Preoperative Therapy and Pancreatoduodenectomy for Pancreatic Ductal Adenocarcinoma: a 25-Year Single-Institution Experience

Journal of Gastrointestinal Surgery

Volumn 21, Issue 1, 2017, Pages 164-174

  Cloyd, Jordan M ^a   Katz, Matthew H G ^a   Prakash, Laura ^a   Varadhachary, Gauri R ^a   Wolff, Robert A ^a   Shroff, Rachna T ^a   Javle, Milind ^a   Fogelman, David ^a   Overman, Michael ^a   Crane, Christopher H ^a   Koay, Eugene J ^a   Das, Prajnan ^a   Krishnan, Sunil ^a   Minsky, Bruce D ^a   Lee, Jeffrey H ^a   Bhutani, Manoop S ^a   Weston, Brian ^a   Ross, William ^a   Bhosale, Priya ^a   Tamm, Eric P ^a   Wang, Huamin ^a   Maitra, Anirban ^a   Kim, Michael P ^a   Aloia, Thomas A ^a   Vauthey, Jean Nicholas ^a   Fleming, Jason B ^a   Abbruzzese, James L ^b   Pisters, Peter W T ^c   Evans, Douglas B ^d   Lee, Jeffrey E ^a   more..

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY HEALTH NETWORK   (Canada)

^d MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

Neoadjuvant therapy; Pancreatectomy; Pancreatic ductal adenocarcinoma; Pancreatoduodenectomy

Indexed keywords

ADENOCARCINOMA; ADJUVANT CHEMOTHERAPY; CHEMORADIOTHERAPY; FEMALE; HUMAN; MALE; MIDDLE AGED; NEOADJUVANT THERAPY; PANCREAS CARCINOMA; PANCREAS TUMOR; PANCREATICODUODENECTOMY; PREOPERATIVE CARE; RETROSPECTIVE STUDY; TUMOR RECURRENCE;

ADENOCARCINOMA; CARCINOMA, PANCREATIC DUCTAL; CHEMORADIOTHERAPY; CHEMOTHERAPY, ADJUVANT; FEMALE; HUMANS; MALE; MIDDLE AGED; NEOADJUVANT THERAPY; NEOPLASM RECURRENCE, LOCAL; PANCREATIC NEOPLASMS; PANCREATICODUODENECTOMY; PREOPERATIVE CARE; RETROSPECTIVE STUDIES;

EID: 84992223585     PISSN: 1091255X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11605-016-3265-1     Document Type: Article

References (65)

