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Surgical margins for duodenopancreatectomy

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Abstract

Microscopic residual tumor (R1) affects prognosis of resected pancreatic head cancer patients. Surgeon’s ability, caseload and accuracy of pathological staging affect the rate of R1 resections. The goal of this study was to verify if a standardized histopathological workup of the specimen affects the rate of microscopic residual tumor after PD for cancer. Two groups of specimens were managed with (Group 1, Standardized Group, SG) or without (Group 2, Non Standardized Group, NSG) a standardized histopathological workup reported by the Royal College of Pathologists. Group 1 included 50 cases of PD for periampullary cancer treated between October 2010 and July 2012. Group 2 included 50 cases of PD for periampullary cancer treated between September 2005 and September 2010. The primary endpoint of the study was to verify the differences in terms of R1 rate in the two groups. Correlation between presence/absence of microscopic residual tumor status and local recurrence was also evaluated. The cohort of 100 patients consisted of 66 pancreatic ductal adenocarcinoma (PDAC) (SG: 35; NSG: 31), 15 distal common bile duct cancer (SG: 9; NSG: 6) and 19 cancer of the ampulla of Vater (SG: 6; NSG: 13). The rate of R1 resections resulted higher in the SG (66% vs 10%, p < 0.05). The rate of local recurrence did not differ in the two groups (NSG 23.4%, SG 27.6%). No relationships were found between R1 status and development of local recurrence in both groups. Local recurrence occurred in 20% of R1-NSG and in 34.3% of R1-SG. Our study showed that the standardized method determines a significant increase of R1 resection if compared with other non-standardized methods. This difference is due to the different definition of minimum clearance (0-mm- vs 1-mm rule). Even if not significantly, the standardized method seems to better discriminate the patients in terms of local recurrence risk after R1 vs R0 in SG (34 vs 11%) in comparison with R1 vs R0 in NSG (20 vs 27%).

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References

  1. Chandrasegaram MD, Goldstein D, Simes J et al (2015) Meta-analysis of radical resection rates and margin assessment in pancreatic cancer. Br J Surg 102:1459–1472

    Article  CAS  PubMed  Google Scholar 

  2. Neoptolemos JP, Stocken DD, Dunn JA, Almond J, Beger HG, Pederzoli P et al (2001) European Study Group for Pancreatic Cancer. Influence of resection margins on survival for patients with pancreatic cancer treated by adjuvant chemoradiation and/or chemotherapy in the ESPAC-1 randomized controlled trial. Ann Surg 234:758–768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Matsuno S, Egawa S, Unno M (2007) R0 resection for ductal pancreatic cancer—Japanese experience. Am J Surg 194:S110–S114

    Article  Google Scholar 

  4. Hruban RH et al (2010) WHO classification of Tumours of Digestive System, Fourth Edition. ISBN-13 9789283224327

  5. Evans DB, Farnell MB et al (2009) Surgical treatment of resectable and borderline resectable pancreas cancer: expert consensus statement. Ann Surg Oncol 16:1736–1744

    Article  PubMed  Google Scholar 

  6. Oettle H, Post S, Neuhaus P, Gellert K, Langrehr J, Ridwelski K, Schramm H, Fahlke J, Zuelke C, Burkart C, Gutberlet K, Kettner E, Schmalenberg H, Weigang-Koehler K, Bechstein WO, Niedergethmann M, Schmidts-Wolf I, Roll L, Doerken B, Riess H (2007) Adjuvant chemotherapy with gemcitabine vs observation in patients undergoing curative-intent resection of pancreatic cancer: a randomized controlled trial. JAMA 297:267–277

    Article  CAS  PubMed  Google Scholar 

  7. Richter A, Niedergethmann M, Sturm JW, Lorenz D, Post S, Trede M (2003) Long-term results of partial pancreaticoduodenectomy for ductal adenocarcinoma of the pancreatic head: 25-year experience. World J Surg 27:324–329

