Meta-analysis of radical resection rates and margin assessment in pancreatic cancer

British Journal of Surgery

Volumn 102, Issue 12, 2015, Pages 1459-1472

  Chandrasegaram, M D ^a,i,j   Goldstein, D ^b   Simes, J ^a   Gebski, V ^a   Kench, J G ^c,h   Gill, A J ^d   Samra, J S ^e,h   Merrett, N D ^f,j   Richardson, A J ^g,h   Barbour, A P ^k   Fawcett, J ^k   Grimison, P S ^a   Christophi, C ^l   Padbury, R ^m   Haghighi, K S ⁿ   Chen, J W ^m   Nikfarjam, M ^l   O'Rourke, N ^o   Spry, N ^p  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c ROYAL PRINCE ALFRED HOSPITAL   (Australia)

^d UNIVERSITY OF SYDNEY   (Australia)

^e ROYAL NORTH SHORE HOSPITAL   (Australia)

^f UNIVERSITY OF WESTERN SYDNEY   (Australia)

^g WESTMEAD HOSPITAL   (Australia)

^h UNIVERSITY OF SYDNEY   (Australia)

ⁱ UNIVERSITY OF ADELAIDE   (Australia)

^j THE PRINCE CHARLES HOSPITAL   (Australia)

^k UNIVERSITY OF QUEENSLAND   (Australia)

^l UNIVERSITY OF MELBOURNE   (Australia)

^m FLINDERS MEDICAL CENTRE   (Australia)

ⁿ PRINCE OF WALES HOSPITAL   (Australia)

^o ROYAL BRISBANE AND WOMEN'S HOSPITAL   (Australia)

^p UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

more..

Author keywords

[No Author keywords available]

Indexed keywords

EPIDEMIOLOGY; HEALTH; HUMAN; INCIDENCE; META ANALYSIS; PANCREAS RESECTION; PANCREATIC NEOPLASMS; PROCEDURES; PROGNOSIS; TUMOR RECURRENCE;

GLOBAL HEALTH; HUMANS; INCIDENCE; NEOPLASM RECURRENCE, LOCAL; PANCREATECTOMY; PANCREATIC NEOPLASMS; PROGNOSIS;

EID: 84944097183     PISSN: 00071323     EISSN: 13652168     Source Type: Journal    
DOI: 10.1002/bjs.9892     Document Type: Review

References (70)