1. American Cancer Society. Cancer Facts & Figures 2016 [Internet]. Atlanta: Atlanta: American Cancer Society; 2016. Available from: http://www.cancer.org/acs/groups/content/@research/documents/document/acspc-047079.pdf
2. Oettle H, Post S, Neuhaus P, Gellert K, Langrehr J, Ridwelski K, et al. Adjuvant chemotherapy with gemcitabine vs observation in patients undergoing curative-intent resection of pancreatic cancer: a randomized controlled trial. JAMA. 2007;297:267–77.
3. Bilimoria KY, Bentrem DJ, Ko CY, Tomlinson JS, Stewart AK, Winchester DP, et al. Multimodality therapy for pancreatic cancer in the U.S.: utilization, outcomes, and the effect of hospital volume. Cancer. 2007;110:1227–34.
4. Tzeng C-WD, Fleming JB, Lee JE, Xiao L, Pisters PWT, Vauthey J-N, et al. Defined clinical classifications are associated with outcome of patients with anatomically resectable pancreatic adenocarcinoma treated with neoadjuvant therapy. Ann. Surg. Oncol. 2012;19:2045–53.
5. Tzeng C-WD, Tran Cao HS, Lee JE, Pisters PWT, Varadhachary GR, Wolff RA, et al. Treatment sequencing for resectable pancreatic cancer: influence of early metastases and surgical complications on multimodality therapy completion and survival. J. Gastrointest. Surg. Off. J. Soc. Surg. Aliment. Tract. 2014;18:16-24-25.
6. Aloia TA, Aloia TE, Lee JE, Vauthey J-N, Abdalla EK, Wolff RA, et al. Delayed recovery after pancreaticoduodenectomy: a major factor impairing the delivery of adjuvant therapy? J. Am. Coll. Surg. 2007;204:347–55.
7. Fathi A, Christians KK, George B, Ritch PS, Erickson BA, Tolat P, et al. Neoadjuvant therapy for localized pancreatic cancer: guiding principles. J. Gastrointest. Oncol. 2015;6:418–29.
8. Sutton JM, Abbott DE. Neoadjuvant therapy for pancreas cancer: past lessons and future therapies. World J. Gastroenterol. 2014;20:15564–79.
9. Pilepich MV, Miller HH. Preoperative irradiation in carcinoma of the pancreas. Cancer. 1980;46:1945–9.
10. Le Scodan R, Mornex F, Partensky C, Mercier C, Valette P-J, 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;31:545–52.
11. Evans DB, Varadhachary GR, Crane CH, Sun CC, Lee JE, Pisters PWT, et al. Preoperative gemcitabine-based chemoradiation for patients with resectable adenocarcinoma of the pancreatic head. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 2008;26:3496–502.
12. Varadhachary GR, Wolff RA, Crane CH, Sun CC, Lee JE, Pisters PWT, et al. Preoperative gemcitabine and cisplatin followed by gemcitabine-based chemoradiation for resectable adenocarcinoma of the pancreatic head. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 2008;26:3487–95.
13. Turrini O, Ychou M, Moureau-Zabotto L, Rouanet P, Giovannini 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. J. Eur. Soc. Surg. Oncol. Br. Assoc. Surg. Oncol. 2010;36:987–92.
14. Sahora K, Kuehrer I, Eisenhut A, Akan B, Koellblinger C, Goetzinger P, et al. NeoGemOx: Gemcitabine and oxaliplatin as neoadjuvant treatment for locally advanced, nonmetastasized pancreatic cancer. Surgery. 2011;149:311–20.
15. Pipas JM, Zaki BI, McGowan MM, Tsapakos MJ, Ripple GH, Suriawinata AA, et al. Neoadjuvant cetuximab, twice-weekly gemcitabine, and intensity-modulated radiotherapy (IMRT) in patients with pancreatic adenocarcinoma. Ann. Oncol. Off. J. Eur. Soc. Med. Oncol. ESMO. 2012;23:2820–7.
16. Kim EJ, Ben-Josef E, Herman JM, Bekaii-Saab T, Dawson LA, Griffith KA, et al. A multi-institutional phase 2 study of neoadjuvant gemcitabine and oxaliplatin with radiation therapy in patients with pancreatic cancer. Cancer. 2013;119:2692–700.
