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ASO Practice Guidelines Series: Management of Resectable, Borderline Resectable, and Locally Advanced Pancreas Cancer

  • Pancreatic Tumors
  • Published:
Annals of Surgical Oncology Aims and scope Submit manuscript

Abstract

Pancreatic adenocarcinoma is an aggressive disease marked by high rates of both local and distant failure. In the minority of patients with potentially resectable disease, multimodal treatment paradigms have allowed for prolonged survival in an increasingly larger pool of well-selected patients. Therefore, it is critical for surgical oncologists to be abreast of current guideline recommendations for both surgical management and multimodal therapy for pancreas cancer. We discuss these guidelines, as well as the underlying data supporting these positions, to offer surgical oncologists a framework for managing patients with pancreatic adenocarcinoma.

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References

  1. SEER Cancer Stat Facts: Pancreatic Cancer. National Cancer Institute. Bethesda. https://seer.cancer.gov/statfacts/html/pancreas.html. https://seer.cancer.govhttps://seer.cancer.gov/statfacts/html/pancreas.html. Accessed 30 July 2023.

  2. Society AC. Cancer facts and figures 2021. Atlanta: American Cancer Society; 2021.

    Google Scholar 

  3. Hingorani SR, Petricoin EF, Maitra A, et al. Preinvasive and invasive ductal pancreatic cancer and its early detection in the mouse. Cancer Cell. 2003;4(6):437–50.

    Article  CAS  PubMed  Google Scholar 

  4. Makohon-Moore AP, Matsukuma K, Zhang M, et al. Precancerous neoplastic cells can move through the pancreatic ductal system. Nature. 2018;561(7722):201–5.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  5. Wu J, Matthaei H, Maitra A, et al. Recurrent GNAS mutations define an unexpected pathway for pancreatic cyst development. Sci Transl Med. 2011;3(92):92–66.

    Article  Google Scholar 

  6. Wood LD, Canto MI, Jaffee EM, Simeone DM. Pancreatic cancer: pathogenesis, screening, diagnosis, and treatment. Gastroenterology. 2022;163(2):386–402.

    Article  PubMed  Google Scholar 

  7. Park W, Chawla A, O’Reilly EM. Pancreatic cancer: a review. JAMA. 2021;326(9):851–62.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Oettle H, Neuhaus P, Hochhaus A, et al. Adjuvant chemotherapy with gemcitabine and long-term outcomes among patients with resected pancreatic cancer: the CONKO-001 randomized trial. JAMA. 2013;310(14):1473–81.

    Article  CAS  PubMed  Google Scholar 

  9. Rhim AD, Mirek ET, Aiello NM, et al. EMT and dissemination precede pancreatic tumor formation. Cell. 2012;148(1–2):349–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Gemenetzis G, Groot VP, Yu J, et al. Circulating tumor cells dynamics in pancreatic adenocarcinoma correlate with disease status: Results of the prospective CLUSTER study. Ann Surg. 2018;268(3):408–20.

    Article  PubMed  Google Scholar 

  11. Conroy T, Hammel P, Hebbar M, et al. FOLFIRINOX or gemcitabine as adjuvant therapy for pancreatic cancer. N Engl J Med. 2018;379(25):2395–406.

    Article  CAS  PubMed  Google Scholar 

  12. Vincent A, Herman J, Schulick R, Hruban RH, Goggins M. Pancreatic cancer. Lancet. 2011;378(9791):607–20.

    Article  PubMed  PubMed Central  Google Scholar 

  13. National Comprehensive Cancer Network. Pancreatic cancer (Version 2.2023). Accessed 20 Aug 2023.

  14. Canto MI, Harinck F, Hruban RH, et al. International Cancer of the Pancreas Screening (CAPS) consortium summit on the management of patients with increased risk for familial pancreatic cancer. Gut. 2013;62(3):339–47.

    Article  PubMed  Google Scholar 

  15. National Comprehensive Cancer Network. Genetic/familial high-risk assessment: breast, ovarian, and pancreatic (Version 3.2023). Accessed 22 Aug 2023.