1. Butturini G, Stocken DD, Wente MN, Jeekel H, Klinkenbijl JH, Bakkevold KE, et al. Influence of resection margins and treatment on survival in patients with pancreatic cancer: metaanalysis of randomized controlled trials. Arch Surg 2008; 143: 75-83.
2. Speer AG, Thursfield VJ, Torn-Broers Y, Jefford M,. Pancreatic cancer: surgical management and outcomes after 6 years of follow-up. Med J Aust 2012; 196: 511-515.
3. Sharp L, Carsin AE, Cronin-Fenton DP, O'Driscoll D, Comber H,. Is there under-treatment of pancreatic cancer? Evidence from a population-based study in Ireland. Eur J Cancer 2009; 45: 1450-1459.
4. Verbeke CS, Leitch D, Menon KV, McMahon MJ, Guillou PJ, Anthoney A,. Redefining the R1 resection in pancreatic cancer. Br J Surg 2006; 93: 1232-1237.
5. Esposito I, Kleef J, Bergmann F, Reiser C, Herpel E, Friess H, et al. Most pancreatic resections are R1 resections. Ann Surg Oncol 2008; 15: 1651-1660.
6. Campbell F, Smith RA, Whelan P, Sutton R, Raraty M, Neoptolemos JP, 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: 277-283.
7. Büchler MW, Werner J, Weitz J,. R0 in pancreatic cancer surgery: surgery, pathology, biology, or definition matters? Ann Surg 2010; 251: 1011-1012.
8. Hartwig W, Hackert T, Hinz U, Gluth A, Bergmann F, Strobel O, et al. Pancreatic cancer surgery in the new millennium: better prediction of outcome. Ann Surg 2011; 254: 311-319.
9. Royal College of Pathologists of Australasia (RCPA). Cancer of the Exocrine Pancreas, Ampulla of Vater and Distal Common Bile Duct. Structured Reporting Protocol, 1st Edition 2014. https://www.rcpa.edu.au/getattachment/3b6a41df-939d-492e-bc6b-35fc264bd89b/Protocol-pancreatic-cancer.aspx [accessed 2 July 2015 ].
10. Bockhorn M, Uzunoglu FG, Adham M, Imrie C, Milicevic M, Sandberg AA, et al. Borderline resectable pancreatic cancer: a consensus statement by the International Study Group of Pancreatic Surgery (ISGPS). Surgery 2014; 155: 977-988.
11. Jamieson NB, Foulis AK, Oien KA, Going JJ, Glen P, Dickson EJ, et al. Positive mobilization margins alone do not influence survival following pancreatico-duodenectomy for pancreatic ductal adenocarcinoma. Ann Surg 2010; 251: 1003-1010.
12. Gebauer F, Tachezy M, Vashist YK, Marx AH, Yekebas E, Izbicki JR, et al. Resection margin clearance in pancreatic cancer after implementation of the Leeds Pathology Protocol (LEEPP): clinically relevant or just academic? World J Surg 2015; 39: 493-499.
13. Verbeke CS,. Resection margins and R1 rates in pancreatic cancer-are we there yet? Histopathology 2008; 52: 787-796.
14. Moher D, Liberati A, Tetzlaff J, Altmann DG,. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol 2009; 62: 1006-1012.
15. Verbeke CS,. Resection margins in pancreatic cancer. Surg Clin N Am 2013; 93: 647-662.
16. StatsDirect. StatsDirect version 3. http://www.statsdirect.com [accessed 24 June 2015 ].
17. Higgins JP, Thompson SG, Deeks JJ, Altman DG,. Measuring inconsistency in meta-analyses. BMJ 2003; 327: 557-560.
18. Egger M, Davey Smith G, Schneider M, Minder C,. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997; 315: 629-634.
19. Delpero JR, Bachellier P, Regenet N, Le Treut YP, Paye F, Carrere N, et al. Pancreaticoduodenectomy for pancreatic ductal adenocarcinoma: a French multicentre prospective evaluation of resection margins in 150 evaluable specimens. HPB (Oxford) 2014; 16: 20-33.
20. Jamieson NB, Chan NIJ, Foulis AK, Dickson EJ, McKay CJ, Carter CR,. The prognostic influence of resection margin clearance following pancreaticoduodenectomy for pancreatic ductal adenocarcinoma. J Gastrointest Surg 2013; 17: 511-521.