17. Hwang RF, Wang H, Lara A, Gomez H, Chang T, Sieffert N, et al. Development of an integrated biospecimen bank and multidisciplinary clinical database for pancreatic cancer. Ann. Surg. Oncol. 2008;15:1356–66.
18. Katz MHG, Pisters PWT, Evans DB, Sun CC, Lee JE, Fleming JB, et al. Borderline resectable pancreatic cancer: the importance of this emerging stage of disease. J. Am. Coll. Surg. 2008;206:833-846-848.
19. Varadhachary GR, Tamm EP, Abbruzzese JL, Xiong HQ, Crane CH, Wang H, et al. Borderline resectable pancreatic cancer: definitions, management, and role of preoperative therapy. Ann. Surg. Oncol. 2006;13:1035–46.
20. 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. Chic. Ill 1960. 1992;127:1335–9.
21. 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. Off. J. Am. Soc. Clin. Oncol. 1998;16:3843–50.
22. Pisters PWT, 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. Off. J. Am. Soc. Clin. Oncol. 2002;20:2537–44.
23. Phase II study of preoperation mFOLFIRINOX and chemoradiation for high-risk resectable and borderline resectable pancreatic adenocarcinoma. J. Clin. Oncol. [Internet]. 2015 [cited 2016 Apr 20];Suppl 3. Available from: http://meetinglibrary.asco.org/content/140403-158
24. Katz MG, 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;e161137.
25. Katz MHG, Wang H, Balachandran A, Bhosale P, Crane CH, Wang X, et al. Effect of neoadjuvant chemoradiation and surgical technique on recurrence of localized pancreatic cancer. J. Gastrointest. Surg. Off. J. Soc. Surg. Aliment. Tract. 2012;16:68-78-79.
26. Katz MHG, Lee JE, Pisters PWT, Skoracki R, Tamm E, Fleming JB. Retroperitoneal Dissection in Patients with Borderline Resectable Pancreatic Cancer: Operative Principles and Techniques. J. Am. Coll. Surg. 2012;215:e11–8.
27. Liu L, Katz MH, Lee SM, Fischer LK, Prakash L, Parker N, et al. Superior Mesenteric Artery Margin of Posttherapy Pancreaticoduodenectomy and Prognosis in Patients With Pancreatic Ductal Adenocarcinoma. Am. J. Surg. Pathol. 2015;39:1395–403.
28. Chatterjee D, Katz MH, Rashid A, Varadhachary GR, Wolff RA, Wang H, et al. Histologic grading of the extent of residual carcinoma following neoadjuvant chemoradiation in pancreatic ductal adenocarcinoma: a predictor for patient outcome. Cancer. 2012;118:3182–90.
29. Tzeng C-WD, Abbott DE, Cantor SB, Fleming JB, Lee JE, Pisters PWT, et al. Frequency and intensity of postoperative surveillance after curative treatment of pancreatic cancer: a cost-effectiveness analysis. Ann. Surg. Oncol. 2013;20:2197–203.
30. Tzeng C-WD, Fleming JB, Lee JE, Wang X, Pisters PWT, Vauthey J-N, et al. Yield of clinical and radiographic surveillance in patients with resected pancreatic adenocarcinoma following multimodal therapy. HPB. 2012;14:365–72.
31. Bakkevold KE, Arnesjø B, Dahl O, Kambestad B. Adjuvant combination chemotherapy (AMF) following radical resection of carcinoma of the pancreas and papilla of Vater--results of a controlled, prospective, randomised multicentre study. Eur. J. Cancer Oxf. Engl. 1990. 1993;29A:698–703.
32. Kosuge T, Kiuchi T, Mukai K, Kakizoe T, Japanese Study Group of Adjuvant Therapy for Pancreatic Cancer (JSAP). A multicenter randomized controlled trial to evaluate the effect of adjuvant cisplatin and 5-fluorouracil therapy after curative resection in cases of pancreatic cancer. Jpn. J. Clin. Oncol. 2006;36:159–65.
33. Burris HA, Moore MJ, Andersen J, Green MR, Rothenberg ML, Modiano MR, et al. Improvements in survival and clinical benefit with gemcitabine as first-line therapy for patients with advanced pancreas cancer: a randomized trial. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 1997;15:2403–13.
