Surgical Resection for Pancreatic Cancer Using the International Study Group of Pancreatic Surgery (ISGPS) Classifications

  • Thilo Hackert
  • Christoph W. Michalski
  • Markus W. Büchler
Reference work entry


The International Study Group of Pancreatic Surgery (ISGPS) has published a number of definitions within the last decade to standardize terminology and reporting in the field of pancreatic surgery. Furthermore, the group has also extended their approach of summarizing expert opinions in terms of recommendations for the surgical treatment of pancreatic cancer. These definitions and consensus statements have been highly accepted in the worldwide surgical community, and the citations of the respective papers are steadily increasing, which underlines their importance not only in clinical practice but also in the setting of study conductance and scientific reporting. Besides the initial definitions of postoperative complications (postoperative pancreatic fistula, hemorrhage, and delayed gastric emptying), the recent ISGPS publications have addressed important issues of pancreatic cancer (PDAC) surgery, especially with regard to preoperative evaluation of resectability, extended resections, and lymph node management during PDAC resection. Currently, more ISGPS publications are being prepared to cover the entire field of surgical and perioperative management in pancreatic surgery.

This chapter gives a general overview of the ISGPS definitions and consensus recommendations and, in addition, puts a special focus on the publications of the group dealing with PDAC surgery.


Pancreatic cancer International Study Group for Pancreatic Surgery Consensus statement Lymphadenectomy Borderline resectable pancreatic cancer Extended resection 


  1. 1.
    Bassi C, et al. Postoperative pancreatic fistula: an international study group (ISGPF) definition. Surgery. 2005;138(1):8–13.CrossRefGoogle Scholar
  2. 2.
    Bassi C, et al. Pancreatic fistula rate after pancreatic resection. The importance of definitions. Dig Surg. 2004;21(1):54–9.CrossRefGoogle Scholar
  3. 3.
    Hackert T, Hinz U, Pausch T, Fesenbeck I, Strobel O, Schneider L, Fritz S, Büchler MW. Postoperative pancreatic fistula: we need to redefine grades B and C. Surgery. 2016;159(3):872–7.CrossRefGoogle Scholar
  4. 4.
    Hackert T, et al. Postoperative pancreatic fistula: we need to redefine grades B and C. Surgery. 2016;159(3):872–7.CrossRefGoogle Scholar
  5. 5.
    Wente MN, et al. Postpancreatectomy hemorrhage (PPH): an International Study Group of Pancreatic Surgery (ISGPS) definition. Surgery. 2007;142(1):20–5.CrossRefGoogle Scholar
  6. 6.
    Wente MN, et al. Delayed gastric emptying (DGE) after pancreatic surgery: a suggested definition by the International Study Group of Pancreatic Surgery (ISGPS). Surgery. 2007;142(5):761–8.CrossRefGoogle Scholar
  7. 7.
    Shukla PJ, et al. Toward improving uniformity and standardization in the reporting of pancreatic anastomoses: a new classification system by the International Study Group of Pancreatic Surgery (ISGPS). Surgery. 2010;147(1):144–53.CrossRefGoogle Scholar
  8. 8.
    Tol JA, et al. Definition of a standard lymphadenectomy in surgery for pancreatic ductal adenocarcinoma: a consensus statement by the International Study Group on Pancreatic Surgery (ISGPS). Surgery. 2014;156(3):591–600.CrossRefGoogle Scholar
  9. 9.
    Hartwig W, et al. Extended pancreatectomy in pancreatic ductal adenocarcinoma: definition and consensus of the International Study Group for Pancreatic Surgery (ISGPS). Surgery. 2014;156(1):1–14.CrossRefGoogle Scholar
  10. 10.
    Bockhorn M, et al. Borderline resectable pancreatic cancer: a consensus statement by the International Study Group of Pancreatic Surgery (ISGPS). Surgery. 2014;155(6):977–88.CrossRefGoogle Scholar
  11. 11.
    Klauss M, et al. A new invasion score for determining the resectability of pancreatic carcinomas with contrast-enhanced multidetector computed tomography. Pancreatology. 2008;8(2):204–10.CrossRefGoogle Scholar
  12. 12.
