaadeh, VM, SEvdW, MBruno, EPCR, PDeprez, ASauvanet, LBolm, TKeck, RSouche, J-MF, NM, GK, SSeyfried, MCP, AM, ZP, GB, SC, MF, SP, BY, IED, GOC, SSatoi, JMR, JG, AR, AAnderloni, CV, FCasciani, MDC, AO, RDS, AB, LM, RSalvia, PS, DW, YI, MDR, AL, DL, TKleemann, VS, MI, RA, JL, BS, DA, TC, LBarbier, ES, TJW, DH, AAlves, EK, NR, AD, SM, ST, KC, BM, BPM, MT, DB, RCM, EW, KSalzmann, MBruzzi, RML, PDavid, ASchmidt and CDP. AHoffmeister, KVT, JR, SK, PM, JW, KStrupas, LS, MS, TP, MBrunel, JCV, CL, RB, RC, P-ND, FP and JML collected data and revised the manuscript. All authors approved the manuscript.

      • Funding The authors have not declared a specific grant for this research from any funding agency in the public, commercial or not-for-profit sectors.

      • Competing interests MH: Honoraria from FUJIFILM for lectures and expert panel. Honoraria from Falk Foundation for lectures. MBruno: Boston Scientific: consultant (money to institution), support for industry and investigator-initiated studies. Cook Medical: consultant (money to institution), support for industry and investigator-initiated studies. Pentax Medical: consultant (money to institution), support for investigator-initiated studies. Mylan: lecturer, support for investigator-initiated studies. ChiRoStim: support for investigator-initiated studies.

        MDC received a research grant Boston from Haemonetics,INC and he is co-PI of a Boston Scientific sponsored study

      • Patient and public involvement Patients and/or the public were not involved in the design, or conduct, or reporting, or dissemination plans of this research.

      • Provenance and peer review Not commissioned; externally peer reviewed.

      • Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.