34. Conroy T, Desseigne F, Ychou M, Bouché O, Guimbaud R, Bécouarn Y, et al. FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer. N. Engl. J. Med. 2011;364:1817–25.
35. Von Hoff DD, Ervin T, Arena FP, Chiorean EG, Infante J, Moore M, et al. Increased survival in pancreatic cancer with nab-paclitaxel plus gemcitabine. N. Engl. J. Med. 2013;369:1691–703.
36. Ferrone CR, Marchegiani G, Hong TS, Ryan DP, Deshpande V, McDonnell EI, et al. Radiological and surgical implications of neoadjuvant treatment with FOLFIRINOX for locally advanced and borderline resectable pancreatic cancer. Ann. Surg. 2015;261:12–7.
37. Nanda RH, El-Rayes B, Maithel SK, Landry J. Neoadjuvant modified FOLFIRINOX and chemoradiation therapy for locally advanced pancreatic cancer improves resectability. J. Surg. Oncol. 2015;111:1028–34.
38. Blazer M, Wu C, Goldberg RM, Phillips G, Schmidt C, Muscarella P, et al. Neoadjuvant modified (m) FOLFIRINOX for locally advanced unresectable (LAPC) and borderline resectable (BRPC) adenocarcinoma of the pancreas. Ann. Surg. Oncol. 2015;22:1153–9.
39. Petrelli F, Coinu A, Borgonovo K, Cabiddu M, Ghilardi M, Lonati V, et al. FOLFIRINOX-based neoadjuvant therapy in borderline resectable or unresectable pancreatic cancer: a meta-analytical review of published studies. Pancreas. 2015;44:515–21.
40. Improving resection rates in borderline resectable pancreatic cancer: Pilot study shows favorable results [Internet]. The Bulletin. [cited 2015 Oct 25]. Available from: http://bulletin.facs.org/2015/10/improving-resection-rates-in-borderline-resectable-pancreatic-cancer-pilot-study-shows-favorable-results/
41. Verbeke CS, Gladhaug IP. Resection margin involvement and tumour origin in pancreatic head cancer. Br. J. Surg. 2012;99:1036–49.
42. Iacobuzio-Donahue CA, Fu B, Yachida S, Luo M, Abe H, Henderson CM, et al. DPC4 gene status of the primary carcinoma correlates with patterns of failure in patients with pancreatic cancer. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 2009;27:1806–13.
43. Cloyd JM, Crane CH, Koay EJ, Das P, Krishnan S, Prakash L, et al. Impact of hypofractionated and standard fractionated chemoradiation before pancreatoduodenectomy for pancreatic ductal adenocarcinoma. Cancer. 2016;122(17):2671–9.
44. Katz MHG, Fleming JB, Pisters PWT, 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;248:1098–102.
45. Tseng JF, Raut CP, Lee JE, Pisters PWT, Vauthey J-N, Abdalla EK, et al. Pancreaticoduodenectomy with vascular resection: margin status and survival duration. J. Gastrointest. Surg. Off. J. Soc. Surg. Aliment. Tract. 2004;8:935-949-950.
46. Cameron JL, He J. Two thousand consecutive pancreaticoduodenectomies. J. Am. Coll. Surg. 2015;220:530–6.
47. Serrano PE, Cleary SP, Dhani N, Kim PTW, Greig PD, Leung K, et al. Improved long-term outcomes after resection of pancreatic adenocarcinoma: a comparison between two time periods. Ann. Surg. Oncol. 2015;22:1160–7.
48. Yeo CJ, Cameron JL, Lillemoe KD, Sitzmann JV, Hruban RH, Goodman SN, et al. Pancreaticoduodenectomy for cancer of the head of the pancreas. 201 patients. Ann. Surg. 1995;221:721-731-733.
49. Winter JM, Brennan MF, Tang LH, D’Angelica MI, Dematteo RP, Fong Y, et al. Survival after resection of pancreatic adenocarcinoma: results from a single institution over three decades. Ann. Surg. Oncol. 2012;19:169–75.
50. Salem AI, Alfi M, Winslow E, Cho CS, Weber SM. Has survival following pancreaticoduodenectomy for pancreas adenocarcinoma improved over time? J. Surg. Oncol. 2015;112:643–9.