    Shrikhande SV, et al. Multimodality imaging of pancreatic ductal adenocarcinoma: a review of the literature. HPB (Oxford). 2012;14(10):658–68.CrossRefGoogle Scholar
  13. 13.
    Tempero MA, et al. Pancreatic adenocarcinoma, version 2.2014: featured updates to the NCCN guidelines. J Natl Compr Cancer Netw. 2014;12(8):1083–93.CrossRefGoogle Scholar
  14. 14.
    Zhou Y, et al. Pancreatectomy combined with superior mesenteric vein-portal vein resection for pancreatic cancer: a meta-analysis. World J Surg. 2012;36(4):884–91.CrossRefGoogle Scholar
  15. 15.
    Pedrazzoli S, et al. Standard versus extended lymphadenectomy associated with pancreatoduodenectomy in the surgical treatment of adenocarcinoma of the head of the pancreas: a multicenter, prospective, randomized study. Lymphadenectomy Study Group. Ann Surg. 1998;228(4):508–17.CrossRefGoogle Scholar
  16. 16.
    Yeo CJ, et al. Pancreaticoduodenectomy with or without extended retroperitoneal lymphadenectomy for periampullary adenocarcinoma: comparison of morbidity and mortality and short-term outcome. Ann Surg. 1999;229(5):613–22; discussion 622–4.CrossRefGoogle Scholar
  17. 17.
    Yeo CJ, et al. Pancreaticoduodenectomy with or without distal gastrectomy and extended retroperitoneal lymphadenectomy for periampullary adenocarcinoma, part 2: randomized controlled trial evaluating survival, morbidity, and mortality. Ann Surg. 2002;236(3):355–66; discussion 366–8.CrossRefGoogle Scholar
  18. 18.
    Farnell MB, et al. A prospective randomized trial comparing standard pancreatoduodenectomy with pancreatoduodenectomy with extended lymphadenectomy in resectable pancreatic head adenocarcinoma. Surgery. 2005;138(4):618–28; discussion 628–30.CrossRefGoogle Scholar
  19. 19.
    Riall TS, et al. Pancreaticoduodenectomy with or without distal gastrectomy and extended retroperitoneal lymphadenectomy for periampullary adenocarcinoma – part 3: update on 5-year survival. J Gastrointest Surg. 2005;9(9):1191–204; discussion 1204–6.CrossRefGoogle Scholar
  20. 20.
    Nimura Y, et al. Standard versus extended lymphadenectomy in radical pancreatoduodenectomy for ductal adenocarcinoma of the head of the pancreas: long-term results of a Japanese multicenter randomized controlled trial. J Hepatobiliary Pancreat Sci. 2012;19(3):230–41.CrossRefGoogle Scholar
  21. 21.
    Michalski CW, et al. Systematic review and meta-analysis of standard and extended lymphadenectomy in pancreaticoduodenectomy for pancreatic cancer. Br J Surg. 2007;94(3):265–73.CrossRefGoogle Scholar
  22. 22.
    Kawarada Y. New classification of pancreatic carcinoma – Japan Pancreas Society. Nihon Shokakibyo Gakkai Zasshi. 2003;100(8):974–80.PubMedGoogle Scholar
  23. 23.
    Valsangkar NP, et al. N0/N1, PNL, or LNR? The effect of lymph node number on accurate survival prediction in pancreatic ductal adenocarcinoma. J Gastrointest Surg. 2013;17(2):257–66.CrossRefGoogle Scholar
  24. 24.
    Hartwig W, et al. Pancreatic cancer surgery in the new millennium: better prediction of outcome. Ann Surg. 2011;254(2):311–9.CrossRefGoogle Scholar
  25. 25.
    Strobel O, et al. Pancreatic adenocarcinoma: number of positive nodes allows to distinguish several N categories. Ann Surg. 2015;261(5):961–9.CrossRefGoogle Scholar
  26. 26.
    Iqbal N, et al. A comparison of pancreaticoduodenectomy with extended pancreaticoduodenectomy: a meta-analysis of 1909 patients. Eur J Surg Oncol. 2009;35(1):79–86.CrossRefGoogle Scholar
  27. 27.