    Article  PubMed  Google Scholar 

  8. Wagner M, Redaelli C, Lietz M, Seiler CA, Friess H, Buchler MW (2004) Curative resection is the single most important factor determining outcome in patients with pancreatic adenocarcinoma. Br J Surg 91:586–594

    Article  CAS  PubMed  Google Scholar 

  9. Hishinuma S, Ogata Y, Tomikawa M, Ozawa I, Hirabayashi K, Igarashi S (2006) Patterns of recurrence after curative resection of pancreatic cancer, based on autopsy findings. J Gastrointest Surg 10:511–518

    Article  PubMed  Google Scholar 

  10. Sperti C, Pasquali C, Piccoli A, Pedrazzoli S (1997) Recurrence after resection for ductal adenocarcinoma of the pancreas. World J Surg 21:195–200

    Article  CAS  PubMed  Google Scholar 

  11. Raut CP, Tseng JF, Sun CC, Wang H, Wolff RA, Crane CH et al (2007) Impact of resection status on pattern of failure and survival after pancreaticoduodenectomy for pancreatic adenocarcinoma. Ann Surg 246:52–60

    Article  PubMed  PubMed Central  Google Scholar 

  12. Butturini G, Stocken DD, Wente MN, Jeekel H, Klinkbijl JHG, Bakkevold K et al (2008) Influence of resection margins and treatment on survival in patients with pancreatic cancer. Meta-analysis of randomized controlled trials. Arch Surg 143:75–83

    Article  PubMed  Google Scholar 

  13. Kayahara M, Nagakawa T, Ueno K, Ohta T, Takeda T, Miyazaki I (1993) An evaluation of radical resection for pancreatic cancer based on the mode of recurrence as determined by autopsy and diagnostic imaging. Cancer 71:2118–2223

    Article  Google Scholar 

  14. Westerdahl J, Andren-Sandberg A, Ihse I (1993) Recurrence of exocrine pancreatic cancer: local or hepatic? Hepatogastroenterology 40:384–387

    CAS  PubMed  Google Scholar 

  15. Butler J, Ahmad S, Katz M, Cioffi J, Zyromski N (2016) A systematic review of the role of periadventitial dissection of the superior mesenteric artery in affecting margin status after pancreaticoduodenectomy for pancreatic adenocarcinoma. HPB 18:305–311

    Article  PubMed  PubMed Central  Google Scholar 

  16. Rau Bettina et al (2012) R1 resection in pancreatic cancer has significant impact on long-term outcome in standardized pathology modified for routine use. Surgery 152(3 Suppl 1):S103–S111

    Article  PubMed  Google Scholar 

  17. Verbeke CS, Leitch D, Menon KV, McMahon MJ, Guillou PJ, Anthoney A (2006) Redefining the R1 resection in pancreatic cancer. Br J Surg 93:1232–1237

    Article  CAS  PubMed  Google Scholar 

  18. Esposito I, Kleef J, Friess H (2007) Surgical treatment of pancreatic cancer. J Am Coll Surg 205:S81–S86

    Google Scholar 

  19. Menon KV, Gomez D, Smith AM, Anthoney A, Verbeke CS (2009) Impact of margin status on survival following pancreaticoduodenectomy for cancer: the Leeds Pathology Protocol (LEEPP). HPB 11:18–24

    Article  PubMed  PubMed Central  Google Scholar 

  20. Michalski CW, Kleff J, Wente MN et al (2007) Systematic review and meta-analysis of standard and extended lymphadenectomy in pancreaticoduodenectomy for pancreatic cancer. Br J Surg 94:265–273

    Article  CAS  PubMed  Google Scholar 

  21. The Royal College of Pathologists (2002) Standards and minimum datasets for reporting cancers. Minimum dataset for the histopathological reporting of pancreatic, ampulla of Vater and bile duct carcinoma. The Royal College of Pathologists, London