21. John BJ, Naik P, Ironside A, Davidson BR, Fusai G, Gillmore R, et al. Redefining the R1 resection for pancreatic ductal adenocarcinoma: tumour lymph nodal burden and lymph node ratio are the only prognostic factors associated with survival. HPB (Oxford) 2013; 15: 674-680.
22. Menon KV, Gomez D, Smith AM, Anthoney A, Verbeke CS,. Impact of margin status on survival following pancreatoduodenectomy for cancer: the Leeds Pathology Protocol (LEEPP). HPB (Oxford) 2009; 11: 18-24.
23. Chang DK, Johns AL, Merrett ND, Gill AJ, Colvin EK, Scarlett CJ, et al. Margin clearance and outcome in resected pancreatic cancer. J Clin Oncol 2009; 27: 2855-2863.
24. Gnerlich JL, Luka SR, Deshpande AD, Dubray BJ, Weir JS, Carpenter DH, et al. Microscopic margins and patterns of treatment failure in resected pancreatic adenocarcinoma. Arch Surg 2012; 147: 753-760.
25. Konstantinidis IT, Warshaw AL, Allen JN, Blaszkowsky LS, Castillo CF, Deshpande V, et al. Pancreatic ductal adenocarcinoma: is there a survival difference for R1 resections versus locally advanced unresectable tumors? What is a 'true' R0 resection? Ann Surg 2013; 257: 731-736.
26. Pang TC, Wilson O, Argueta MA, Hugh TJ, Chou A, Samra JS, et al. Frozen section of the pancreatic neck margin in pancreatoduodenectomy for pancreatic adenocarcinoma is of limited utility. Pathology 2014; 46: 188-192.
27. Sugiura T, Uesaka K, Mihara K, Sasaki K, Kanemoto H, Mizuno T, et al. Margin status, recurrence pattern, and prognosis after resection of pancreatic cancer. Surgery 2013; 154: 1078-1086.
28. Westgaard A, Tafjord S, Farstad IN, Cvancarova M, Eide TJ, Mathisen O, et al. Resectable adenocarcinomas in the pancreatic head: the retroperitoneal resection margin is an independent prognostic factor. BMC Cancer 2008; 8: 5.
29. Howard TJ, Krug JE, Yu J, Zyromski NJ, Schmidt CM, Jacobson LE, et al. A margin-negative R0 resection accomplished with minimal postoperative complications is the surgeon's contribution to long-term survival in pancreatic cancer. J Gastrointest Surg 2006; 10: 1338-1345.
30. Kimbrough CW, St Hill CR, Martin RCG, McMasters KM, Scoggins CR,. Tumor-positive resection margins reflect an aggressive tumor biology in pancreatic cancer. J Surg Oncol 2013; 107: 602-607.
31. Mathur A, Ross SB, Luberice K, Kurian T, Vice M, Toomey P, et al. Margin status impacts survival after pancreaticoduodenectomy but negative margins should not be pursued. Am Surg 2014; 80: 353-360.
32. Raut CP, Tseng JF, Sun CC, Wang H, Wolff RA, Crane CH, et al. Impact of resection status on pattern of failure and survival after pancreaticoduodenectomy for pancreatic adenocarcinoma. Ann Surg 2007; 246: 52-60.
33. Rau BM, Moritz K, Schuschan S, Alsfasser G, Prall F, Klar E,. R1 resection in pancreatic cancer has significant impact on long-term outcome in standardized pathology modified for routine use. Surgery 2012; 152: S103-S111.
34. Campbell F, Bennett M, Foulis AJ,. Minimum Dataset for Histopathological Reporting of Pancreatic, Ampulla of Vater and Bile Duct Carcinoma. Royal College of Pathologists: London, 2002.
35. Gill AJ, Johns AL, Eckstein R, Samra JS, Kaufman A, Chang DK, et al. Synoptic reporting improves histopathological assessment of pancreatic resection speciments. Pathology 2008; 6: 1-7.
36. Staley CA, Cleary KR, Abbruzzese JL, Lee JE, Ames FC, Fenoglio CJ, et al. The need for standardised pathologic staging of pancreaticoduodenectomy specimens. Pancreas 1996; 12: 373-380.
37. Japan Pancreas Society (ed.) General Rules for the Study of Pancreatic Cancer (2nd edn). Kanehara: Tokyo, 2003.
38. Greene FI, Page DL, Fleming ID, (eds). Exocrine pancreas. In AJCC Cancer Staging Manuel (6th edn). Springer: New York, 2002; 157-164.