    Fujita T, et al. Evaluation of the prognostic factors and significance of lymph node status in invasive ductal carcinoma of the body or tail of the pancreas. Pancreas. 2010;39(1):e48–54.CrossRefGoogle Scholar
  28. 28.
    Lin CC, Chen CL, Cheng YF. Modified extended distal pancreatectomy for carcinoma of body and tail of pancreas. Hepato-Gastroenterology. 2005;52(64):1090–1.PubMedGoogle Scholar
  29. 29.
    Fortner JG. Regional resection of cancer of the pancreas: a new surgical approach. Surgery. 1973;73(2):307–20.PubMedPubMedCentralGoogle Scholar
  30. 30.
    Giovinazzo F, et al. Meta-analysis of benefits of portal-superior mesenteric vein resection in pancreatic resection for ductal adenocarcinoma. Br J Surg. 2016;103(3):179–91.CrossRefGoogle Scholar
  31. 31.
    Dokmak S, et al. Parietal peritoneum as an autologous substitute for venous reconstruction in hepatopancreatobiliary surgery. Ann Surg. 2015;262(2):366–71.CrossRefGoogle Scholar
  32. 32.
    Del Chiaro M, et al. Cattell-braasch maneuver combined with artery-first approach for superior mesenteric-portal vein resection during pancreatectomy. J Gastrointest Surg. 2015;19(12):2264–8.CrossRefGoogle Scholar
  33. 33.
    Chu CK, et al. Prosthetic graft reconstruction after portal vein resection in pancreaticoduodenectomy: a multicenter analysis. J Am Coll Surg. 2010;211(3):316–24.CrossRefGoogle Scholar
  34. 34.
    Beltrame V, et al. Mesenteric-portal vein resection during pancreatectomy for pancreatic cancer. Gastroenterol Res Pract. 2015;2015:659730.CrossRefGoogle Scholar
  35. 35.
    Murakami Y, et al. Portal or superior mesenteric vein resection in pancreatoduodenectomy for pancreatic head carcinoma. Br J Surg. 2015;102(7):837–46.CrossRefGoogle Scholar
  36. 36.
    Hartwig W, et al. Multivisceral resection for pancreatic malignancies: risk-analysis and long-term outcome. Ann Surg. 2009;250(1):81–7.CrossRefGoogle Scholar
  37. 37.
    Hackert T, Weitz J, Buchler MW. Splenic artery use for arterial reconstruction in pancreatic surgery. Langenbeck’s Arch Surg. 2014;399(5):667–71.CrossRefGoogle Scholar
  38. 38.
    Mollberg N, et al. Arterial resection during pancreatectomy for pancreatic cancer: a systematic review and meta-analysis. Ann Surg. 2011;254(6):882–93.CrossRefGoogle Scholar
  39. 39.
    Weitz J, et al. The “artery first” approach for resection of pancreatic head cancer. J Am Coll Surg. 2010;210(2):e1–4.CrossRefGoogle Scholar
  40. 40.
    Inoue Y, et al. Pancreatoduodenectomy with systematic mesopancreas dissection using a supracolic anterior artery-first approach. Ann Surg. 2015;262(6):1092–101.CrossRefGoogle Scholar
  41. 41.
    Sanjay P, et al. ‘Artery-first’ approaches to pancreatoduodenectomy. Br J Surg. 2012;99(8):1027–35.CrossRefGoogle Scholar
  42. 42.
    Jing W, et al. Distal pancreatectomy with en bloc celiac axis resection for the treatment of locally advanced pancreatic body and tail cancer. Hepato-Gastroenterology. 2013;60(121):187–90.PubMedGoogle Scholar
  43. 43.
    Strasberg SM, Fields R. Left-sided pancreatic cancer: distal pancreatectomy and its variants: radical antegrade modular pancreatosplenectomy and distal pancreatectomy with celiac axis resection. Cancer J. 2012;18(6):562–70.CrossRefGoogle Scholar
  44. 44.
    Okada K, et al. Surgical strategy for patients with pancreatic body/tail carcinoma: who should undergo distal pancreatectomy with en-bloc celiac axis resection? Surgery. 2013;153(3):365–72.CrossRefGoogle Scholar
  45. 45.