  16. Shindo K, Yu J, Suenaga M, et al. Deleterious germline mutations in patients with apparently sporadic pancreatic adenocarcinoma. J Clin Oncol. 2017;35(30):3382–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Golan T, Hammel P, Reni M, et al. Maintenance olaparib for germline BRCA-mutated metastatic pancreatic cancer. N Engl J Med. 2019;381(4):317–27.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Al-Hawary MM, Francis IR, Chari ST, et al. Pancreatic ductal adenocarcinoma radiology reporting template: consensus statement of the society of abdominal radiology and the American pancreatic association. Gastroenterology. 2014;146(1):291–304.

    Article  PubMed  Google Scholar 

  19. Vachiranubhap B, Kim YH, Balci NC, Semelka RC. Magnetic resonance imaging of adenocarcinoma of the pancreas. Top Magn Reson Imaging. 2009;20(1):3–9.

    Article  PubMed  Google Scholar 

  20. Motosugi U, Ichikawa T, Morisaka H, et al. Detection of pancreatic carcinoma and liver metastases with gadoxetic acid-enhanced MR imaging: comparison with contrast-enhanced multi-detector row CT. Radiology. 2011;260(2):446–53.

    Article  PubMed  Google Scholar 

  21. Expert Panel on Gastrointestinal I, Qayyum A, Tamm EP, et al. ACR Appropriateness Criteria® staging of pancreatic ductal adenocarcinoma. J Am Coll Radiol. 2017;14(11S):S560-9.

    Google Scholar 

  22. Steinberg W. The clinical utility of the CA 19–9 tumor-associated antigen. Am J Gastroenterol. 1990;85(4):350–5.

    CAS  PubMed  Google Scholar 

  23. Ong SL, Sachdeva A, Garcea G, et al. Elevation of carbohydrate antigen 19.9 in benign hepatobiliary conditions and its correlation with serum bilirubin concentration. Dig Dis Sci. 2008;53(12):3213–7.

    Article  CAS  PubMed  Google Scholar 

  24. Committee ASoP, Eloubeidi MA, Decker GA, et al. The role of endoscopy in the evaluation and management of patients with solid pancreatic neoplasia. Gastrointest Endosc. 2016;83(1):17–28.

    Article  Google Scholar 

  25. Deerenberg EB, Poley JW, Hermans JJ, Ganesh S, van der Harst E, van Eijck CH. Role of endoscopic ultrasonography in patients suspected of pancreatic cancer with negative helical MDCT scan. Dig Surg. 2011;28(5–6):398–403.

    Article  PubMed  Google Scholar 

  26. Nawaz H, Fan CY, Kloke J, et al. Performance characteristics of endoscopic ultrasound in the staging of pancreatic cancer: a meta-analysis. JOP. 2013;14(5):484–97.

    PubMed  Google Scholar 

  27. Levine I, Trindade AJ. Endoscopic ultrasound fine needle aspiration vs fine needle biopsy for pancreatic masses, subepithelial lesions, and lymph nodes. World J Gastroenterol. 2021;27(26):4194–207.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Micames C, Jowell PS, White R, et al. Lower frequency of peritoneal carcinomatosis in patients with pancreatic cancer diagnosed by EUS-guided FNA vs. percutaneous FNA. Gastrointest Endosc. 2003;58(5):690–5.

    Article  PubMed  Google Scholar 

  29. Davids PH, Groen AK, Rauws EA, Tytgat GN, Huibregtse K. Randomised trial of self-expanding metal stents versus polyethylene stents for distal malignant biliary obstruction. Lancet. 1992;340(8834–8835):1488–92.

    Article  CAS  PubMed  Google Scholar 

  30. van der Gaag NA, Rauws EA, van Eijck CH, et al. Preoperative biliary drainage for cancer of the head of the pancreas. N Engl J Med. 2010;362(2):129–37.

    Article  PubMed  Google Scholar 

  31. De Bellis M, Sherman S, Fogel EL, et al. Tissue sampling at ERCP in suspected malignant biliary strictures (Part 1). Gastrointest Endosc. 2002;56(4):552–61.

    Article  PubMed  Google Scholar 

  32. Nakao A, Kanzaki A, Fujii T, et al. Correlation between radiographic classification and pathological grade of portal vein wall invasion in pancreatic head cancer. Ann Surg. 2012;255(1):103–8.

    Article  PubMed  Google Scholar 

  33. Ghaneh P, Kleeff J, Halloran CM, et al. The impact of positive resection margins on survival and recurrence following resection and adjuvant chemotherapy for pancreatic ductal adenocarcinoma. Ann Surg. 2019;269(3):520–9.