    Google Scholar 

  22. Rosai J (2004) Appendix E. Rosai and Ackerman’s surgical pathology, 9th edn. Mosby, Edinburgh, pp 2953–Y2954

    Google Scholar 

  23. Cox DR (1972) Regression models and life-tables. J Roy Stat Soc B 34(2):187–220

    Google Scholar 

  24. Verbeke CS (2008) Resection margins and R1 rates in pancreatic cancer—are we there yet? Histopathology 52:787–796

    Article  CAS  PubMed  Google Scholar 

  25. Liszka L, Pajak J, Zielinska-Pajak E, Golka D, Mrowiec S, Lampe P (2010) Different approaches to assessment of lymph nodes and surgical margin status in patients with ductal adenocarcinoma of the pancreas treated with pancreaticoduodenectomy. Pathology 42:138–146

    Article  PubMed  Google Scholar 

  26. Khalifa MA, Maksymov V, Rowsell CH, Hanna S (2007) A novel approach to the intraoperative assessment of the uncinate margin of the pancreaticoduodenectomy specimen. HPB 9:146–149

    Article  PubMed  PubMed Central  Google Scholar 

  27. Compton CC, Henson DE (1997) Protocol for the examination of specimens removed from patients with carcinoma of the exocrine pancreas; a basis for checklists. Cancer Committee, College of American Pathologists. Arch Pathol Lab Med 121:1129–1136

    CAS  PubMed  Google Scholar 

  28. Luttges J, Vogel I, Menke M, Henne-Bruns D, Kremer B, Kloppel G (1998) The retroperitoneal resection margin and vessel involvement are important factors determining survival after pancreaticoduodenectomy for ductal adenocarcinoma of the head of the pancreas. Virchows Arch 433:237–242

    Article  CAS  PubMed  Google Scholar 

  29. Washington K et al (2013) Protocol for the examination of specimens from patients with carcinoma of the exocrine pancreas. College of American Pathologists. Based on AJCC/UICC  TNM, 7th edition

  30. Campbell Dr F et al (2010) Dataset for the histopathological reporting of carcinomas of the pancreas, ampulla of Vater and common bile duct. The Royal College of Pathologists

  31. Capella et al (2011) Carcinoma of the exocrine pancreas: the histology report. Dig Liver Dis 43S:S282–S292

    Article  Google Scholar 

  32. Verbeke CS, Gladhaug IP (2012) Resection margin involvement and tumour origin in pancreatic head cancer. Br J Surg 99:1036–1049

    Article  CAS  PubMed  Google Scholar 

  33. Verbeke CS, Menon KV (2009) Redefining resection margin status in pancreatic cancer. HPB 11:282–289

    Article  PubMed  PubMed Central  Google Scholar 

  34. Campbell F, Smith RA, Whelan P, Sutton R, Raraty M, Neoptolemos JP et al (2009) Classification of R1 resections for pancreatic cancer: the prognostic relevance of tumour involvement within 1 mm of a resection margin. Histopathology 55:277–283

    Article  PubMed  Google Scholar 

  35. Gaedcke J, Gunawan B, Grade M, Szoke R, Liersch T, Becker H et al (2010) The mesopancreas is the primary site for R1 resection in pancreatic head cancer: relevance for clinical trials. Lagenbecks Arch Surg 395:451–458

    Article  CAS  Google Scholar 

  36. Schlitter AM, Esposito I (2010) Definition of microscopic tumour clearance (R0) in pancreatic cancer resections. Cancers 2:2001–2010

    Article  PubMed  PubMed Central  Google Scholar 

  37. Albores-Saavedra J, Heffess C, Hruban RH, Klimstra D, Longnecker D (1999) Recommendations for the reporting of pancreatic specimens containing malignant tumours. The Association of Directors of Anatomic and Surgical Pathology. Am J Clin Pathol 11:304–307

    Article  Google Scholar 

  38. Chatelain D, Flejou JF (2002) Pancreatectomy for adenocarcinoma: prognostic factors, recommendations for pathological reports. Ann Pathol 22:422–431

    PubMed  Google Scholar 

  39. Hruban RH, Pitman MB, Klimstra DS (2007) Tumors of the pancreas. Atlas of tumor pathology 4th Series, Fascicle 6. Armed Forces Institute of Pathology, Washington