51. Millikan KW, Deziel DJ, Silverstein JC, Kanjo TM, Christein JD, Doolas A, et al. Prognostic factors associated with resectable adenocarcinoma of the head of the pancreas. Am. Surg. 1999;65:618-623-624.
52. Lewis R, Drebin JA, Callery MP, Fraker D, Kent TS, Gates J, et al. A contemporary analysis of survival for resected pancreatic ductal adenocarcinoma. HPB. 2013;15:49–60.
53. Raigani S, Ammori J, Kim J, Hardacre JM. Trends in the treatment of resectable pancreatic adenocarcinoma. J. Gastrointest. Surg. Off. J. Soc. Surg. Aliment. Tract. 2014;18:113–23.
54. Evans DB, George B, Tsai S. Non-metastatic Pancreatic Cancer: Resectable, Borderline Resectable, and Locally Advanced-Definitions of Increasing Importance for the Optimal Delivery of Multimodality Therapy. Ann. Surg. Oncol. 2015;22:3409–13.
55. Tzeng C-WD, Balachandran A, Ahmad M, Lee JE, Krishnan S, Wang H, et al. Serum carbohydrate antigen 19-9 represents a marker of response to neoadjuvant therapy in patients with borderline resectable pancreatic cancer. HPB. 2014;16:430–8.
56. Katz MHG, Varadhachary GR, Fleming JB, Wolff RA, Lee JE, Pisters PWT, et al. Serum CA 19-9 as a marker of resectability and survival in patients with potentially resectable pancreatic cancer treated with neoadjuvant chemoradiation. Ann. Surg. Oncol. 2010;17:1794–801.
57. Mavros MN, Xu L, Maqsood H, Gani F, Ejaz A, Spolverato G, et al. Perioperative Blood Transfusion and the Prognosis of Pancreatic Cancer Surgery: Systematic Review and Meta-analysis. Ann. Surg. Oncol. 2015;
58. Kantor O, Talamonti MS, Stocker SJ, Wang C-H, Winchester DJ, Bentrem DJ, et al. A Graded Evaluation of Outcomes Following Pancreaticoduodenectomy with Major Vascular Resection in Pancreatic Cancer. J. Gastrointest. Surg. Off. J. Soc. Surg. Aliment. Tract. 2015;
59. Winter JM, Cameron JL, Campbell KA, Arnold MA, Chang DC, Coleman J, et al. 1423 pancreaticoduodenectomies for pancreatic cancer: A single-institution experience. J. Gastrointest. Surg. Off. J. Soc. Surg. Aliment. Tract. 2006;10:1199-1210-1211.
60. Konstantinidis IT, Warshaw AL, Allen JN, Blaszkowsky LS, Castillo CF-D, 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;257:731–6.
61. Chatterjee D, Katz MH, Rashid A, Wang H, Iuga AC, Varadhachary GR, et al. Perineural and intraneural invasion in posttherapy pancreaticoduodenectomy specimens predicts poor prognosis in patients with pancreatic ductal adenocarcinoma. Am. J. Surg. Pathol. 2012;36:409–17.
62. Weber CE, Bock EA, Hurtuk MG, Abood GJ, Pickleman J, Shoup M, et al. Clinical and pathologic features influencing survival in patients undergoing pancreaticoduodenectomy for pancreatic adenocarcinoma. J. Gastrointest. Surg. Off. J. Soc. Surg. Aliment. Tract. 2014;18:340–7.
63. Riediger H, Keck T, Wellner U, zur Hausen A, Adam U, Hopt UT, et al. The lymph node ratio is the strongest prognostic factor after resection of pancreatic cancer. J. Gastrointest. Surg. Off. J. Soc. Surg. Aliment. Tract. 2009;13:1337–44.
64. Fischer LK, Katz MH, Lee SM, Liu L, Wang H, Varadhachary GR, et al. The number and ratio of positive lymph nodes affect pancreatic cancer patient survival after neoadjuvant therapy and pancreaticoduodenectomy. Histopathology. 2015;
65. Roland CL, Katz MHG, Tzeng C-WD, Lin H, Varadhachary GR, Shroff R, et al. The Addition of Postoperative Chemotherapy is Associated with Improved Survival in Patients with Pancreatic Cancer Treated with Preoperative Therapy. Ann. Surg. Oncol. 2015;