    Article  PubMed  Google Scholar 

  34. Sohal DPS, Duong M, Ahmad SA, et al. Efficacy of perioperative chemotherapy for resectable pancreatic adenocarcinoma: a phase 2 randomized clinical trial. JAMA Oncol. 2021;7(3):421–7.

    Article  PubMed  Google Scholar 

  35. Chatzizacharias NA, Tsai S, Griffin M, et al. Locally advanced pancreas cancer: staging and goals of therapy. Surgery. 2018;163(5):1053–62.

    Article  PubMed  Google Scholar 

  36. Katz MH, Marsh R, Herman JM, et al. Borderline resectable pancreatic cancer: need for standardization and methods for optimal clinical trial design. Ann Surg Oncol. 2013;20(8):2787–95.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Bernard V, Kim DU, San Lucas FA, et al. Circulating nucleic acids are associated with outcomes of patients with pancreatic cancer. Gastroenterology. 2019;156(1):108–18.

    Article  CAS  PubMed  Google Scholar 

  38. Patel SH, Katz MHG, Ahmad SA. The landmark series: preoperative therapy for pancreatic cancer. Ann Surg Oncol. 2021;28(8):4104–29.

    Article  PubMed  Google Scholar 

  39. Khorana AA, McKernin SE, Berlin J, et al. Potentially curable pancreatic adenocarcinoma: ASCO clinical practice guideline update. J Clin Oncol. 2019;37(23):2082–8.

    Article  CAS  PubMed  Google Scholar 

  40. Hurria A, Togawa K, Mohile SG, et al. Predicting chemotherapy toxicity in older adults with cancer: a prospective multicenter study. J Clin Oncol. 2011;29(25):3457–65.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Dale W, Hemmerich J, Kamm A, et al. Geriatric assessment improves prediction of surgical outcomes in older adults undergoing pancreaticoduodenectomy: a prospective cohort study. Ann Surg. 2014;259(5):960–5.

    Article  PubMed  Google Scholar 

  42. Palta M, Godfrey D, Goodman KA, et al. Radiation therapy for pancreatic cancer: executive summary of an ASTRO clinical practice guideline. Pract Radiat Oncol. 2019;9(5):322–32.

    Article  PubMed  Google Scholar 

  43. Conroy T, Pfeiffer P, Vilgrain V, et al. Pancreatic cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2023. https://doi.org/10.1016/j.annonc.2023.08.009.

    Article  PubMed  Google Scholar 

  44. Pawlik TM, Laheru D, Hruban RH, et al. Evaluating the impact of a single-day multidisciplinary clinic on the management of pancreatic cancer. Ann Surg Oncol. 2008;15(8):2081–8.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Brauer DG, Strand MS, Sanford DE, et al. Utility of a multidisciplinary tumor board in the management of pancreatic and upper gastrointestinal diseases: an observational study. HPB (Oxford). 2017;19(2):133–9.

    Article  PubMed  Google Scholar 

  46. Birkmeyer JD, Siewers AE, Finlayson EV, et al. Hospital volume and surgical mortality in the United States. N Engl J Med. 2002;346(15):1128–37.

    Article  PubMed  Google Scholar 

  47. Bilimoria KY, Bentrem DJ, Ko CY, et al. Multimodality therapy for pancreatic cancer in the U.S.: utilization, outcomes, and the effect of hospital volume. Cancer. 2007;110(6):1227–34.

    Article  PubMed  Google Scholar 

  48. Hoos WA, James PM, Rahib L, Talley AW, Fleshman JM, Matrisian LM. Pancreatic cancer clinical trials and accrual in the United States. J Clin Oncol. 2013;31(27):3432–8.

    Article  PubMed  Google Scholar 

  49. Oettle H, Neuhaus P, Hochhaus A, et al. Adjuvant chemotherapy with gemcitabine and long-term outcomes among patients with resected pancreatic cancer: the CONKO-001 randomized trial. JAMA. 2013;310(14):1473–81.

    Article  CAS  PubMed  Google Scholar 

  50. Nassour I, Parrish A, Baptist L, et al. National adoption of neoadjuvant chemotherapy: paradigm shift in the treatment of pancreatic cancer. HPB (Oxford). 2023;2023:1323–8.