    Google Scholar 

  40. Khalifa MA (2007) Intraoperative assessment of the Whipple resection specimen. J Clin Pathol 60:975–980

    Article  PubMed  PubMed Central  Google Scholar 

  41. Nagtegaal ID, Corrie A, Marijen M, Kranenbarg EK, van de Velde CJH, van Krieken JHJM (2002) Circumferential margin involvement is still an important predictor of local recurrence in rectal carcinoma. Not 1 mm but 2 mm is the limit. Am J Surg Pathol 26:350–357

    Article  PubMed  Google Scholar 

  42. Wibe A, Rendedal PR, Svensson E, Norstein J, Eide TJ, Myrvold HE et al (2002) Prognostic significance of the circumferential resection margin following total mesorectal excision for rectal cancer. Br J Surg 89:327–334

    Article  CAS  PubMed  Google Scholar 

  43. Osipov A, Naziri J, Hendifar A et al (2015) Impact of margin status and lymphadenectomy on clinical outcomes in resected pancreatic adenocarcinoma: implications for adjuvant radiotherapy. J Gastrointest Oncol 7:239–247

    Google Scholar 

  44. Howard TJ, Krug JE, Yu J, Zyromski NJ, Schmidt CM, Jacobson LE et al (2006) A margin negative R0 resection accomplished with minimal postoperative complications is the surgeon’s contribution to longterm survival in pancreatic cancer. J Gastrointest Surg 10:1338–1345

    Article  PubMed  Google Scholar 

  45. Westgard A, Tafjord S, Farstaid IN, Cvancarova M, Eide TJ, Mathisen O et al (2008) Patterns of recurrence after curative resection of pancreatic ductal adenocarcinoma. Eur J Surg Oncol 35:600–604

    Google Scholar 

  46. Ferrone CR, Pieretti-Vanmarcke R, Bloom JP, Zheng H, Szymonifka J, Wargo JA et al (2012) Pancreatic ductal adenocarcinoma: longterm survival does not equal cure. Surgery 152(Suppl.):43–49

    Article  Google Scholar 

  47. Fatima J, Schnelldorfer T, Barton J, Wood CM, Wiste JH, Smryk TC et al (2010) Pancreaticoduodenectomy for ductal adenocarcinoma: implications of positive margin on survival. Arch Surg 145:165–172

    Article  Google Scholar 

  48. Hartwing W, Hackert T, Hinz U, Gluth A, Bergmann F, Strobel O et al (2011) Pancreatic cancer surgery in the new millennium: better prediction of outcome. Ann Surg 254:311–319

    Article  Google Scholar 

  49. Buchler MW, Werner J, Weitz J (2010) R0 in pancreatic cancer: surgery, pathology, biology, or definition matters? Ann Surg 251:1011–1012

    Article  PubMed  Google Scholar 

  50. Jamieson NB, Denley SM, Logue J, MacKenzie DJ, Foulis AK, Dickson EJ et al (2011) A prospective comparison of the prognostic value of tumour and patient-related factors in patients undergoing potentially curative surgery for pancreatic ductal adenocarcinoma. Ann Surg Oncol 18:2318–2328

    Article  PubMed  Google Scholar 

  51. Van der Broeck A, Sergeant G, Ectors N, Van Steenbergen W, Aerts R, Topal B (2009) Patterns of recurrence after curative resection of pancreatic ductal adenocarcinoma. Eur J Surg Oncol 35:600–604

    Article  PubMed  Google Scholar 

  52. Rau BM, Moritz K, Schuschan S, Alsfasser G, Prall F, Klar E (2012) R1 resection in pancreatic cancer has significant impact on longterm outcome in standardized pathology modified for routine use. Surgery 152(Suppl.):103–111

    Article  Google Scholar 

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Coppola, R., Cartillone, M., Borzomati, D. et al. Surgical margins for duodenopancreatectomy. Updates Surg 68, 279–285 (2016). https://doi.org/10.1007/s13304-016-0404-x

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