    Hackert T, et al. Clinical significance of liver ischaemia after pancreatic resection. Br J Surg. 2011;98(12):1760–5.CrossRefGoogle Scholar
  46. 46.
    Gaujoux S, et al. Ischemic complications after pancreaticoduodenectomy: incidence, prevention, and management. Ann Surg. 2009;249(1):111–7.CrossRefGoogle Scholar
  47. 47.
    Kulemann B, et al. Perioperative and long-term outcome after standard pancreaticoduodenectomy, additional portal vein and multivisceral resection for pancreatic head cancer. J Gastrointest Surg. 2015;19(3):438–44.CrossRefGoogle Scholar
  48. 48.
    Burdelski CM, et al. Multivisceral resections in pancreatic cancer: identification of risk factors. World J Surg. 2011;35(12):2756–63.CrossRefGoogle Scholar
  49. 49.
    Hartwig W, et al. Outcomes after extended pancreatectomy in patients with borderline resectable and locally advanced pancreatic cancer. Br J Surg. 2016;103(12):1683–94.CrossRefGoogle Scholar
  50. 50.
    Gillen S, et al. Preoperative/neoadjuvant therapy in pancreatic cancer: a systematic review and meta-analysis of response and resection percentages. PLoS Med. 2010;7(4):e1000267.CrossRefGoogle Scholar
  51. 51.
    Petrelli F, et al. FOLFIRINOX-based neoadjuvant therapy in borderline resectable or unresectable pancreatic cancer: a meta-analytical review of published studies. Pancreas. 2015;44(4):515–21.CrossRefGoogle Scholar
  52. 52.
    Katz MH, et al. Response of borderline resectable pancreatic cancer to neoadjuvant therapy is not reflected by radiographic indicators. Cancer. 2012;118(23):5749–56.CrossRefGoogle Scholar
  53. 53.
    Tachezy M, et al. Sequential neoadjuvant chemoradiotherapy (CRT) followed by curative surgery vs. primary surgery alone for resectable, non-metastasized pancreatic adenocarcinoma: NEOPA- a randomized multicenter phase III study (NCT01900327, DRKS00003893, ISRCTN82191749). BMC Cancer. 2014;14:411.CrossRefGoogle Scholar
  54. 54.
    Tang K, et al. Neoadjuvant therapy for patients with borderline resectable pancreatic cancer: a systematic review and meta-analysis of response and resection percentages. Pancreatology. 2016;16(1):28–37.CrossRefGoogle Scholar
  55. 55.
    Blazer M, et al. Neoadjuvant modified (m) FOLFIRINOX for locally advanced unresectable (LAPC) and borderline resectable (BRPC) adenocarcinoma of the pancreas. Ann Surg Oncol. 2015;22(4):1153–9.CrossRefGoogle Scholar
  56. 56.
    Faris JE, et al. FOLFIRINOX in locally advanced pancreatic cancer: the Massachusetts General Hospital Cancer Center experience. Oncologist. 2013;18(5):543–8.CrossRefGoogle Scholar
  57. 57.
    Ajani JA, et al. Esophageal and esophagogastric junction cancers, version 1.2015. J Natl Compr Cancer Netw. 2015;13(2):194–227.CrossRefGoogle Scholar
  58. 58.
    Ferrone CR, et al. Radiological and surgical implications of neoadjuvant treatment with FOLFIRINOX for locally advanced and borderline resectable pancreatic cancer. Ann Surg. 2015;261(1):12–7.CrossRefGoogle Scholar
  59. 59.
    Takahashi H, et al. Perineural invasion and lymph node involvement as indicators of surgical outcome and pattern of recurrence in the setting of preoperative gemcitabine-based chemoradiation therapy for resectable pancreatic cancer. Ann Surg. 2012;255(1):95–102.CrossRefGoogle Scholar
  60. 60.
    Tian H, et al. Extrapancreatic neural plexus invasion by carcinomas of the pancreatic head region: evaluation using thin-section helical CT. Radiat Med. 2007;25(4):141–7.CrossRefGoogle Scholar
  61. 61.
    Patel BN, et al. Three-dimensional volume-rendered multidetector CT imaging of the posterior inferior pancreaticoduodenal artery: its anatomy and role in diagnosing extrapancreatic perineural invasion. Cancer Imaging. 2013;13(4):580–90.CrossRefGoogle Scholar
  62. 62.