    Article  Google Scholar 

  51. Yeung RS, Weese JL, Hoffman JP, et al. Neoadjuvant chemoradiation in pancreatic and duodenal carcinoma. A phase II study. Cancer. 1993;72(7):2124–33.

    Article  CAS  PubMed  Google Scholar 

  52. Versteijne E, van Dam JL, Suker M, et al. Neoadjuvant chemoradiotherapy versus upfront surgery for resectable and borderline resectable pancreatic cancer: long-term results of the Dutch randomized PREOPANC trial. J Clin Oncol. 2022;40(11):1220–30.

    Article  CAS  PubMed  Google Scholar 

  53. Jang JY, Han Y, Lee H, et al. Oncological benefits of neoadjuvant chemoradiation with gemcitabine versus upfront surgery in patients with borderline resectable pancreatic cancer: a prospective, randomized, open-label, multicenter phase 2/3 trial. Ann Surg. 2018;268(2):215–22.

    Article  PubMed  Google Scholar 

  54. Katz MHG, Shi Q, Meyers J, et al. Efficacy of preoperative mFOLFIRINOX vs mFOLFIRINOX plus hypofractionated radiotherapy for borderline resectable adenocarcinoma of the pancreas: the A021501 Phase 2 Randomized Clinical Trial. JAMA Oncol. 2022;8(9):1263–70.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Hammel P, Huguet F, van Laethem JL, et al. Effect of chemoradiotherapy vs chemotherapy on survival in patients with locally advanced pancreatic cancer controlled after 4 months of gemcitabine with or without Erlotinib: the LAP07 randomized clinical trial. JAMA. 2016;315(17):1844–53.

    Article  CAS  PubMed  Google Scholar 

  56. Katz MH, Shi Q, Ahmad SA, et al. Preoperative modified FOLFIRINOX treatment followed by capecitabine-based chemoradiation for borderline resectable pancreatic cancer: alliance for clinical trials in oncology trial A021101. JAMA Surg. 2016;151(8):e161137.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Ferrone CR, Marchegiani G, Hong TS, 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.

    Article  PubMed  Google Scholar 

  58. Tzeng CW, Balachandran A, Ahmad M, et al. Serum carbohydrate antigen 19–9 represents a marker of response to neoadjuvant therapy in patients with borderline resectable pancreatic cancer. HPB (Oxford). 2014;16(5):430–8.

    Article  PubMed  Google Scholar 

  59. Heger U, Sun H, Hinz U, et al. Induction chemotherapy in pancreatic cancer: CA 19–9 may predict resectability and survival. HPB (Oxford). 2020;22(2):224–32.

    Article  PubMed  Google Scholar 

  60. Khorana AA, Mangu PB, Berlin J, et al. Potentially curable pancreatic cancer: American Society of Clinical Oncology clinical practice guideline. J Clin Oncol. 2016;34(21):2541–56.

    Article  PubMed  Google Scholar 

  61. Valle JW, Palmer D, Jackson R, et al. Optimal duration and timing of adjuvant chemotherapy after definitive surgery for ductal adenocarcinoma of the pancreas: ongoing lessons from the ESPAC-3 study. J Clin Oncol. 2014;32(6):504–12.

    Article  PubMed  Google Scholar 

  62. Labori KJ, Bratlie SO, Biörserud C, et al. Short-course neoadjuvant FOLFIRINOX versus upfront surgery for resectable pancreatic head cancer: a multicenter randomized phase-II trial (NORPACT-1). J Clin Oncol. 2023;41(17_suppl):LBA4005.

    Article  Google Scholar 

  63. Chawla A, Shi Q, Ko AH, et al. Alliance A021806: a phase III trial evaluating perioperative versus adjuvant therapy for resectable pancreatic cancer. J Clin Oncol. 2023;41(16_suppl):TPS4204.

    Article  Google Scholar 

  64. Janssen QP, van Dam JL, Bonsing BA, et al. Total neoadjuvant FOLFIRINOX versus neoadjuvant gemcitabine-based chemoradiotherapy and adjuvant gemcitabine for resectable and borderline resectable pancreatic cancer (PREOPANC-2 trial): study protocol for a nationwide multicenter randomized controlled trial. BMC Cancer. 2021;21(1):300.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. van Dam JL, Verkolf EMM, Dekker EN, et al. Perioperative or adjuvant mFOLFIRINOX for resectable pancreatic cancer (PREOPANC-3): study protocol for a multicenter randomized controlled trial. BMC Cancer. 2023;23(1):728.