39. Washington K, Berlin J, Branton P, Burgart LJ, Carter DK, Fitzgibbons P, et al.; College of American Pathologists. Protocol for the Examination of Specimens from Patients with Carcinoma of the Exocrine Pancreas; 2013. http://www.cap.org/ShowProperty?nodePath=/UCMCon/Contribution%20Folders/WebContent/pdf/pancreasexo-13protocol-3201.pdf [accessed 2 July 2015].
40. Sobin L., International Union Against Cancer: TNM Classification of Malignant Tumours. Wiley-Liss: New York, 1997.
41. Noto M, Miwa K, Kitagawa H, Kayahara M, Takamura H, Shimizu K, et al. Pancreas head carcinoma: frequency of invasion to soft tissue adherent to the superior mesenteric artery. Am J Surg Pathol 2005; 29: 1056-1061.
42. Kooby DA, Lad NL, Squires MH III, Maithel SK, Sarmiento JM, Staley CA, et al. Value of intraoperative neck margin analysis during Whipple for pancreatic adenocarcinoma. A multicenter analysis of 1399 patients. Ann Surg 2014; 260: 494-501.
43. Hernandez J, Mullinax J, Clark W, Toomey P, Villadolid D, Morton C, et al. Survival after pancreaticoduodenectomy is not improved by extending resections to achieve negative margins. Ann Surg 2009; 250: 76-80.
44. Khalifa MA, Maksymov V, Rowsell C,. Retroperitoneal margin of the pancreaticoduodenectomy specimen: anatomic mapping for the surgical pathologist. Virchows Arch 2009; 454: 125-131.
45. Neoptolemos JP, Stocken DD, Dunn JA, Almond J, Beger HG, Pederzoli P, et al. 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 2001; 234: 758-768.
46. Hishinuma S, Ogata Y, Tomikawa M, Ozawa I, Hirabayashi K, Igarashi S,. Patterns of recurrence after curative resection of pancreatic cancer, based on autopsy findings. J Gastrointest Surg 2006; 10: 511-518.
47. Feakins R, Campbell F, Verbeke CS,. Survey of UK histopathologists' approach to the reporting of resection specimens for carcinomas of the pancreatic head. J Clin Pathol 2013; 66: 715-717.
48. Verbeke CS, Gladhaug IP,. Resection margin involvement and tumour origin in pancreatic head cancer. Br J Surg 2012; 99: 1036-1049.
49. Schlitter AM, Esposito I,. Definition of microscopic tumour clearance (R0) in pancreatic cancer resections. Cancers (Basel) 2010; 2: 2001-2010.
50. Bandyopadhyay S, Basturk O, Coban I, Thirabanjasak D, Liang H, Altinel D, et al. Isolated solitary ducts (naked ducts) in adipose tissue: a specific but underappreciated finding of pancreatic adenocarcinoma and one of the potential reasons of understaging and high recurrence rate. Am J Surg Pathol 2009; 33: 425-429.
51. Evans DB, Farnell MB, Lillemoe KD, Vollmer C Jr, Strasberg SM, Schulick RD,. Surgical treatment of resectable and borderline resectable pancreas cancer: expert consensus statement. Ann Surg Oncol 2009; 16: 1736-1744.
52. Evans DB, Rich TA, Byrd DR, Cleary KR, Connelly JH, Levin B, et al. Preoperative chemoradiation and pancreaticoduodenectomy for adenocarcinoma of the pancreas. Arch Surg 1992; 127: 1335-1339.
53. Pisters PW, Abbruzzese JL, Janjan NA, Cleary KR, Charnsangavej C, Goswitz MS, et al. Rapid-fractionation preoperative chemoradiation, pancreaticoduodenectomy, and intraoperative radiation therapy for resectable pancreatic adenocarcinoma. J Clin Oncol 1998; 12: 3843-3850.
54. Hoffman JP, Lipsitz S, Pisansky T, Weese JL, Solin L, Benson AB III,. Phase II trial of preoperative radiation therapy and chemotherapy for patients with localized, resectable adenocarcinoma of the pancreas: an Eastern Cooperative Oncology Group Study. J Clin Oncol 1998; 16: 317-323.
55. White RR, Hurwitz HI, Morse MA, Lee C, Anscher MS, Paulson EK, et al. Neoadjuvant chemoradiation for localized adenocarcinoma of the pancreas. Ann Surg Oncol 2001; 8: 758-765.