    De Robertis R, et al. Prognostication and response assessment in liver and pancreatic tumors: the new imaging. World J Gastroenterol. 2015;21(22):6794–808.CrossRefGoogle Scholar
  63. 63.
    Mornex F, et al. Radiochemotherapy in the management of pancreatic cancer – part I: neoadjuvant treatment. Semin Radiat Oncol. 2005;15(4):226–34.CrossRefGoogle Scholar
  64. 64.
    Strobel O, et al. Resection after neoadjuvant therapy for locally advanced, “unresectable” pancreatic cancer. Surgery. 2012;152(3 Suppl 1):S33–42.CrossRefGoogle Scholar
  65. 65.
    Nanda RH, et al. Neoadjuvant modified FOLFIRINOX and chemoradiation therapy for locally advanced pancreatic cancer improves resectability. J Surg Oncol. 2015;111(8):1028–34.CrossRefGoogle Scholar
  66. 66.
    Christians KK, et al. Neoadjuvant FOLFIRINOX for borderline resectable pancreas cancer: a new treatment paradigm? Oncologist. 2014;19(3):266–74.CrossRefGoogle Scholar
  67. 67.
    James ET, Yao X, Cong X, Li J, Hahn C, Kaley K, Kortmansky JS, Fischbach NA, Chang BW, Salem RR, Cha C, Stein S, Hochster HS, Lacy J. Interim analysis of a phase II study of dose-modified FOLFIRINOX (mFOLFIRINOX) in locally advanced (LAPC) and metastatic pancreatic cancer (MPC). J Clin Oncol. 2014;3:32.Google Scholar
  68. 68.
    Conroy T, et al. FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer. N Engl J Med. 2011;364(19):1817–25.CrossRefGoogle Scholar
  69. 69.
    Hackert T, et al. locally advanced pancreatic cancer: neoadjuvant therapy with Folfirinox results in resectability in 60% of the patients. Ann Surg. 2016;264(3):457–63.CrossRefGoogle Scholar
  70. 70.
    Katz MH, et al. Borderline resectable pancreatic cancer: the importance of this emerging stage of disease. J Am Coll Surg. 2008;206(5):833–46; discussion 846–8.CrossRefGoogle Scholar
  71. 71.
    Hartwig W, et al. CA19-9 in potentially resectable pancreatic cancer: perspective to adjust surgical and perioperative therapy. Ann Surg Oncol. 2013;20(7):2188–96.CrossRefGoogle Scholar
  72. 72.
    Aldakkak M, et al. Pre-treatment carbohydrate antigen 19-9 does not predict the response to neoadjuvant therapy in patients with localized pancreatic cancer. HPB (Oxford). 2015;17(10):942–52.CrossRefGoogle Scholar
  73. 73.
    Boone BA, et al. Serum CA 19-9 response to neoadjuvant therapy is associated with outcome in pancreatic adenocarcinoma. Ann Surg Oncol. 2014;21(13):4351–8.CrossRefGoogle Scholar
  74. 74.
    Kurahara H, et al. Prognostication by inflammation-based score in patients with locally advanced pancreatic cancer treated with chemoradiotherapy. Pancreatology. 2015;15(6):688–93.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Thilo Hackert
    • 1
  • Christoph W. Michalski
    • 1
  • Markus W. Büchler
    • 2
  1. 1.Department of General, Visceral and Transplantation SurgeryHeidelberg University HospitalHeidelbergGermany
  2. 2.Department of General, Visceral and Transplantation SurgeryUniversity of HeidelbergHeidelbergGermany

Section editors and affiliations

  • James L. Abbruzzese
    • 1
  • Raul A. Urrutia
    • 2
  • John Neoptolemos
    • 3
  • Markus W. Büchler
    • 4
  1. 1.Duke University Medical CenterDurhamUSA
  2. 2.Mayo Clinic Cancer CenterMayo ClinicRochesterUSA
  3. 3.Division of Surgery and OncologyUniversity of LiverpoolLiverpoolUK
  4. 4.Department of General, Visceral and Transplantation SurgeryUniversity of HeidelbergHeidelbergGermany

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