    Article  PubMed  PubMed Central  Google Scholar 

  66. Murphy JE, Wo JY, Ryan DP, et al. Total neoadjuvant therapy with FOLFIRINOX followed by individualized chemoradiotherapy for borderline resectable pancreatic adenocarcinoma: a phase 2 clinical trial. JAMA Oncol. 2018;4(7):963–9.

    Article  PubMed  PubMed Central  Google Scholar 

  67. Schwarz L, Bachet J-B, Meurisse A, et al. Resectable pancreatic adenocarcinoma neo-adjuvant FOLF(IRIN)OX-based chemotherapy: a multicenter, non-comparative, randomized, phase II trial (PANACHE01-PRODIGE48 study). J Clin Oncol. 2022;40(16_suppl):4134.

    Article  Google Scholar 

  68. Versteijne E, Suker M, Groothuis K, et al. Preoperative chemoradiotherapy versus immediate surgery for resectable and borderline resectable pancreatic cancer: results of the Dutch randomized phase III PREOPANC trial. J Clin Oncol. 2020;38(16):1763–73.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Koerkamp BG, Janssen QP, Dam JL, et al. Neoadjuvant chemotherapy with FOLFIRINOX versus neoadjuvant gemcitabine-based chemoradiotherapy for borderline resectable and resectable pancreatic cancer (PREOPANC-2): a multicenter randomized controlled trial. Ann Oncol. 2023;34:S1254-335.

    Google Scholar 

  70. Ghaneh P, Palmer D, Cicconi S, et al. Immediate surgery compared with short-course neoadjuvant gemcitabine plus capecitabine, FOLFIRINOX, or chemoradiotherapy in patients with borderline resectable pancreatic cancer (ESPAC5): a four-arm, multicentre, randomised, phase 2 trial. Lancet Gastroenterol Hepatol. 2023;8(2):157–68.

    Article  PubMed  Google Scholar 

  71. Hurt CN, Mukherjee S, Bridgewater J, et al. Health-related quality of life in SCALOP, a randomized phase 2 trial comparing chemoradiation therapy regimens in locally advanced pancreatic cancer. Int J Radiat Oncol Biol Phys. 2015;93(4):810–8.

    Article  PubMed  PubMed Central  Google Scholar 

  72. Katz MHG, Shi Q, Meyers JP, et al. Alliance A021501: preoperative mFOLFIRINOX or mFOLFIRINOX plus hypofractionated radiation therapy (RT) for borderline resectable (BR) adenocarcinoma of the pancreas. J Clin Oncol. 2021;39(3_suppl):377.

    Article  Google Scholar 

  73. Ghaneh P, Palmer DH, Cicconi S, et al. ESPAC-5F: four-arm, prospective, multicenter, international randomized phase II trial of immediate surgery compared with neoadjuvant gemcitabine plus capecitabine (GEMCAP) or FOLFIRINOX or chemoradiotherapy (CRT) in patients with borderline resectable pancreatic cancer. J Clin Oncol. 2020;38(15_suppl):4505.

    Article  Google Scholar 

  74. Jones RP, Psarelli EE, Jackson R, et al. Patterns of recurrence after resection of pancreatic ductal adenocarcinoma: a secondary analysis of the ESPAC-4 randomized adjuvant chemotherapy trial. JAMA Surg. 2019;154(11):1038–48.

    Article  PubMed  PubMed Central  Google Scholar 

  75. Turner KM, Delman AM, Kharofa JR, et al. Radiation therapy in borderline resectable pancreatic cancer: a review. Surgery. 2022;172(1):284–90.

    Article  PubMed  Google Scholar 

  76. Fietkau R, Ghadimi M, Grützmann R, et al. Randomized phase III trial of induction chemotherapy followed by chemoradiotherapy or chemotherapy alone for nonresectable locally advanced pancreatic cancer: first results of the CONKO-007 trial. J Clin Oncol. 2022;40(16_suppl):4008.

    Article  Google Scholar 

  77. Neoptolemos JP, Stocken DD, Friess H, et al. A randomized trial of chemoradiotherapy and chemotherapy after resection of pancreatic cancer. N Engl J Med. 2004;350(12):1200–10.