56. Pisters PW, Wolff RA, Janjan NA, Cleary KR, Charnsangavej C, Crane CN, et al. Preoperative paclitaxel and concurrent rapid-fractionation radiation for resectable pancreatic adenocarcinoma: toxicities, histologic response rates and event-free outcome. J Clin Oncol 2002; 20: 2537-2544.
57. Calvo FA, Matute R, Garcia-Sabrido JL, Gomez-Espi M, Martinez NE, Lozano MA, et al. Neoadjuvant chemoradiation with tegafur in cancer of the pancreas: initial analysis of clinical tolerance and outcome. Am J Clin Oncol 2004; 27: 343-349.
58. Talamonti MS, Small W Jr, Mulcahy MF, Wayne JD, Attaluri V, Colletti LM, et al. A multi-institutional phase II trial of preoperative full-dose gemcitabine and concurrent radiation for patients with potentially resectable pancreatic carcinoma. Ann Surg Oncol 2005; 13: 150-158.
59. Le Scodan R, Mornex F, Partensky C, Mercier C, Valette PJ, Ychou M, et al. Histopathological response to preoperative chemoradiation for resectable pancreatic adenocarcinoma: the French Phase II FFCD 9704-SFRO Trial. Am J Clin Oncol 2008; 31: 545-552.
60. Evans DB, Varadhachary GR, Crane CH, Sun CC, Lee JE, Pisters PW, et al. Pre-operative gemcitabine-based chemoradiation for patients with resectable adenocarcinoma of the pancreatic head. J Clin Oncol 2008; 26: 3496-3502.
61. Varadhachary GR, Wolff RA, Crane CH, Sun CC, Lee JE, Pisters PW, et al. Preoperative gemcitabine and cisplatin followed by gemcitabine-based chemoradiation for resectable adenocarcinoma of the pancreatic head. J Clin Oncol 2008; 26: 3487-3495.
62. Turrini O, Viret F, Moureau-Zabotto L, Guiramand J, Moutardier V, Lelong B, et al. Neoadjuvant 5 fluorouracil-cisplatin chemoradiation effect on survival in patients with resectable pancreatic head adenocarcinoma: a ten-year single institution experience. Oncology 2009; 76: 413-419.
63. Turrini O, Ychou M, Moureau-Zabotto L, Rouanet P, Giovanni M, Moutardier V, et al. Neoadjuvant docetaxel-based chemoradiation for resectable adenocarcinoma of the pancreas: new neoadjuvant regimen was safe and provided an interesting pathologic response. Eur J Surg Oncol 2010; 36: 987-992.
64. Takahashi H, Ohigashi H, Gotoh K, Marubashi S, Yamada T, Murata M, et al. Preoperative gemcitabine-based chemoradiation therapy for resectable and borderline resectable pancreatic cancer. Ann Surg 2013; 258: 1040-1050.
65. Palmer DH, Stocken DD, Hewitt H, Markham CE, Hassan B, Johnson PJ, et al. A randomized phase 2 trial of neoadjuvant chemotherapy in resectable pancreatic cancer: gemcitabine alone versus gemcitabine combined with cisplatin. Ann Surg Oncol 2007; 14: 2088-2096.
66. Heinrich S, Pestalozzi BC, Schafer M, Weber A, Bauerfeind P, Knuth A, et al. Prospective phase II trial of neoadjuvant chemotherapy with gemcitabine and cisplatin for resectable adenocarcinoma of the pancreatic head. J Clin Oncol 2008; 26: 2526-2531.
67. Greene FL,. TNM staging for malignancies of the digestive tract: 2003 changes and beyond. Semin Surg Oncol 2003; 21: 23-29.
68. Sobin LH, Wittekind C, (eds). TNM Classification of Malignant Tumours (6th edn). Wiley-Liss: New York, 2002.
69. O'Reilly EM, Perelshteyn A, Jarnagin WR, Schattner M, Gerdes H, Capanu M, et al. A single-arm, nonrandomised phase II trial of neoadjuvant gemcitabine and oxaliplatin in patients with resectable pancreas adenocarcinoma. Ann Surg 2014; 260: 142-148.
70. Barbour N, O'Rourke N, Samra JS, Haghighi KS, Kench J, Mitchell J, et al. A multicenter, phase II trial of preoperative gemcitabine and nab-paclitaxel for resectable pancreas cancer: the AGITG GAP study. J Clin Oncol 2015; 33 (Suppl 3); abstract 387.