    Article  CAS  PubMed  Google Scholar 

  78. Neoptolemos JP, Palmer DH, Ghaneh P, et al. Comparison of adjuvant gemcitabine and capecitabine with gemcitabine monotherapy in patients with resected pancreatic cancer (ESPAC-4): a multicentre, open-label, randomised, phase 3 trial. Lancet. 2017;389(10073):1011–24.

    Article  CAS  PubMed  Google Scholar 

  79. Conroy T, Hammel P, Hebbar M, et al. FOLFIRINOX or gemcitabine as adjuvant therapy for pancreatic cancer. N Engl J Med. 2018;379(25):2395–406.

    Article  CAS  PubMed  Google Scholar 

  80. Tempero MA, Pelzer U, O’Reilly EM, et al. Adjuvant nab-paclitaxel + gemcitabine in resected pancreatic ductal adenocarcinoma: results from a randomized, open-label, phase III trial. J Clin Oncol. 2023;41(11):2007–19.

    Article  CAS  PubMed  Google Scholar 

  81. Kalser MH, Ellenberg SS. Pancreatic cancer. Adjuvant combined radiation and chemotherapy following curative resection. Arch Surg. 1985;120(8):899–903.

    Article  CAS  PubMed  Google Scholar 

  82. Klinkenbijl JH, Jeekel J, Sahmoud T, et al. Adjuvant radiotherapy and 5-fluorouracil after curative resection of cancer of the pancreas and periampullary region: phase III trial of the EORTC gastrointestinal tract cancer cooperative group. Ann Surg. 1999;230(6):776–82 (discussion 782–4).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Smeenk HG, van Eijck CH, Hop WC, et al. Long-term survival and metastatic pattern of pancreatic and periampullary cancer after adjuvant chemoradiation or observation: long-term results of EORTC trial 40891. Ann Surg. 2007;246(5):734–40.

    Article  PubMed  Google Scholar 

  84. Neoptolemos JP, Stocken DD, Bassi C, et al. Adjuvant chemotherapy with fluorouracil plus folinic acid vs gemcitabine following pancreatic cancer resection: a randomized controlled trial. JAMA. 2010;304(10):1073–81.

    Article  CAS  PubMed  Google Scholar 

  85. Regine WF, Winter KA, Abrams RA, et al. Fluorouracil vs gemcitabine chemotherapy before and after fluorouracil-based chemoradiation following resection of pancreatic adenocarcinoma: a randomized controlled trial. JAMA. 2008;299(9):1019–26.

    Article  CAS  PubMed  Google Scholar 

  86. Neoptolemos JP, Palmer DH, Ghaneh P, et al. ESPAC-4: a multicenter, international, open-label randomized controlled phase III trial of adjuvant combination chemotherapy of gemcitabine (GEM) and capecitabine (CAP) versus monotherapy gemcitabine in patients with resected pancreatic ductal adenocarcinoma: five-year follow-up. J Clin Oncol. 2020;38(15):4516.

    Article  Google Scholar 

  87. Conroy T, Castan F, Lopez A, et al. Five-year outcomes of FOLFIRINOX vs gemcitabine as adjuvant therapy for pancreatic cancer: a randomized clinical trial. JAMA Oncol. 2022;8(11):1571–8.

    Article  PubMed  PubMed Central  Google Scholar 

  88. Beall MS, Dyer GA, Stephenson HE Jr. Disappointments in the management of patients with malignancy of pancreas, duodenum, and common bile duct. Arch Surg. 1970;101(4):461–5.

    Article  CAS  PubMed  Google Scholar 

  89. Cameron JL, He J. Two thousand consecutive pancreaticoduodenectomies. J Am Coll Surg. 2015;220(4):530–6.

    Article  PubMed  Google Scholar 

  90. Altman AM, Wirth K, Marmor S, et al. Completion of adjuvant chemotherapy after upfront surgical resection for pancreatic cancer is uncommon yet associated with improved survival. Ann Surg Oncol. 2019;26(12):4108–16.

    Article  PubMed  Google Scholar 

  91. Whipple AO, Parsons WB, Mullins CR. Treatment of carcinoma of the ampulla of vater. Ann Surg. 1935;102(4):763–79.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Katz MH, Merchant NB, Brower S, et al. Standardization of surgical and pathologic variables is needed in multicenter trials of adjuvant therapy for pancreatic cancer: results from the ACOSOG Z5031 trial. Ann Surg Oncol. 2011;18(2):337–44.

    Article  PubMed  Google Scholar 

  93. Nelson H, Hunt K, Veeramachaneni N, et al. Operative standards for cancer surgery. Alphen aan den Rijn: Wolter Kluwer; 2015.

    Google Scholar 

  94. Gudmundsdottir H, Yonkus JA, Alva-Ruiz R, et al. Yield of staging laparoscopy for pancreatic cancer in the modern era: analysis of more than 1,000 consecutive patients. J Am Coll Surg. 2023;237(1):49–57.

    Article  PubMed  PubMed Central  Google Scholar 

  95. van Dongen JC, Versteijne E, Bonsing BA, et al. The yield of staging laparoscopy for resectable and borderline resectable pancreatic cancer in the PREOPANC randomized controlled trial. Eur J Surg Oncol. 2023;49(4):811–7.

    Article  PubMed  Google Scholar 

  96. Kooby DA, Lad NL, Squires MH 3rd, et al. Value of intraoperative neck margin analysis during Whipple for pancreatic adenocarcinoma: a multicenter analysis of 1399 patients. Ann Surg. 2014;260(3):494–501 (discussion 501–3).

    Article  PubMed  Google Scholar 

  97. Baque P, Iannelli A, Delotte J, de Peretti F, Bourgeon A. Division of the right posterior attachments of the head of the pancreas with a linear stapler during pancreaticoduodenectomy: vascular and oncological considerations based on an anatomical cadaver-based study. Surg Radiol Anat. 2009;31(1):13–7.

    Article  PubMed  Google Scholar 

  98. Strasberg SM, Linehan DC, Hawkins WG. Radical antegrade modular pancreatosplenectomy procedure for adenocarcinoma of the body and tail of the pancreas: ability to obtain negative tangential margins. J Am Coll Surg. 2007;204(2):244–9.

    Article  PubMed  Google Scholar 

  99. Shoup M, Conlon KC, Klimstra D, Brennan MF. Is extended resection for adenocarcinoma of the body or tail of the pancreas justified? J Gastrointest Surg. 2003;7(8):946–52 (discussion 952).

    Article  PubMed  Google Scholar 

  100. Tol JA, Gouma DJ, Bassi C, 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.

    Article  PubMed  Google Scholar 

  101. Yeo CJ, Cameron JL, Lillemoe KD, 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).

    Article  PubMed  PubMed Central  Google Scholar 

  102. Farnell MB, Pearson RK, Sarr MG, 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).

    Article  PubMed  Google Scholar 

  103. Pawlik TM, Abdalla EK, Barnett CC, et al. Feasibility of a randomized trial of extended lymphadenectomy for pancreatic cancer. Arch Surg. 2005;140(6):584–9 (discussion 589–91).

    Article  PubMed  Google Scholar 

  104. Zhou Y, Zhang Z, Liu Y, Li B, Xu D. Pancreatectomy combined with superior mesenteric vein-portal vein resection for pancreatic cancer: a meta-analysis. World J Surg. 2012;36(4):884–91.

    Article  PubMed  Google Scholar 

  105. Tseng JF, Raut CP, Lee JE, et al. Pancreaticoduodenectomy with vascular resection: margin status and survival duration. J Gastrointest Surg. 2004;8(8):935–49 (discussion 949–50).

    Article  PubMed  Google Scholar 

  106. Katz MH, Fleming JB, Pisters PW, Lee JE, Evans DB. Anatomy of the superior mesenteric vein with special reference to the surgical management of first-order branch involvement at pancreaticoduodenectomy. Ann Surg. 2008;248(6):1098–102.

    Article  PubMed  Google Scholar 

  107. Ferreira N, Oussoultzoglou E, Fuchshuber P, et al. Splenic vein-inferior mesenteric vein anastomosis to lessen left-sided portal hypertension after pancreaticoduodenectomy with concomitant vascular resection. Arch Surg. 2011;146(12):1375–81.

    Article  PubMed  Google Scholar 

  108. Asbun HJ, Moekotte AL, Vissers FL, et al. The Miami International evidence-based guidelines on minimally invasive pancreas resection. Ann Surg. 2020;271(1):1–14.

    Article  PubMed  Google Scholar 

  109. Hirono S, Kawai M, Okada K, et al. Pancreatic neck cancer has specific and oncologic characteristics regarding portal vein invasion and lymph node metastasis. Surgery. 2016;159(2):426–40.

    Article  PubMed  Google Scholar 

  110. Peters NA, Javed AA, Cameron JL, et al. Modified appleby procedure for pancreatic adenocarcinoma: Does improved neoadjuvant therapy warrant such an aggressive approach? Ann Surg Oncol. 2016;23(11):3757–64.

    Article  PubMed  Google Scholar 

  111. Datta J, Wilson GC, D’Angelica MI, et al. A call for caution in overinterpreting exceptional outcomes after radical surgery for pancreatic cancer: let the data speak. Ann Surg. 2021;274(1):e82-4.

    Article  PubMed  Google Scholar 

  112. Tee MC, Krajewski AC, Groeschl RT, et al. Indications and perioperative outcomes for pancreatectomy with arterial resection. J Am Coll Surg. 2018;227(2):255–69.

    Article  PubMed  Google Scholar 

  113. Burgart LJ, Chopp WV, Jain D. College of American Pathologists: protocol for the examination of specimens from patients with carcinoma of the Pancreas. 2021. Accessed 24 Aug 2023.

  114. Huebner M, Kendrick M, Reid-Lombardo KM, et al. Number of lymph nodes evaluated: prognostic value in pancreatic adenocarcinoma. J Gastrointest Surg. 2012;16(5):920–6.

    Article  PubMed  Google Scholar 

  115. Feinstein AR, Sosin DM, Wells CK. The Will rogers phenomenon. Stage migration and new diagnostic techniques as a source of misleading statistics for survival in cancer. N Engl J Med. 1985;312(25):1604–8.

    Article  CAS  PubMed  Google Scholar 

  116. Verbeke CS, Leitch D, Menon KV, McMahon MJ, Guillou PJ, Anthoney A. Redefining the R1 resection in pancreatic cancer. Br J Surg. 2006;93(10):1232–7.

    Article  CAS  PubMed  Google Scholar 

  117. Campbell F, Smith RA, Whelan P, et al. Classification of R1 resections for pancreatic cancer: the prognostic relevance of tumour involvement within 1 mm of a resection margin. Histopathology. 2009;55(3):277–83.

    Article  PubMed  Google Scholar 

  118. Verbeke CS, Menon KV. Redefining resection margin status in pancreatic cancer. HPB (Oxford). 2009;11(4):282–9.

    Article  PubMed  Google Scholar 

  119. Pishvaian MJ, Blais EM, Brody JR, et al. Overall survival in patients with pancreatic cancer receiving matched therapies following molecular profiling: a retrospective analysis of the know your tumor registry trial. Lancet Oncol. 2020;21(4):508–18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Dreyer SB, Rae S, Bisset K, et al. The impact of molecular subtyping on pathological staging of pancreatic cancer. Ann Surg. 2023;277(2):e396-405.

    Article  PubMed  Google Scholar 

  121. Kelly D, Jonker DJ, Ko Y-J, et al. GATA6 Expression as a predictor of response to perioperative chemotherapy in resectable pancreatic adenocarcinoma: a multicenter Canadian phase II study (NeoPancONE). J Clin Oncol. 2022;40(4_suppl):TPS638.

    Article  Google Scholar 

  122. Zhou Y, Song A, Wu L, Si X, Li Y. Second pancreatectomy for recurrent pancreatic ductal adenocarcinoma in the remnant pancreas: a pooled analysis. Pancreatology. 2016;16(6):1124–8.

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Surgery, University of Cincinnati College of Medicine, Cincinnati, OH, USA

    Kevin M. Turner MD

  2. Division of Surgical Oncology, Department of Surgery, University of Cincinnati College of Medicine, Cincinnati, OH, USA

    Gregory C. Wilson MD, Sameer H. Patel MD & Syed A. Ahmad MD

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  2. Gregory C. Wilson MD
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  3. Sameer H. Patel MD
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Turner, K.M., Wilson, G.C., Patel, S.H. et al. ASO Practice Guidelines Series: Management of Resectable, Borderline Resectable, and Locally Advanced Pancreas Cancer. Ann Surg Oncol 31, 1884–1897 (2024). https://doi.org/10.1245/s10434-023-14585-y

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